Jdpjournalfall2006

Volume 1

Vol. 1 Fall 2006

ISBN number: 0-9767758-4-0

The Journal of Developmental Processes

Sponsored by the Interdisciplinary Council on Developmental and Learning Disorders (ICDL), the Council of Human Development, and the Milton and Ethel Harris Research Initiative www.icdl.com www.councilhd.ca www.mehri.ca

Fall 2006

The Journal of Developmental Processes

Journal of Developmental Processes Submission Guidelines Description The goal of the Journal of Developmental Processes is to provide a vehicle for research and clinical studies that advance knowledge of the complexity inherent in all developmental processes. The JDP encourages exchange of ideas across fields including, but not limited to, animal behavior, anthropology, biology, education, linguistics, neuroscience, occupational and speech and language therapy, primatology, psychiatry, psychology, public policy, sociology, and social work.

The Journal is interested in both experimental and descriptive studies, including basic research, detailed case reports, ethnographic analysis, and theoretical explorations.

Particularly welcome are innovative conceptual frameworks and methods that capture the complexity of developmental processes as well as assessment procedures and interventions that enable children and families to overcome mental health, developmental, social, and learning challenges.

Submissions Send queries and submissions on clinical aspects and applications to Associate Editor Ira Glovinsky at ira1834@sbcglobal.net; all other queries and submissions, and books for potential review, should go to Editor Barbara J. King at bjking@wm.edu or Department of Anthropology, College of William and Mary, Williamsburg, VA, USA, 23187-8795.

Please submit manuscripts electronically, preferably in Microsoft Word® format.

Length is negotiable with the editor, but generally should not exceed 50 manuscript pages, including references. Submit your contact information, including phone, fax, and postal mailing address. Also enclose a cover letter indicating that the article has not been published, and is not under consideration elsewhere.

Tables, figures, and photographs should be used sparingly. Please include a high gloss black-and-white copy of the image as well as an electronic file in TIFF, EPS, or JPG format. Clearly indicate where the image should appear, as well as a title and explanatory note. Line art should have a resolution of 1200 dots per inch for good print quality.

References References should be listed in alphabetical order. Each listed reference should be cited in the text, and each text citation should be listed in the References. We follow the APA style, e.g., Greenspan, S. I., & Shanker, S. G. (2004). The first idea: How symbols, language, and intelligence evolved from our primate ancestors to modern humans. Cambridge, MA: Da Capo.

Greenspan, S. I., & Shanker, S. G. (2005). Developmental Research. In E. S. Person, A. M. Cooper, & G. O. Gabbard, American psychiatric publishing textbook of psychoanalysis (pp. 335–360). Washington, DC: American Psychiatric Publishing.

Greenspan, S. I., & Wieder, S. (1997). Developmental patterns and outcomes in infant and children with disorders in relating and communicating: A chart review of 200 cases of children with autistic spectrum diagnosis. Journal of Developmental and Learning Disorders, 1, 87–141.

To purchase a copy of the Journal of Developmental Processes or to subscribe to future issues, please visit www.icdl.com or call 301-656-2667 for information

THE JOURNAL OF DEVELOPMENTAL PROCESSES

Volume 1

2006

CONTENTS

Introductory Notes—Stanley I. Greenspan

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A Welcome, and an Invitation, from the Editor—Barbara J. King

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Dynamic Systems Research on Interindividual Communication: The Transformation of Meaning-Making—Alan Fogel

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Early Family Trauma and the Ontogeny of Glucocorticoid Stress Response in the Human Child: Grandmother as a Secure Base— Mark V. Flinn and David V. Leone

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The Development of Spontaneous Gestures in Zoo-living Gorillas and Sign-taught Gorillas: From Action and Location to Object Representation—Joanne E. Tanner, Francine G. Patterson, and Richard W. Byrne

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The Kids Are Alright: Maternal Behavioral Interactions and Stress Reactivity in Infants of Differentially Reared Rhesus Monkeys— Peter G. Roma, Angela M. Ruggiero, Melanie L. Schwandt, J. Dee Higley, and Stephen J. Suomi

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The Literacy of Interaction: Are Infants and Young Children Receiving a “Mental Diet” Conducive for Future Learning?—Pnina S. Klein

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Toward a Behavior of Reciprocity—Morton Ann Gernsbacher

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Book Review: Parenting for Primates—Barbara J. King

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Bethesda, Maryland

Copyright © 2006

The Journal of Developmental Processes Editor in Chief Stanley I. Greenspan Chair, Interdisciplinary Council for Developmental and Learning Disorders Departments of Psychiatry, Behavioral Sciences, and Pediatrics George Washington University Medical School Washington, DC, USA Editor Barbara J. King Department of Anthropology College of William and Mary Williamsburg, Virginia, USA bjking@wm.edu

Associate Editor Ira Glovinsky The Interdisciplinary Center for the Family West Bloomfield, Michigan, USA ira1834@sbcglobal.net Administrative Editor Jane Mild LaRoque Lexington, Massachusetts, USA jmlaroque@rcn.com Editorial Assistant Meghan Habas Siudzinski College of William and Mary Williamsburg, Virginia, USA megsudz@gmail.com

Associate Editor in Chief Serena Wieder Interdisciplinary Council on Developmental and Learning Disorders Bethesda, Maryland, USA JDP Editorial Board Margaret Bauman The Ladders Program Harvard University Wellesley, Massachusetts, USA

Robert Lickliter Department of Psychology Florida International University Miami, Florida, USA

Leon Cytryn Departments of Psychiatry, Behavioral Sciences, and Pediatrics George Washington University Washington, DC, USA

Pedro Reygadas Department of Social Sciences and Humanities Autonomous University of San Luis Potosi San Luis Potosi, Mexico

Alan Fogel Department of Psychology University of Utah Salt Lake City, Utah, USA Gil Foley Department of Psychology Ferkauf Graduate School Yeshiva University Bronx, New York, USA Sima Gerber Department of Linguistics and Communication Disorders Queens College, CUNY Flushing, New York, USA Morton Ann Gernsbacher Department of Psychology University of Wisconsin-Madison Madison, Wisconsin, USA Barbara Kalmanson Clinical Psychologist San Francisco, California, USA Pnina Klein School of Education Bar-Ilan University Ramat-Gan, Israel Marc Lewis Department of Human Development and Applied Psychology University of Toronto Canada

Ricki G. Robinson Descanso Medical Center for Development & Learning University of Southern California La Canada, California, USA Rebecca Shahmoon Shanok Jewish Board of Family Services Child Development Center New York, New York, USA Stuart Shanker Distinguished Research Professor of Philosophy and Psychology Director, the Milton and Ethel Harris Research Initiative York University Toronto, Ontario, Canada Barbara Smuts Department of Psychology University of Michigan Ann Arbor, Michigan, USA Richard Solomon Ann Arbor Center for Developmental and Behavioral Pediatrics Ann Arbor, Michigan, USA Christina Toren Department of Anthropology University of St. Andrews St. Andrews, Scotland Ann Turnbull Beach Center on Disability The University of Kansas Lawrence, Kansas, USA

The Journal gratefully acknowledges the financial support of the Milton and Ethel Harris Research Initiative (MEHRI), York University, Toronto, Canada. For more information, please see www.MEHRI.ca

Introductory Notes Stanley I. Greenspan, MD Editor in Chief Interdisciplinary Council for Developmental Learning Disorders Department of Psychiatry, Behavioral Sciences, and Pediatrics George Washington University Medical School Washington, DC

The Journal of Developmental and Learning Disorders has expanded its focus and become the Journal of Developmental Processes (JDP). The Editor, Barbara J. King, Professor of Anthropology at The College of William and Mary, embodies the spirit of the Journal in her own outstanding work, and beautifully describes it in the editorial that follows. The expanded editorial board and sponsoring organizations—the Council of Human Development, the Milton and Ethel Harris Research Initiative, in addition to the Interdisciplinary Council on Developmental and Learning Disorders— reflect the broad focus of the Journal. As will readily be seen, the JDP includes all the disciplines that contribute to our understanding of human development, the factors that influence it, the mechanisms through which they work, and the enormous variations observed throughout the course of life. The Journal embraces clinical studies and case descriptions in keeping with the traditions established by its predecessor, the Journal of Developmental and Learning Disorders. It also, however, focuses on a broad range of studies and narratives that are necessary for a full understanding of developmental processes. I want to welcome you to our new Journal and hope that you will not only enjoy reading it, but will also become part of the growing group of colleagues that are actively contributing to our understanding of the full complexity of human experience.

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A Welcome, and an Invitation, from the Editor Barbara J. King, Editor Department of Anthropology College of William and Mary bjking@wm.edu

Capturing the continuous processes of change inherent in development, those stemming from “all the delicate, transparent webs from which we have woven ourselves,”1 is a wondrous challenge for 21st century scientists. In the case of human development, it is a challenge for clinicians and educators as well.

As 21st century science becomes increasingly high-tech, we may take approaches to the study of development using complex population statistics, gene maps, neurochemistry profiles, and MRI images. These avenues of research have much to teach us, but are not enough in themselves. Living, breathing, ever-changing flesh-andblood individuals belong front and center in our research in all their beautiful or distressing deviation from “the norm,” whatever that may be. When we work to understand how infants, juveniles, and subadults—in humans and other animals—come to communicate, learn, and negotiate the rules of the social systems in which they live, we learn a great deal by going beyond the statistically significant patterns in our data to embrace all the ways of being, becoming, and behaving that we can identify.

To recognize and describe change as it occurs is critical, because change is always occurring even as we study the organisms before us. The situation is not a dichotomous one, with normative versus non-normative development as two mutually exclusive pathways available for our scrutiny. An understanding of developmental systems allows us to see that stresses of some sort will always impact individuals. When dealing with human development, an important goal is to determine when and how best to intervene in order to help children (and adults) who are struggling because of the stresses of their own unique developmental profiles. The trick, both for clinical professionals who may step in directly and for academics who may provide information in aid of this intervention, is to identify the differences that make a difference (apologies to anthropologist Gregory Bateson for my mangling of the letter, but I think not the spirit, of his famous phrase).

In short, scientists, clinicians, educators, and others who study aspects of development may embrace an array of exciting options. We can seek to discover precisely how mammalian/primate/human nurturing interactions that surround the genes affect developmental outcomes; how emotions are created by, and in turn help create, the processes of the brain; and how the social, cultural, and indeed global interdependencies that make up our world affect all living creatures in it.

1. David Grossman, Be My Knife (New York: Farrar, Straus, and Giroux, 1998), p. 69.

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The central mission of the Journal of Developmental Processes is to reflect, and to foster, these nuanced and diverse responses to the challenges of studying development. The JDP wishes to publish a wide variety of theories and methods, more powerful in the collective than in the singular, that are sensitive to the dynamic processes of development.

The JDP aims to be interdisciplinary and international, but this is only a first step.

The ways in which we intend to make a distinctive contribution are reflected in our mission statement. We welcome qualitative research reports as much as we do quantitative ones, and indeed hope to publish many examples where qualitative and quantitative approaches reinforce each other. Case studies, generated by both academic and clinical research or reflection, will be a key part of the journal’s content, as will theoretically innovative articles and book essays. In short, the JDP is open to new, comprehensive approaches to development in a number of formats.

The six articles and single book essay in this inaugural issue reflect the principles I have just described. Psychologist Alan Fogel leads off with a compelling and provocative discussion of methodologies for studying how systems change over time, not only in frequencies, durations, and sequential patterns, but also in meaning. Anthropologists Mark V. Flinn and David V. Leone report results from field research on the island of Dominica that elegantly brings together behavioral and hormonal assessment of children’s stress responses. Primate researchers Joanne E. Tanner, Francine G. Patterson, and Richard W. Byrne compare the development of gesturing in zoo-living and sign-taught gorillas, with insightful analysis of the influence of a highly social process that they call action-mapping.

Flinn and Leone’s theme of stress as measured hormonally and behaviorally is echoed in a second article from primate studies, written by Peter G. Roma, Angela M. Ruggerio, Melanie L. Schwandt, J. Dee Higley, and Stephen J. Suomi. Intriguingly, and surprisingly, this research team found that, in a colony of rhesus monkeys, mothers’ rearing condition did not affect infant stress responses.

The final two articles return us to the realm of human behavioral development.

Pnina S. Klein describes a developmental mediation approach available to parents and educators to aid children’s learning; she identifies several significant ways in which this approach differs from existing early intervention projects in many parts of the world. Focusing on autism, Morton S. Gernsbacher writes about reciprocity, offering incisive remarks about the far-reaching effects that professionals, peers, and parents may see when they are encouraged to act reciprocally with autistic children. Finally, rounding out the first issue and revisiting once more a broad primate level of development, I discuss the strengths and weaknesses of Harriet Smith’s book Parenting for Primates.

As this summary indicates, JDP’s first issue is diverse, and no single journal issue could hope to be fully comprehensive on development. Yet more needs to be done. All but two of the authors, one in Scotland and and another in Israel, work in North America. I want to publish the best work on development from Latin America, Asia, Africa, and the Pacific as well. Results on nonhuman primates are well-represented, but there’s room in these pages too for birds, cetaceans, dogs, elephants, rodents, and any other species studied developmentally. Finally, I aim for broader representation of aca-

A Welcome, and an Invitation, from the Editor

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demic and clinical fields and subfields, in terms of articles, book essays, and names to broaden our pool of peer readers who may advise the editorial board on submitted manuscripts.

Please consider this editorial an invitation to contact me with your ideas for articles, nominations, including self-nominations, for experts to join our reviewing pool, and any suggestions and questions that might be appropriate as JDP undergoes the early days of its own developmental process.

In closing, I would like to thank Stanley Greenspan, MD, and Serena Wieder, PhD, (Associate Editor in Chief), whose vision is responsible for creating the JDP. I would also like to thank Serena for her work on the clinical articles. The three of us, in turn, acknowledge the skilled work of Jane Mild LaRoque, Sharon Markus, and Meghan Habas Siudzinski. Grateful appreciation is offered to our sponsoring organizations: the Interdisciplinary Council on Developmental and Learning Disorders, the Council of Human Development, and the Milton and Ethel Harris Research Initiative.

Dynamic Systems Research on Interindividual Communication: The Transformation of Meaning-Making Alan Fogel Department of Psychology University of Utah alan.fogel@psych.utah.edu

Abstract: This paper presents a dynamic systems methodology for the study of interindividual communication in social systems. Since dynamic social systems are fluid, changing, emergent, developing, and yield created information in a meaning-making process, it follows that dynamic systems research best serves scientific discovery by substantiating these same processes in the method. The dynamic systems methods presented here place the scientist in the system, not knowing the answer, but working through a dynamic process of engagement with the system, toward an emergent understanding of the patterns of communication and their changes over time with respect to the limitations of the observer’s method and point of view.

Introduction Dynamic systems theory addresses the problem of describing the ways in which complex systems change over time. The focus of this paper is to highlight the unique conceptual and research issues that arise when change in social communication systems is the topic of investigation. Specifically, in addition to quantitative indices of change in frequencies, durations, and sequential patterning of communicative behavior, research on communication can also encompass the meaning in the system. Meaning, similar to any other pattern formation process in a dynamic system, can be thought of as emerging and stabilizing dynamically through a process of self-organization. This paper presents a research model that includes both developmental changes in quantity and in meaning. These terms are defined and the methods are explained and illustrated in a lengthy research example.

The study of change is paradoxical. The phenomenon that one wishes to observe in one moment is no longer the same in the next moment. Yet, as human observers, we are capable of perceiving and describing when behavior at two or more moments in time appears to be the “same” or “different” (Popper, 1968). This is particularly relevant to the problem of studying communication because meaning can be defined as

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the perception of a “difference” between two or more communicative actions. But the meaning of the perceived difference can only become manifest in the changing actions or interpretations of participants in a communication process. Meaning-making is thus part of the way in which human observers interpret some complex series of changes as “having” a pattern, structure, or order. Any time an observer declares the presence of a pattern, in other words, the observer becomes a part of the dynamic system being observed. The stars in a galaxy do not in fact have, own, or possess a pattern. The pattern (the galaxy) emerges in the relationship of the stars to the observer.

The study of complex dynamic systems takes as a premise that individual components and constituents are best understood as part of a collective in which each affects the others to create pattern and order at the level of the collective, an order which may not be obvious at the level of the behavior of each of the constituents. This paper takes the perspective that the study of dynamic systems involves one additional constituent to any collective that is being observed: the observer’s point of view. The observer, in other words, is part of the description or model of the system. Although complex systems exist in the absence of the observer, the patterns and processes that are described, counted, and analyzed emerge from the relationship between the observer and the system. This point refers to the role of scientists on systems in which they are not participants. Should they be participants, their behavior and presence becoming part of the system, in addition to their point of view contributing to how that system comes to be understood by others?

The pattern, furthermore, emerges over some finite period of time. One looks at the world and patterns seem to appear instantaneously. There is, however, at least some period of microseconds required for the brain and sense organs to organize the perceptual flow into a flower, tree, or galaxy. Even that relatively rapid emergent process, however, is founded upon an earlier, and considerably longer, period of engagement in that person’s life, a period in which patterns were not apparent and needed days, weeks, or months to be discovered through some process of engagement with the world. The pattern coalesces and stabilizes into a consistent attractor in the brain-behavior-sensory system, making the recognition of the pattern on future occasions more rapid and efficient (Lewis, 1995; 2005; Thelen & Smith, 1994).

This longer process of meaning-making could, of course, be applied to an infant or child who must discover through perception and action, or “re-create,” the meanings of words and gestures via a process of co-regulation with adults (Fogel, 1993; King, 2004). In this paper, however, we apply the same notion to the scientist. Faced with a complex system whose patterns do not easily appear to the observer, patterns may—through a process of prolonged engagement, discovery, and meaning-making— finally emerge.

It is not the intention here to review the growing literature on dynamic systems research and theory. Where needed, the principles of dynamic systems theory are briefly mentioned. The central theme of dynamic systems theory is to understand how the patterning of the collective is related to the co-regulation between the constituents. In the view of dynamic systems theory, the constituents of a system act together to constrain the multiple actions of other constituents so that the complex system organizes and reorganizes over time into a series of semi-stable patterns of behavior called attractors

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(Kelso, 1995; Kugler, Kelso, & Turvey, 1982; Prigogine & Stengers, 1984). Constituents, in other words, change each other in the process of convergence toward an attractor. Two people in a long-term partnership change each other in the process of forming a “couple” with recognizable patterns and habits.

Each time an attractor is re-constituted, the actions within the attractor, the microlevel activity of the system, are somewhat different from the previous occurrence of that same attractor. The concept of dynamic stability replaces the concept of structure, habit, and association in traditional theories of behavior regularities (Capra, 1996; Fogel, 1993; Thelen & Smith, 1994). The attractor occurs at an organizational, collective, or macrolevel of activity, in which the observer’s perception of “sameness” becomes possible.

In the behavioral sciences, complex systems occur for intraindividual, interindividual, ecological, and sociocultural relationships. The intraindividual system involves relationships between the various systems of the body and mind, such as between genes and their cellular environment, between brain and behavior, between muscles that act together to perform an action, or between emotion and intellect. The interindividual system involves social relationships such as between parent-child, close companions, teacher-student, supervisor-employee, therapist-client, romantic partners, and business partners. The ecological system includes relationships between humans and their physical and biological environment such as our relationships with the plants, animals, and the earth. The sociocultural system contains all the relationships within and between groups of people with intersecting histories; it takes in relations of international peace or conflict, systems of kinship and religion, of politics and economics, institutions of education or medical care, systems of government and law.

The Paradox of Change and the Role of the Observer Attractor patterns may become salient to observers in each of these systems. Any type of stable behavior pattern in the intraindividual system, such as walking or smiling, involves microlevel co-activity between muscular, skeletal, neurological, endocrine, and immune systems of the body. Greetings, leave-takings, topics of conversation, and the like are seen as stable attractors in the interindividual system. Taking a pet dog for a walk, or creating artificial ladders for migrating salmon to traverse dams and other human structures on their way upstream, are examples of attractors in the ecological system. Treaties, laws, elections, and classrooms are attractors in a sociocultural system. In these examples, attractors are perceived when patterns of linkage between microlevel constituents recur with regularity and with relatively little variability.

In interindividual communication, for example, people can easily perceive and label the attractor called “greeting” at the macrolevel, even though there are many different types of greetings (formal or informal, distant or intimate, face-to-face, or through some electronic medium). These different types of greetings all show differences in the microlevel of activity within the perceived “sameness” of the attractor pattern. Even within the same interindividual relationship over time, every face-toface greeting is somewhat different in the microlevel pattern of activity. The same pair

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of romantic partners, for example, sometimes kisses, sometimes hugs, sometimes nods, or does some combination of these and other actions. In sum, • Dynamic systems are always changing.

• Patterns of stability can be perceived from the flow of change.

• “Change” and “stability” are emergent from the engagement of the observer with the system.

• Science is the pattern of meanings that are made from the observer-world system.

This brief discussion highlights a series of methodological dilemmas that a scientist/ observer faces when attempting to understand and study changing dynamic systems.

• Is it possible for scientific meanings to transcend the particularities of how, when, and by whom something is observed?

• Is it possible to capture and analyze a phenomenon that is always changing, that is, is there any such thing as a “phenomenon” to be studied?

These questions may seem to be best left to philosophers rather than to scientists.

Shouldn’t scientists stick to being concrete and practical? Perhaps a scientist may wish for such simplicity. After all, if people can perceive attractors readily, then it should be a relatively easy task for a scientist to make recordings of all instances of greeting patterns in a particular sample of humans or other animals, measure and count how long that pattern lasts, how may times it occurs, under what circumstances it appears, and when it is it likely to change. The scientist can also count the timing, duration, and number of particular actions within the pattern, at the microlevel (the kisses, hugs, nods, etc.). These can be counted separately for each partner, and statistical and simulation models can be used to verify the recurring stable patterns at the macrolevel.

The danger, however, is that this method runs the risk of freezing the phenomenon, that is, of forgetting—after all is counted and analyzed—that patterns like greetings are sustained by a dynamic process.

The main thesis of this paper is that macroscopic order in dynamic systems emerges in the developing relationship between the constituents of the system and in the developing relationship between the observer and the system. Without taking account of these evolving relationships, quantification can lead to reductionism. Quantifying may lose the evolving process for the sake of trying to capture it. And when this has been done, and the paper published in a respectable quantitative empirical scientific journal, the scientist/observer has in fact affected the reader’s understanding of the system by this mode of action on the system, which in the end, is the observer’s choice and a point of view (Toren, 1996).

The result is analogous to trying to understand quantum mechanics by using Newtonian classical mechanics. Quantum mechanics, as a theory of the subatomic world, cannot serve as a theory of the macroscopic world of behavior. There is, however, an analogy between Heisenberg’s uncertainty principle, and other “strange” quantum phenomena, and the behavioral science of dynamic systems. By ignoring the role of the observer, and by trying to impose the observer’s (unacknowledged) perception of stability, we prematurely reify something that is inherently dynamic (because it is always changing).

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Quantification per se, however, is not inherently concretizing and reifying if the observer recognizes that measurement is simply one way of engaging in a scientific relationship with a dynamic system. In this case, reduction to a quantity may be a useful scientific tool so long as this act is placed in the context of other convergent acts of meaning-making by the scientist. The dynamics of behavior, like the subatomic realm, is a strange world that shifts in the way it appears depending upon our point of view. Behavior is not an “it” or a “thing.” Behavior constitutes itself in the very process of forming, acting, changing, and disappearing (Fogel, 1993; Morris, 2004).

Scientific language can literally create a world. To use the scientific term, the noun “behavior” can easily create the illusion that there is a “thingness” to behavior, a substance, and a permanence.

The process of engagement with the written word in a scientific document is also emergent and dynamic. A sociocultural landscape of mutual linguistic understanding emerges (in the time frame of microseconds) when the reader engages with the text.

Behavior is created as a dynamic moment of shared meaning. There is a further choice, however, taken by either the writer or the reader, to assume that what appears in this dynamic moment of shared understanding is therefore substantial and concrete.

This turn toward reification is likely to better reflect the stance and judgment of the observer than the changing and dynamic reality of the system being observed.

This is not a discussion of the fictitious and imaginary, as if the noun were something like “hobbit.” Behavior constitutes a domain we can call “reality,” so long as we understand “reality” to be dynamically constituted, as alive and changing, and as different with respect to the point of view of the observer. This observation has the potential to be profoundly disturbing. On the one hand, few could deny that behavior is dynamically constituted, alive and changing, and that different people describe and interpret it in different ways. On the other hand, few people are likely to explicitly recognize or accept that, therefore, behavior, while real, is not a concrete thing at all.

In English, the verb to know generally leads to the formation of a concrete, factual body of knowledge. The verb to understand, however, refers to an open-ended, experiential, emotional process of knowing that usually occurs between people as they engage over time in close interindividual relationships. To understand in English is equivalent to conocer (Spanish), conòscere (Italian), connaître (French), and conhecer (Portuguese). The corresponding words for concrete knowing in these four languages are saber, sapere, savoir, and saber. Research on the dynamics of meaning-making admits to an inability to know completely (since behavior is changing in the very act of observing and conceptualizing), and instead seeks to engage in a long-term process that may lead to understanding.

The idea that one can have complete knowledge comes from ancient Greek thinking which became the foundation of Western science, what Levinas (1969) calls “totalizing.” Philosophers of intersubjectivity (Buber, 1958; Jopling, 1993; Levinas, 1969), however, point out interindividual communication reflects what Levinas calls “infinitizing,” meaning that we can never completely know another person or completely describe behavior. In an infinitizing stance toward the other, there is no sense of being directed or evaluated; only a feeling of union. One feels connected to the other and meets the other without reserve and in the fullness of the other’s vulnerability to be

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changed. Buber (1958) called these types of relationships “I-Thou” as opposed to the totalizing stance of “I-It” relationships.

Scientists who take as the starting point the slipperiness and ineffability of the very dynamics that they wish to study may aspire to shed light on the underlying dynamics of behavior. No previous reification of behavior dynamics has succeeded in helping us understand why some people contract deadly diseases, why war and violence continue to flare in an enlightened global society, or why poverty and hunger are globally pervasive. Perhaps the answers lie in a dynamic understanding of how these problems develop over time. Perhaps there are no concrete answers, but rather a process of learning how to understand and work with our unimaginably complex universe.

The Conceptualization of Change in Dynamic Systems Theory In the end, the scientist/observer concerned with illuminating and respecting the inherent dynamics of the system is compelled to shift away from a study of structure to a study of process (Capra, 1996). One way out of the dilemma of conceptualizing behavior as a thing is to replace the noun with a verb, “behaving.” Whether noun or verb, naming may eventually lead to reification. Shifting to a verb, however, can be a useful linguistic trope to remind us that the nature of systems is change, and that stability is in the eye of the beholder. Reading and studying dynamic systems requires an active, inquisitive, and critical meta-awareness that the linguistic and mathematical devices of science serve only as signifiers for that which cannot be completely signified. This paper is meant to be read with that type of meta-awareness.

The admonition that “the map is not the territory,” does not quite fit here since the territory is typically seen as fixed. But territory changes with earthquakes, storms and floods. A more radical shift (change) in the scientific stance is called for: from thingsin-themselves to transformations. Territory implies space and boundaries. Transformations imply time and change. As a prelude to the description of research methodology, in the following section, three levels of change are discussed. These are derived from research using the techniques to be presented in this paper.

Sequence vs. Process at the Microlevel (Level 1 Change) Change at the microlevel involves a shift from one to another behavior within an attractor. In mother-infant face-to-face play, for example, there is an iterative cycling in both mother and infant of smiling and not smiling, mutual gaze and gaze elsewhere, and other body movements and facial expressions typical of this type of play. Changes occur as the dyad shifts from one to another mutual action. Each instance of this attractor that recurs over days or weeks also has a similar pattern of activity, yet it is changed from the previous instance of this attractor. These microlevel changes are referred to as Level 1 change, or ordinary variability within a stable attractor (Fogel, Garvey, Hsu, & West-Stroming, 2006a).

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Virtually all studies of microlevel change in the behavioral sciences reduce the flow over time to a probabilistic sequence. Sequences have the form of A → B → C. This scheme can become very complex, as when the behavior of multiple interacting partners is tracked simultaneously. In this case, the behavior of each partner can be observed to precede, follow, or be simultaneous with the other. A wide variety of statistical and simulation models exists to conceptualize and analyze these sequences for regularly recurring patterns. These tools have continued to become more mathematically sophisticated, capable of describing complex lead-lag relationships, timing factors in interaction, and other quantitative indices of social engagement and sensitivity (cf. Jaffe, Beebe, Feldstein, Crown, & Jasnow, 2001; Lewis, Lamey, & Douglas, 1999; Ryan, Gottman, Murray, Carrère, & Swanson, 2000; van Geert, 1998).

The use of any of these tools, however, can imply a reification of change is a linear sequence. This is because, once coded and statistically analyzed, significant probabilities capture attention. The underlying dynamics are messier and less easy to understand and remember. But if behavior at any level of description is always changing, and if those changes occur in the process of forming the relationships that ultimately constitute the perceived attractor, then models of sequence, however, sophisticated, may miss the very dynamics they presume to describe.

In research by the author and his colleagues, we have reported sequential data of the following sort: Infant smiles are more likely occur during maternal smiles; infant smiling tends to follow maternal smiling up until 4 months, after which infants begin to smile in anticipation of the mother’s smile; infant smiles are more likely to occur in particular contexts and not others (e.g., in the climax rather than the setup of a peek-a-boo game) (Fogel, Nelson-Goens, Hsu, & Shapiro, 2000; Messinger, Fogel, & Dickson, 2001). On the other hand, we have published qualitative research on mother-infant smiling that shows how highly variable such sequences can be. Not only that, facial forms of smiling, barely noticeable differences in the “intonation” of the expression but meaningful to the participants, reflect the playfulness and creativity of the underlying dynamics (Fogel, Nwokah, & Karns, 1993; Pantoja, Nelson-Goens, & Fogel, 2001). Neither of these descriptions is the “right” or “correct” one. Rather, they reflect different points of view of the observers and different processes of engagement with the data: one more quantitative and the other more qualitative.

Our research attests that process is much more dynamic and more difficult to describe than structure. No behavior emerges fully formed from the brain without being subject to conditions in the periphery of the body and in the local environment in the very act of formation (Thelen & Smith, 1994). Words, gestures, and expressions can be altered in their shape, intonation, size, explicitness, duration, clarity, force, and on many other dimensions depending upon the ongoing and simultaneous flow of communicative actions. This is the so-called continuous process model of communication, which is contrasted with a discrete state model of communication that is based on sequence rather than process (Fogel, 1993; King, 2004; Shanker & King, 2002).

These co-dynamics cannot always be modeled as a linear sequence. This is because, in some cases, communication functions via information (i.e., meaning-making) rather than by a computation of physical or temporal parameters (Pattee, 1987). Facial expressions, for example, dynamically alter the behavior of social partners. A tiny

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facial movement requiring little energy can induce large expenditures of movement energy in the social partner, as when a smile elicits a partner’s heart rate change and initiates movements of approach. Intracellular communication via the different sequences of bases in DNA and neural communication via different neurotransmitters are other examples of informational dynamic systems (Capra, 1996; Oyama, 1985; Pattee, 1987).

This information approach has an emphasis on the mutuality between constituents which change as they enter into relational processes, altering their identities in order to establish the ground for a relationship. A facial expression, such as a smile, does not contain discrete information about the smiler. Rather, the meaning of the smile depends upon the relationship between the smiler and the partner. People do not typically smile unless the partner is perceived as receptive to opening that line of emotional communication.

In digital and electronic systems, information is usually thought of as discrete bits having a concrete value (either “on” or “off” in a binary system typical of most computers). A dynamic system, however, requires a completely different conceptualization of information that is not fixed in advance and not “transmitted.” Rather, information is created in the process of communication and is always dynamically related to the current state of the entire developing system (Fogel, 1993; Oyama, 1985). In other words, meaning making is the outcome of a finite process of engagement.

In another example, long-term social partners develop between them informational attractors involving unique patterns of speech and expression not shared outside the relationship. Words and gestures of endearment for a romantic couple (sweetie, lover, honey, etc.) mean (are informed by) the entire history of their communication, recreating particular feelings and perhaps further states of intimacy. Yet, words and gestures are not fixed in form and usage. “Honey” can be spoken with love, anger, or impatience depending dynamically on the situation. “Honey,” while meaningful to the partners, does not always mean the same thing because the information is created in the moment of dynamically unfolding feelings and actions.

Sequence vs. Process at the Macrolevel (Level 2 Change) Attractors at the macrolevel grow out of these co-dynamics at the microlevel and reflect qualitatively different modes of system organization (Kelso, 2000). Furthermore, one of the tenets of dynamic systems theory is that out of ordinary variability (Level 1 change), there sometimes arise changes that are more salient, different, or innovative (Level 2 change). Changes at Level 2 are innovations, perceived as different from the ordinary variability of Level 1 change. Innovations are changes that play a different role in the complex system than ordinary variability. They may precipitate a change from one attractor to another, or even a developmental change (Level 3 change, see below) in the entire system of attractors (Fogel et al., 2006a; Thelen & Smith, 1994).

No simple numerical index can fully describe the transition from one attractor to another. The collective behavior of the states of H2O (i.e., ice, water, and steam) differ in quality. Ice has crystals and water does not. Water and steam have dynamic flow patterns and stable ice does not. Although the different states can be represented by a quantitative parameter, temperature or energy, this parameter does not in any way de-

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scribe the complex dynamics at the micro- and macrolevels that constitute the different states and the ways in which one state changes into another.

From a quantitative perspective, when a dynamic system is in a stable attractor, it is in an energetically conservative mode where it maintains its stability. In order to change from one attractor to another, for the system to re-organize, energy is required to move the system from this stable state. As water is heated, for example, there is an increasing disorganization of the water’s movements, a relatively chaotic state. At some point, however, boiling water begins to form rolling patterns, a Level 2 change, that more efficiently move the heat energy from the bottom of the vessel to the surface of the water where it can convert to steam. The water finds a new pattern of selforganization that most effectively dissipates the heat energy. In this kind of dissipative system, new patterns of order—attractors—emerge as systems seek to conserve and release energy in far from equilibrium states (Capra, 1996).

Because the ordinary variability (Level 1 change) of the microlevel system within an attractor is dynamically changing in realtime, an innovation (Level 2 change) is a “change in the pattern of change.” In informational terms, systems make transitions when the change in the pattern of change is noticeable, that is, the change becomes informative or meaningful to the constituents (Pattee, 1987). Information about system change does not exist prior to the change, but rather is created in the moment when a system “notices” a difference, what has been described in informational terms as “a difference that makes a difference” (Bateson, 1975; Oyama, 1985).

Couples in a romantic courtship or dating relationship, for example, may maintain a dynamically stable ordinary variability without any talk of a more serious commitment. When such talk begins—about exclusivity or about marriage—it makes a very big difference for the conduct of the ongoing ordinary variability. This innovation is most likely to be germinated in the ordinary variability of the courtship relationship, as partners may seek to make long-term meaning out of everyday exchanges. The system begins to shift toward another kind of talk about that longer term commitment.

Once that new kind of talk is established, it becomes a new kind of ordinary variability from which further innovations can be launched.

Sequence vs. Process in Developmental Change (Level 3 Change) Developmental change is yet another level of the change process in social and behavioral systems, designated as Level 3 (Fogel et al., 2006a). At any given time, a social behavioral system has a finite number of different attractors, such as different types of play in the parent-child relationship. In development, the entire system of attractors— the collective behavior of the system as a whole—changes. Developmental change is the creation of new attractor patterns and the loss of others. Development is the destabilization, re-organization, and re-stabilization of the collective system of historical attractors (Fogel, 1993; Fogel et al., 2006a; Lewis, 1995; Thelen & Smith, 1994).

Another basic tenet of dynamic systems theory is that changes at the developmental level grow out of changes at the micro- and macrolevels that occur through variations and innovations. Some of these variations may increase the level of energy or informational variability beyond the boundaries of the existing attractors. These innovative

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variations often occur spontaneously, such that development emerges from the activity of the system itself (Fogel et al., 2006a; Thelen & Smith, 1994; van Geert, 1998). Dynamic systems, in other words, are historical. The available set of attractors serves as resources for the system to create opportunities for developmental change. The same idea is contained in Piaget’s (1954) thinking: that some chance discovery may eventually change the existing system of schemes via assimilation and accommodation.

The problem of the emergence of new forms is at the very core of developmental inquiry. How does something new emerge from something that has been there in relatively stable form? Dynamic systems theory recognizes the emergence of innovation or novelty as a fundamental feature of complex systems. Non-biological systems, such as chemical reactions and the physical universe, develop over time because novel variability provokes the system into new stable attractors that are neither planned nor preprogrammed (Laszlo, 2001; Prigogine & Stengers, 1984; Weimer, 1987). A growing number of thinkers have embraced the idea that spontaneous emergence is at the heart of behavioral and psychological change. In the behavioral sciences, this concept has also been called discovery, creativity, construction of novelty, and transformation (Carvalho & Pedrosa, 1998; Eckerman, 1993; Fogel, 1993; Gottlieb, 1992; 2003; Lewis, 1995; Lock, 1980, 2000; Lyra, 1998; Mahoney & Moes, 1997; Nelson, 1997; Overton, 2002; Schore, 2003; Stern, 1998; Thelen & Smith, 1994; Tronick, 1998; Valsiner, 1997; 2001).

The indeterminacy in dynamic systems can produce historically unique trajectories that partly account for the formation of individual differences (Fogel, 1990; Fogel & Branco, 1997; Fogel, Lyra, & Valsiner, 1997; van Geert, 1997; Kellert, 1993; Thelen, 1990; Valsiner, 1997). Informational approaches to dynamic systems perspectives can help us understand why historical changes in people, groups, or societies can never exactly repeat, why every social system is unique, and why these differences are contingent on the dynamics of the communication process and not always amenable to prediction (Fogel, Lyra, & Valsiner, 1997; Gould, 1977).

Dynamic Systems Methods for the Study of System Change The focus of dynamic systems theory is change. Research questions about change dynamics can be formulated at all three levels of change. For any level, one can ask: How does change occur? What mechanisms produce change? What conditions are likely to promote the emergence of change? These questions may be cast in terms of basic or applied research. Basic research might seek to uncover the processes of change in naturally occurring social systems. Applied research—as in international policy, therapeutic intervention, or education—may seek to uncover the basic principles of change in order to promote desired changes in a system and avoid undesired changes.

Questions may be framed about the stability vs. instability of new attractor patterns that emerge as a consequence of a naturally occurring or induced change process. Educationally or therapeutically induced changes that do not last are less desirable than ones that can be sustained over time. Research can seek to uncover the processes that create lasting change as well as the processes that maintain systems in desirable states.

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Does the emergence of new behavior patterns tend to suppress the old patterns or to coexist with them? If a person is relieved of a phobic disorder or alcoholism through therapy, is that phobia still lurking somewhere, ready to be reactivated under particular environmental conditions? When a peace between warring nations is negotiated, under what conditions will that peace last, and is there any likelihood that old hostilities will re-appear?

Microgenetic Research Designs The hallmark of dynamic systems research is the study of change while it is occurring, instead of merely comparing “before” and “after” observations. The primary tool for doing change research from a dynamic systems perspective is the microgenetic research design (Fogel et al., 2006a; Lavelli, Pantoja, Hsu, Messinger, & Fogel, 2005; Siegler, 1996). Microgenetic research designs are specifically intended to allow the researcher to closely observe processes of change, instead of products or outcomes. Typically, some period is selected in which the system is expected to undergo a Level 2 or Level 3 change. Then observations are made on particular cases relatively frequently before, during, and after the change in order to observe the relevant Level 1 changes that may contribute to the Level 2 or 3 change (see Figure 1).

Regardless of the researchers’ theoretical perspectives and the developmental domains under investigation, microgenetic designs are defined by the following key characteristics: • Cases (particular systems of interest) are observed through a period of developmental change.

• Observations are conducted before, during, and after a period during which rapid change in a particular domain occurs. That is, observation is not simply con-

t

T

t = observation interval T = developmental interval t < < T

FIGURE 1.

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ducted before and after the change takes place. The change may be a spontaneous developmental change or it may be a planned intervention.

• There is an elevated density of observations within the transition period. That is, observations are conducted at time intervals that are considerably shorter than the time intervals required for the developmental change to occur. For instance, if a developmental change takes place over several months, then observations should be conducted weekly or even more frequently.

• Observed behaviors are intensively analyzed, both qualitatively and quantitatively, with the goal of identifying the historical processes that give rise to the developmental change.

The unit of analysis is one of the types of systems described earlier: intraindividual, interindividual, ecological, and sociocultural. In the interindividual system, for example, as an individual develops, its relation to the external world changes, such that its effective environment—the actual physical, biological, and social factors with which it interacts—also changes. One of the challenges of systems research is to interpret the concept of environment in such a way that it incorporates an appropriately dynamic view of the changing relations between the developing individual and his or her context. This requires observation across representative developmental contexts to identify the range of behavioral capacities and developmental trends characteristic of the organism-environment system.

Microgenetic research has the advantage of being able to trace the historical development of change over time within the same system. The historical approach has been applied using microgenetic research designs (Bruner, 1983; Fogel, 1990; Fogel et al., 2006a; Granott & Parziale, 2002; Greenspan, 1997; King, 2004; Lavelli et al., 2005; Overton, 2002; Rosenwald & Ochberg, 1992; Shanker & King, 2002; Siegler & Crowley, 1991; Thelen & Smith, 1994; van Geert, 1998). These studies involve both quantitative tracking of developmental trajectories and qualitative analysis of life history narratives that reveal developmental shifts in shared information relative to new behavior coordinations in interindividual systems.

Recent advances have given dynamic systems scientists new tools for the study of change processes. There now exists a new class of statistical models called hierarchical linear models or multilevel models (Bryk & Raudenbush, 1992; Butt, Choi, & Jaeger, 2005; Prosser, Rasbash, & Goldstein, 1991) that allow researchers to examine developmental trajectories in microgenetic designs, made by tracking a key measure over frequent observations, for the group as a whole and for each individual. There have also been recent improvements in qualitative research methods, giving new credibility and rigor to the use of narrative descriptions of observed behavior and life history narratives (Denzin & Lincoln, 1994; Polkinghorne, 1995). These new quantitative and qualitative methods fit perfectly with the focus of dynamic systems on change over time in the qualitative macroscopic attractors.

In addition to observations of the natural evolution of systems, systems research often includes systematic experimental intervention or manipulation to uncover and identify the developmental resources necessary and sufficient to foster developmental change. In the intraindividual and interindividual systems, these resources include genes, cell and tissue interactions, sensory experience, diet and exercise, and social relations with conspecifics, to name but a few.

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Dynamic systems experimental interventions or manipulations attempt to discover the differences that make an impact by following developing systems as they develop and add or subtract features of normally occurring experience or activity to identify those developmental resources and their relationships that are necessary and sufficient to foster change. These differences are hypothesized to be innovations that have the potential to alter the system. The key idea is that the experimental alteration must never be so drastic as to destroy the possibility for the system to transform over time.

The following are examples of dynamic systems experimental procedures (Gottlieb & Lickliter, 2004; Lickliter & Honeycutt, 2003).

1. Experiential attenuation is when features of normally occurring experience are removed from the developmental context, allowing researchers to better identify how change is influenced by specific developmental resources in real time.

2. Experiential enhancement is when additional experience is added to the individual’s developmental context. This can be done by experiential substitution, in which normally occurring experience is replaced with a different form of experience, or experiential displacement, in which the temporal relations between features of experience are shifted or rearranged to allow deeper insight into the history or process of specific reorganizations.

These types of manipulations and the evaluation of their consequences on developmental change are often used in parallel with one another to explore the complexity and contingency of developmental processes. Combining microgenetic observation, which documents the process of change, with experimental manipulation, which identifies the developmental resources contributing to change, provides a powerful method for identifying the conditions under which change is most likely to occur.

In summary, dynamic systems research: 1. seeks primarily to probe the systemic and simultaneous linkages in the network of relationships that sustain particular patterns of development over time; 2. aims to uncover the possible pathways that lead to changes in certain undesirable patterns; and 3. attempts to discover the processes required to sustain and foster the development and maintenance of a healthy developmental trajectory, or a more desirable network of relationships needed for effective decision-making and positive social change.

In intervention research, for example, systems don’t get “fixed” or “cured” with a simple formula. Rather, the dysfunctional system must be allowed to transform slowly over time, systemically, into a more functional system. In dynamic systems science, we seek to understand the laws of transformation.

Qualitative Research and the Role of the Observer In the traditional quantitative research paradigm, one constructs hypotheses at the beginning of the study, carries out the planned observational or experimental procedure on a randomly selected sample from the population, derives numerical or categorical measures, analyzes the data in a manner directly driven by the hypotheses, and

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makes an interpretation. If the original hypothesis needs to be altered, the researcher returns to the population to test another sample with a variant of the procedure, or to re-code the data based on a different set of observational categories.

One of the central principles of qualitative research, in contrast, is an iterative, cyclical approach to interpretation during the data sampling, coding, and analysis. Thus, hypotheses, methods, and interpretations inform each other and change each other as a process, creating an inductive spiral known as the hermeneutic circle (Bromley, 1986; Robson, 1993). The observer, neither naïve nor objective, becomes an informed and involved scientist. Hermeneutic approaches have been used in case study, ethnographic, rhetorical, phenomenological, feminist, and symbolic interactional methods in the humanities and behavioral sciences (Bernstein, 1983; von Eckartsberg, 1986; Erickson, 1992; Gaskins, 1994; Lather, 1991; McCall & Wittner, 1990; Rogoff, Mistry, Goncu, & Mosier, 1993; Schwandt, 1994).

The principles of qualitative research are similar to the principles of qualitative, informational dynamic systems. In qualitative research, the investigator is part of the system being studied and engages with the system itself or with the data recorded from the system. A dynamic system is continually in a process of change in which no part of the system is permanently objective or fixed. Even so, in a dynamic system, semi-stable attractors can persist as the system cycles through iterations that, from the observer’s perspective, appear to be similar to each other. Similarly, there are no fixed hypotheses, categories, or conclusions in qualitative research. The qualitative scientist cycles iteratively through the data, each pass revealing a new working hypothesis and a new way to categorize. Yet eventually, these working interpretations coalesce into a semi-stable model of the system. The interpretation of the data becomes an attractor in a scientific system of information and communication. The iteration, interpretation, and revision continue until the observers feel confident of an emerging consistency and until new interpretations do not emerge during the process of reading and re-reading the data, which has been called the constant comparative method (Patton, 1990; Strauss & Corbin, 1990).

Credibility is a criterion used in qualitative research methods to evaluate whether the investigation successfully captures the meaning for the participants. Credibility parallels the notion of internal validity in quantitative methods. Observers are deemed more credible if they have a prolonged engagement with the data, the participants, and a record of persistent observation of the phenomenon under investigation (Denzin & Lincoln, 1994; Savage-Rumbaugh & Fields, 2000). Credibility is also enhanced if the investigators share excerpts of the original videos or transcriptions to allow the readers to make their own interpretations of the material (Rogoff et al., 1993).

These research methods are designed to create, via a meaning-making process, a semi-stable view of what is informative or meaningful for the participants in the social process. “The inquirer constructs a reading of the meaning-making process of the people he or she studies . . . The activity of understanding unfolds as one looks over one’s respondents’ shoulders at what they are doing” (Schwandt, 1994, p. 123).

Meaning making is equivalent to information creation in a qualitative dynamic system. To “make meaning” or to “create information” refers to the detection of a difference that makes a difference. How can scientists be assured that their interpretation

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of the subjects’ meanings are in accord with those of the subjects? At issue is the extent to which the warrant for interpretation of participants’ meaning is based on: (1) the investigator’s subjective identification with the participants using empathy, (2) the investigator’s construction of the participants’ meaning system within their own sociocultural context, or (3) the investigator’s linking of the interpretation of a particular case with the history of interpretations of other such cases within the literary genre that defines the investigator’s field of inquiry (Bradley, 1994; Jansen & Peshkin, 1992; Keegan & Gruber, 1994; Schwandt, 1994; Toren, 1996).

In practice, qualitative research involves all three of these warranting procedures.

Empathy is used, but it has a limit as a scientific tool since our participants are not the same as ourselves. Observers “can only approximate others’ experiences and so gain only limited access to their knowledge” (Belenky, Clinchy, Goldberger, & Tarule, 1986, p. 113). This sense of incompleteness, the inability to fully define and categorize another person, “marks the tragic, perpetually inadequate aspect of social research” (Reinharz, 1984, p. 365). This is perhaps especially the case when we study non-verbal infants, non-human animals, or people from very different cultures.

The limits of empathy point out the tragic fragility of scientific interpretations of behavior and stand in sharp contrast to the hubris of objectivist approaches. In the objectivist approach, the measures of individuals and groups are presumed to accurately stand for the real thing. What’s more, the appeal to a value-free, objective science adds to the warrant for making subjects of research into objects of study, less than fully alive beings. The qualitative scientist, by admitting the limits of inquiry and the indeterminacy of the findings, may seem weak and non-scientific by comparison.

Qualitative research, however, is a demanding exercise in not knowing, a deliberate attempt to hold back from premature interpretation and to capture the process of emergence. By making a conscious choice to stand outside of the objectivity of method, the qualitative scientist becomes a living part of the system. At the risk of seeming biased, qualitative researchers opt to expose the inherent dynamics of the social process. They accept as truth that which emerges from a process, and they see their own work as a reflection of the way in which the universe actually operates.

Qualitative investigators can rely on the literature in their field only so far because much of that work is done from a normative and seemingly objective point of view.

There are also limits to the researchers’ ability to step outside their own sociocultural and disciplinary point of view. The key to successful qualitative research, however, is to clarify one’s limitations and to engage in an active meaning-making process by which those perspectives and limitations are clarified. Again, the goal is not some ideal answer or result, but rather to engage in a process of meaning making that is likely to converge on an emergent description of the data. That description is accompanied by a description of the limits of the observer, as well as evidence for their credibility.

Research Example It is difficult to present a complete dynamic systems research example in the short space of this paper. Many more detailed examples of qualitative dynamic systems

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research using these principles can be found in Fogel et al. (2006a), King (2004), and Fogel, King, & Shanker (2006). In addition, a description of applied dynamic systems research methods is given in Fogel, Greenspan, King, Lickliter, Reygadas, Shanker & Toren (2006).

Here, an excerpt is presented from Fogel et al. (2006a) that illustrates the description of a developmental (Level 3) change in one mother-infant dyad during the period between 2 and 6 months. The attractors of interindividual relationships are regularly recurring patterns of communication called frames. Frames are segments of co-action that have a coherent theme, that take place in a specific location, and that involve particular forms of mutual co-orientation between participants. Because frames recur repeatedly over weeks and months, they have the features of an attractor in a dynamic system since they are reconstituted dynamically and dyadically on each reappearance.

Frames are semi-stable, lasting for only a finite period in an interindividual relationship. They emerge at one point in time and dissolve or disappear at another point in time. In a romantic partnership, for example, engagement or betrothal is a frame that has a limited time of life between courtship and marriage.

The communication between the 13 mother-infant dyads in this study was videotaped weekly during the 4-month observation period, meeting the conditions for a microgenetic research design (Figure 1). These videos were coded into four mutually exclusive and exhaustive relationship frames. The social frame was coded when the topic of communication was face-to-face play without objects. The guided object frame was coded when the mother took an active role in demonstrating and scaffolding the infant’s use of objects. The non-guided object frame was coded when the infant played with objects without the mother’s direct assistance but with her ongoing attention and verbal commentary. The social-object mixed frame was coded when elements both of face-to-face play and guided-object play appeared at the same time, as when a mother used a toy to touch the infant’s face or body while vocalizing in an expressive manner typical of the social frame.

The durations of each of the frames, measured as a percentage of time in the observation session (sessions lasted 10 minutes) is shown graphically in Figure 2 for one dyad, Betsy and her mother. Notice that the durations of the social and the guidedobject frames decline over this period, while the not-guided-object frame and the social-object mixed frame increase in duration.

In this example, the focus is on the sessions in which developmental change is most rapidly occurring, sessions 7 and 8, in which Betsy is 17 and 19 weeks old. During session 6, Betsy for the first time reaches for an object while looking at it. In session 7, the social frame declines dramatically. Betsy continues to look at her mother and smile during the other frames, thereby maintaining a connection with her mother, and thus blending the social frame into the other frames. This is seen especially in the rapid increase in duration of the social-object mixed frame. Sessions 7 and 8 are the first time that the not-guided object frame emerges as an entirely new frame, separate from the other object-related frames, in which Betsy explores objects without the mother’s assistance (as in the guided object and social-object mixed frame).

With the increasing growth of the not-guided-object frame, the guided-object frame, while actually declining quantitatively over time, continues to develop qualita-

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100

13 Social

90

Guided Object

80

Not-Guided Object

% of Session

70

Social-Object Mixed

60 50 40 30 20 10 0 1

2

3

4

5

6

7

8

9

*

*

*

Session

FIGURE 2. tively. The mother, for example, gives Betsy certain objects and helps her hold them when needed.

The not-guided-object frame and the guided-object frame now occur in quick succession.

Object manipulation follows a sequence composed of: Betsy actively mouthing an object (i.e., the not-guided-object frame), the mother introducing a new object to Betsy followed

by Betsy reaching for and grasping the new object (i.e., the guided-object frame), and then Betsy manipulating the second object, at times actively mouthing it (i.e., the not-guidedobject frame). This sequential patterning between the guided-object and the not-guidedobject frames appears to constitute a form of historical recapitulation in which an already existing historical frame (i.e., the guided-object frame) is maintained and makes transitions with a newly emergent frame (i.e., not-guided-object frame).

Now that Betsy is becoming more skilled at manipulating objects on her own, a new ordinary variability characterizing the social-object mixed frame also emerges during visits 7 and 8. The mother now uses the object Betsy is holding, making it kiss Betsyâ&#x20AC;&#x2122;s face without taking the object from her. It is as if Betsy is playing the object-touch games herself. Both Betsy and her mother are also becoming more serious, smiling and laughing relatively little and producing fewer vocalizations. The mother, for instance, uses far fewer sound effects with objects during visits 7 and 8. The impression the observer gets is that the social-object mixed frame is gradually becoming transformed as the not-guided-object frame emerges as a new and distinct frame. In fact, certain characteristics of the not-guided-object frame (such as helping Betsy play the object-touch games herself) appear to permeate the social-object mixed frame. (Fogel et al., 2006a)

These two sessions not only show a quantitative change in the frame durations, but there was also a qualitative change in the pattern of organization, both at the microlevel within the frames and the macrolevel of sequencing between the frames for Betsy and her mother. This complex system of linked changes constitutes a developmental (Level 3) change. The developmental change is not merely in the fact that the not-guided-

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object frame emerges for the first time, but rather because the whole system of frames seems to shape-shift in order to give birth to the new frame. All these changes are occurring simultaneously, as a dynamic process rather than a simple sequence.

The not-guided-object frame begins to pervade these sessions with the “support” of the guided-object frame and the social-object mixed frame. Compared to previous sessions, all of the observed frames (i.e., not-guided-object frame, guided-object frame, and socialobject mixed frame) undergo coordinated changes as reflected by the emergence of a new ordinary variability for each of these frames. Specifically, as Betsy becomes more objectfocused and fascinated with the new activity of examining the objects around her, the mother adjusts her object-oriented behaviors and begins providing support to her infant’s object exploration by handing them to Betsy.

The not-guided-object frame begins to become elaborated into a fully developed frame as Betsy spends increasing amounts of time manipulating objects. This constitutes a newly emergent frame that arises out of the innovations (Level 2 change: the mother places objects in Betsy’s hands) within the guided-object frame and social-object mixed frame during sessions 4, 5, and 6. At the same time, the guided-object frame expands its forms as illustrated by the increasing variability in the way the mother presents objects to Betsy. The socialobject mixed frame also changes from its earlier quality of enjoyable social play to becoming more focused on Betsy’s more serious examination of objects.

Furthermore, the dyad’s new ordinary variability (Level 1 change) during sessions 7 and 8 includes a patterned integration of the guided-object frame and the not-guided-object frame.

In this case, it is as if frames (i.e., guided-object frame and not-guided object frame) are blending together at the same time that a historical dynamic is recapitulated by the dyad.

All of these processes—the simultaneous re-organization of each of the frames in relation to each other and the emergence of a new frame in the context of the blending and recapitulation of frames—constitute what we consider to be the conditions of a developmental change (Level 3 change). Innovations (Level 2 change), as seeds for developmental change, alter the ordinary variability within frames on later occasions. This alteration, however, is of the same kind as the innovation when the infant becomes more active across multiple modalities. In the case of this developmental change, however, the entire pattern of communication changes across the whole system: all the frames and transitions are involved. For reasons we do not yet understand, the build-up and elaboration of innovations seems to reach a critical point at which time the “old” or historical system can no longer contain the innovations within ordinary variability. At this time, the system spontaneously shifts to a new system-wide organization that includes new frames, creative blending of old frames, and new actions within frames. It is important to note that we did not observe any single innovation or event that precipitated the developmental transition. (Fogel et al., 2006a)

Although the more detailed account cannot be given here, this excerpt shows the focus on history and meaning, the role of the observer, and the complexity of the co-actions across all three levels of change in the system. It also shows that a qualitative analysis provides something that cannot be gleaned from the quantitative description alone.

The two methods, quantitative and qualitative, support and complement each other as a description of the developmental change process.

Conclusions and Implications If dynamic social systems are fluid, changing, emergent, and yield created information in a meaning-making process, then dynamic systems research best serves sci-

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entific discovery by substantiating these same processes in the method. Applying the standards of research objectivity, with fixed measures and a priori hypotheses can only limit and diminish the phenomenon under study. As a complement to qualitative investigation, quantitative measures can enhance and deepen our understanding of systems phenomena. Quantitative measurement and statistical analyses are seen as one way of understanding, rather than the only way of understanding. Qualitative systems research seeks to place the scientist in the system, not knowing the answer. To become a credible witness, the scientist works toward an emergent understanding, allowing the reader to be part of the discovery process. In the end, the scientist and the reader understand more, while remaining immersed in the boundless possibilities of not knowing.

The closest disciplines to qualitative dynamic systems research are history, biography, and narrative analysis. The historian tracks multiple and related processes (frames) through time and attempts to understand how their co-actions and co-changes illuminate, say, the processes occurring at the beginning or ending of a war. Dynamic systems research can add to this enterprise by the use of the qualitative and quantitative methods and the explicit decomposition of the system into levels of change, as described in the above example.

Dynamic systems are inherently not predictable. The start or end of every war is different because the co-dynamics are always different and changing. Once a system enters into a developmental change period, as in sessions 7 and 8 in the above example, change is often rapid, spontaneous, unpredictable, and probably unstoppable. Notice in Figure 2 that the developmental shift occurs in only 2 or 3 sessions. In the periods before and after sessions 7 and 8, the durations of the frames remain relatively stable.

Developmental change carries a certain momentum such that once the system reaches a critical point, there is no turning back. On the other hand, in the larger study of which this example is a part (cf., Fogel et al., 2006a), we found in all of our dyads signatures of the impending change process in the weeks before it actually occurred: the innovations that began to shake the system loose from its ordinary variability.

If this research model could be applied to social, economic, and political change on a set of national and international cases, to take one example, it may be possible to uncover the underlying dynamics that foreshadow (but not predict) a more precipitous change. Once some of these predisposing factors are identified in naturalistic studies, dynamic systems experiments could be done in which those factors are attenuated or enhanced to diminish the likelihood of less desired subsequent changes and to enhance the likelihood of more desired ones.

The same model of research could be applied to therapeutic and educational interventions, to the emergence of famine, to epidemics and other health crises, and to the deterioration and wellness processes of the human body. The hope is to discover the laws of change and the dynamics of transformation. How much can a system take before it breaks down? What is the process by which transformation occurs? Can developmental change be facilitated even during the rapid (and presumably irreversible) period of change, or only earlier during the pre-change period? Why do some individuals and systems seem to resist change and others embrace change? What are the differences that make a difference for a developmental change in any particular system?

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The tools are now available to address these types of research questions, but these methods are slower and cost more than conventional research. This is because it is necessary to wait for the change to unfold, and many observations must be made in order to track the change process. The gain in understanding, however, is likely to be high.

Qualitative dynamic systems research is ideal for translational applications. Models that are expressed in terms of statistical interactions between quantitative variables are probabilistic and often far removed from the everyday process of meaning making as a social system. New models and interventions that rely on an understanding of the informational dynamics of the change process could be immediately applied to the work of practitioners and participants because these models are expressed in terms of the meanings that are already present in the system.

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Early Family Trauma and the Ontogeny of Glucocorticoid Stress Response in the Human Child: Grandmother as a Secure Base Mark V. Flinn Department of Anthropology and Department of Psychological Sciences University of Missouri FlinnM@Missouri.edu

David V. Leone Department of Anthropology University of North Carolina

Abstract: Loss of a parent by death or divorce is among the most traumatic experiences faced by a human child. Exposure to early family trauma (EFT) can have long-term effects on the limbic hypothalamic-anterior pituitary-adrenal cortex (HPA) axis and other components of neuroendocrine stress response. Because the HPA system has important immunomodulatory functions, children that have endured difficult family social conditions during development may be at higher risk for immune dysfunction and other health problems.

Here we investigate the mediating effects of grandparental relationships, mostly maternal grandmothers, on the ontogeny of HPA stress response among EFT children.

Sample and methods: A longitudinal eighteen-year study (1988â&#x20AC;&#x201C;2006) of child health in a rural community on the island of Dominica provides sequential biyearly data on salivary cortisol, morbidity, growth, and social environment (N= 282 children, 26,738 saliva samples from children + 5,470 saliva samples from their parents and other kin, 89,109 health observations, 46,788 anthropometric measurements, 42 months of residence in the community studying social environment). Patterns of cortisol response, extent of care from grandparents, morbidity, growth, and immune function are examined for associations with trauma at different periods during development.

Results: Grandparents are a common and important mediator of child wellbeing in this community. EFT children with extensive grandparental care are more likely to recover normal HPA function than are EFT children with little or no grandparental care. Lengthy informal discussions with children and their caregivers over the past 18 years suggest that grandparents are important components of their social worlds, including roles as temporary and permanent replacements for parents. EFT children with low contact rates with grandparents have more erratic cortisol profiles, higher morbidity, more growth disruptions, and more behavioral problems than EFT children with extensive grandparental care.

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Summary and conclusions: Grandparents appear to have significant mediating effects on child development in this population. Intensive grandparental care is positively associated with lower average cortisol, normal growth, and lower morbidity. No significant associations were found between grandparental care and parasite loads or average fluctuating asymmetry. Overall these results suggest the importance of grandparents, especially maternal grandmothers, for children who have experienced early trauma in their family environments.

Introduction: Grandparenting as an Evolved Human Adaptation “I love my granbaby more than anything God put here on this earth” . . . “I love Mama”1 . . . mutual hug and laugh. (Bwa Mawego2 grandmother and her granddaughter, from MVF fieldnotes, Oct. 10, 1992).

Grandparents and grandoffspring share 25% of their genes identical by descent, a significant opportunity for kin selection. Few species, however, live in groups with multiple overlapping generations of kin. Fewer still have significant social relationships among individuals two or more generations apart—such as elephants (Lee, 1987), some cetaceans (Mesnick, Evans, Taylor, Hyde, Escorza-Trevino, & Dizon, 2003; Whitehead, 2003), and some primates (Goodall, 1986; Lancaster & King, 1992).

Humans appear rather exceptional in this regard. Grandparenting is cross-culturally ubiquitous and pervasive (Murdock, 1967; e.g., Clarke, 1957; Sear, Mace, & McGregor, 2000). Our life histories allow for significant generational overlaps, including an apparent extended post-reproductive stage facilitated by the unique human physiological adaptation of menopause (Alexander, 1974, 1987; Hawkes, 2003; Williams, 1957).

The neuroendocrinological mechanisms guiding attachment processes in grandrelationships—such as the intense affiliation described in the anecdote above—are uncertain. The maternal neuropeptide oxytocin is a likely candidate. Regardless, the significance of emotional bonding between grandparents and grandchildren is beyond doubt. The evolved functions are uncertain, but likely involve the extraordinary importance of long-term extensive and intensive investment for the human child. The emotional and cognitive processes that guide grand-relationships evolved because they enhanced survival and eventual reproductive success of grandchildren.

Throughout human evolution, most children were likely to have benefited from the extra care provided by grandparents in addition to the investment by the immediate family. Children that for whatever reasons were not receiving much care from one or both parents were at risk, and, therefore, especially dependent upon help from grandparents. In addition to the physical basics of food, protection, and hygienic care, development of the human child is strongly influenced by the dynamics of the social environment (Dunn, 2004; Hetherington, 2003a, 2003b; Hinde & Stevenson-Hinde, 1987; Konner, 1991). Monitoring neuroendocrine stress response systems can provide useful insights into how children are coping with social challenges. Here we first re-

1. This three year-old child referred to her grandmother as “Mama,” and her mother by her given name.

2. All place names and research participant names used here are pseudonyms to protect privacy rights.

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view the potential functions of physiological stress response to stimuli in the social environment. We then investigate the effects of grandparents on the ontogeny of stress response among children that have endured the loss of a parent by death or separation.

The Paradox of Psychosocial Stress Humans elevate levels of the stress hormone cortisol in response to social challenges (Dickerson & Kemeny, 2004; Gunnar, Bruce, & Donzella, 2000). The magnitude and temporal pattern of cortisol release by the limbic hypothalamic-anterior pituitary-adrenal cortex (HPA) system can be altered by traumatic early experiences (Heim, Newport, Heit, Graham, Wilcox, Bonsall, Miller, & Nemeroff, 2000; Mirescu, Peters, & Gould, 2004; Weaver, Cervoni, Champagne, Dâ&#x20AC;&#x2122;Alessio, Sharma, Seckl, Dymov, Szyf, & Meaney, 2004). High levels of the primary stress hormones cortisol, corticotropin releasing hormone (CRH), and epinephrine may be toxic to developing dendrites, neurons, and receptors in the hippocampus and other brain regions that are involved in the negative feedback loop for cortisol regulation (Chen, Bender, Brunson, Pomper, Grigoriadis, Wurst, & Bararn, 2004; Sapolsky, Romero, & Munck, 2000). High levels of cortisol may also affect sensitivity of fear responses mediated by the amygdala. Hence early trauma may lead to permanent HPA-cortisol dysregulation. Because the HPA system has important immuno-modulatory functions (Ader, Felten, & Cohen, 2006; Sapolsky, 2005), children that have endured difficult social conditions during development may be at higher risk for immune dysfunction and other health problems.

The sensitivity of the HPA system to social stimuli presents an evolutionary paradox: why release cortisol if it has negative effects on health? We do not have good explanations for why natural selection favored links between the neuropsychological mechanisms involved with assessment of the social environment and the neuroendocrine mechanisms that regulate stress hormones. We also do not understand why these links are modifiable during development, such that early traumatic experiences may permanently alter hormone response to social challenges. And finally, we do not understand what factors, such as social support, may subsequently ameliorate the negative effects of early trauma on stress response (Caldji, Tannenbaum, Sharma, Francis, Plotsky, & Meaney, 1998; Cameron, Champagne, Parent, Fish, Ozaki-Kuroda, & Meaney, 2005; Francis, Diorio, Plotsky, & Meaney, 2002; Lupien, Fiocco, Wan, Maheu, Lord, Schramek, & Thanh Tu, 2005).

We approach these questions from an evolutionary paradigm that integrates proximate physiological explanations with ontogeny, phylogeny, and adaptive function (Tinbergen, 1963). Here we first briefly review the idea that childhood is an adaptation for coping with an increasingly complex and dynamic social and cultural environment. We then explore relations between physiological stress response and the ontogeny of social competencies. We posit that one of the important functions of the stress response system, in connection with emotional states such as fear or anxiety, is to manage the direction of mental processes to solving specific problems (Ademec, Blundell, & Burton, 2005; Flinn, 2006b, 2006d; Huether, 1998; Kaiser & Sachser,

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2005; Meaney, 2001; Pitman, 1989; Rodriguez Manzanares, Isoari, Carrer, & Molina, 2005). For example, in the relatively straightforward prey-predator situation of a gazelle smelling a lion, a “freeze” response, focused sensory acuities, and neurological circuits for escape behaviors may be enabled. The human child may face more cognitively challenging problems that use more information processing capacity, such as complex social interactions (Roth & Dicke, 2005). For example, when dealing with the challenge of making friends on the first day of school, a child needs to allocate her cognitive efforts to the tasks at hand: prepare for immediate contingencies by recalling salient information, enhancing relevant sensory input, and pre-activating circuits for appropriate actions. Stress hormones may enable not only the acute responses to such challenges, but facilitate their modification during development as well. Parents and grandparents may play an important role in this dynamic interplay between stress response to social challenges and the ontogeny of a child’s coping mechanisms by providing both security and information.

Hypotheses are evaluated with analyses of data from an 18-year study of child stress in a rural community on the island of Dominica. The longitudinal depth, large sample size (30,122 salivary cortisol measures from 282 children and their caregivers), and naturalistic paradigm provide a unique research design for investigating relations between social environment and ontogeny of stress response. Empirical analysis is complicated by the pleiotropic nature of the key stress hormone cortisol.

Moreover, the Dominica study does not have neurological data, hence direct or strong demonstrations of causal links among stress response, neural plasticity, family environment, grandparental care, and ontogeny of social competencies are not possible.

Our initial objective here is to review a plausible model that links stress response to the neural plasticity that enables adaptation to the dynamic human social environment. We then assess the effects of early family trauma on the ontogeny of stress response, and the potentially ameliorative effects of grandparental care. Understanding these relations may have significant consequences for child development and public health because it could provide new insights into associations among stress response, social disparities, and perinatal programming, among other outcomes (Barker, 1998; Dressler, Oths, & Gravely, 2005; Heim & Nemeroff, 2001; Maccari, Darnaudery, Morley-Fletcher, Zuena, Cinque, & Van Reeth, 2003; Marmot, 2004).

HPA Stress Response to Social Events Danny was roaming the Fond Vert area of the village with two of his closest friends, James and Isaiah, on a rainy Saturday morning. They had eaten their fill of mangoes, after pelting a heavily laden tree with stones for nearly an hour, taking turns testing their skill at knocking down breakfast. Now Danny was up the cashew tree in Mr. Pascal’s yard, tossing the yellow and red fruits to the smaller children below who had gathered to benefit from this kindness. Suddenly the sharp voice of his stepfather rang out from the nearby footpath. The bird-like chatter and laughter of the children immediately stopped. Danny’s hand froze mid-way to its next prize, and his head turned to face the direction of the yell with a mixed expression of surprise and fright.

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Ordered down from the tree, Danny headed quickly home, head bowed in apparent numb submission (vignette from MVF field notes, July 14, 1994). Danny’s salivary cortisol level rose from 2.2 to 3.8 µg/dl in little more than an hour. That afternoon, his secretory immunoglobulin-A levels dropped from 5.70 to 3.83 mg/dl. Three days later he had common cold symptoms: runny nose, headache, and fever. His two companions resumed their morning play, exhibiting a normal circadian decline in cortisol, and remained healthy over the next two weeks (Figure 1).

Danny had lost his father in a fishing accident when he was 3 years old. His relationships with his grandparents were not close; he visited them less than one hour a week. His friend James also did not have a co-resident father, as a consequence of a conjugal separation, but in contrast with Danny’s situation, James’ relationship with his maternal grandmother was very close, as illustrated by the following vignette.

James was sitting contentedly sorting rice with Ma Tee-Jean, his maternal grandmother. He startled when I (MVF) kicked a rock on the path to forewarn them of my approach into the household yard, and he inched closer to grandma, who put her arm around him. James was dressed and ready for school. He had left his mother’s house when an argument had broken out between his mother and stepfather last night, walking the 200 meters up the hill in the dark with his sister (MVF field notes, Sept 14, 1992). He was accustomed to this situation; James slept 44 out of 62 nights there in this summer of 1992, splitting his time between both households for most of the past

10:10 July 13 Ordered down from tree

3

17:35 July 17 Runny nose, cough, oral temp. = 101.2°F

s-IgA mg/dl

2

10

Cortisol z-score

1

0

–1

–2 13

14

15

16

17

0

July

FIGURE 1. Morning, mid-morning, and afternoon cortisol levels of Danny and his two friends during summer 1994. Danny’s cortisol levels were elevated and his s-IgA levels diminished after being reprimanded by his stepfather on the morning of July 13. Cortisol z-scores are standardized by fiveminute intervals since wake-up time to control for the circadian patterns of cortisol; s-IgA levels are the raw values. Danny exhibits symptoms of an upper respiratory infection with slight fever on the afternoon of July 20.

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four years, since his father had left when James was three years old and his stepfather had slowly moved in. James had always been close to his grandmother—whom he called “Mama”—as well as his mother—whom he called by her given name Lily.

James’ cortisol levels were often elevated by family conflicts, but the solace he usually found at his grandmother’s often resulted in a return to normal levels.

These anecdotal case examples contribute to a common pattern. Children in this rural Dominican community are more than twice as likely to become ill during the week following a stressful event than during a week when they had not recently experienced any significant stressors (Flinn & England, 2003). Chronic elevation of cortisol levels may have negative consequences for health (Cohen, Doyle, Turner, Alper & Skoner, 2003; Maier, Watkins, & Fleschner, 1994; Marmot & Wilkinson, 1999; Mason, Buescher, Belfer, Artenstein, & Mougey, 1979). Morbidity and mortality rates for children in the stressful environments of orphanages and hospitals, if lacking the evolutionarily-normal intimacy and social contact of the family, can be a significant public health concern worldwide. It is not lack of food or hygienic care, nor just the occurrence of traumatic events that affect child health, but the lack of social support, including parental warmth and other factors that influence emotional states (Belsky, 1997; Davidson, Jackson, & Kalin, 2001; Field, Diego, Hernandez-Reif, Schanberg, & Kuhn, 2003). Why should this be so? Why do social interactions, and a child’s perceptions of them, affect stress physiology and morbidity? And, more generally, why is the social environment of such paramount importance in a child’s world? From the Tinbergen perspective, these “why?” questions ultimately involve understanding the evolutionary design of the ontogeny of the mind and brain of the human child (e.g., Belsky, 1997; Bjorklund & Pellegrini, 2002; Gilbert, 2005).

In Danny and James’ village, located on the east coast of the island of Dominica where I have lived and studied part-time over the past eighteen years, most of a child’s mental efforts seem focused on negotiating social relationships with parents, siblings, grandparents, cousins and other kin, friends, teachers, bus drivers, neighbors, shop owners, and so forth. Foraging for mangoes and guavas, hunting birds, or even fishing in the sea from rock cliffs, are relatively simple cognitive enterprises, complicated by conflicts with property owners, and decisions about which companions to garner and share calories with. The mind of the child seems more concerned with solving social puzzles than with utilitarian concerns of collecting food. Other populations may have more difficult subsistence practices that require more extensive learning (e.g., Bock, 2005), but the social chess game nonetheless appears ubiquitous and cognitively demanding in all cultures (Blurton-Jones & Marlowe, 2002; Hewlett & Lamb, 2005), as it likely was during human evolutionary history (Adolphs, 2003; Alexander, 1979, 1989; Baumeister, 2005; Bowlby, 1969, 1973; Flinn, Geary, & Ward, 2005; Hinde, 1974).

Complex sociality appears to have been an important selective pressure shaping the uniquely human combination of physically altricial but mentally and linguistically precocial infancy, extended childhood, and extended adolescence, enabled by extensive bi-parental and kin care (Alexander, 2005; Geary & Flinn, 2002; Flinn & Ward, 2005). Physiological stress response may help guide both the acute and long-term neurological plasticity (Huether, Doering, Ruger, & Schussler, 1999) necessary for adapting to the dynamic aspects of human sociality (Flinn, 2006b). Grandparents may pro-

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vide important advice and enhance a secure base for the stressful tasks involved in the development of social competencies.

Evolution of the Extended Family as a Nest for the Child’s Social Mind The human family is extraordinary and unique in many respects (Alexander, 1989, 2005; Flinn, Ward, & Noone, 2005; Geary & Flinn, 2001; Lancaster & Lancaster, 1987). Humans are the only primate species to live in multi-male groups with complex coalitions and extensive paternal care. The altricial infant is indicative of a protective environment provided by intense parental and alloparental care in the context of kin groups (Alexander, 1990a; Chisholm, 1999; Hrdy, 1999, 2005; e.g., Ivey, 2000).

The human baby does not need to be physically precocial. Rather than investing in the development of locomotion, defense, and food acquisition systems that function early in ontogeny, the infant can work instead towards building a more effective adult phenotype. The brain continues rapid growth, and the corresponding cognitive competencies largely direct attention toward the social environment. Plastic neural systems adapt to the nuances of the local community (Alexander, 1990b; Bjorklund & Pellegrini, 2002; Geary & Bjorklund, 2000; Geary & Huffman, 2002). In contrast to the slow development of ecological skills of movement, fighting, and feeding, the human infant rapidly acquires skill with the complex communication system of human language (Bloom, 2000; Fisher, 2005; Pinker, 1994; Sakai, 2005). The extraordinary information-transfer abilities enabled by linguistic competency provide a conduit to the knowledge available in other human minds. This emergent capability for intensive and extensive communication potentiates (and presumably co-evolved with) the social dynamics characteristic of human groups (Deacon, 1997a, 1997b; Dunbar, 1997, 1998). The recursive pattern recognition and abstract symbolic representation central to linguistic competencies enable the open-ended, creative, and flexible informationprocessing characteristic of humans—especially of children.

Parents and other kin such as grandparents may be especially important for the child’s mental development of social and cultural maps because they can be relied upon as landmarks who provide relatively honest information. From this perspective, the evolutionary significance of the human family in regard to child development is viewed more as a nest from which social skills may be acquired than just as an economic unit centered on the sexual division of labor. An integration of the attachment paradigm (Bowlby, 1969; Lamb, 2005; Lamb, Bornstein, & Teti, 2002) with approaches emphasizing relationship networks (e.g., Kerr & Bowen, 1988; Suomi, 2005) would be congruent with this evolutionary logic (Belsky, 1997).

Grandparental Relationships Caregiving by individuals other than parents provides important benefits for infants and juveniles in a variety of taxa. “Helpers” in birds, rodents, social carnivores,

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elephants, and non-human primates enhance growth and survival (e.g., Alexander, Noonan, & Crespi, 1991; Brown, 1987; Clutton-Brock, 2002; Lee, 1987; Mitani & Watts, 1997). Kin selection and reciprocity appear to provide the evolutionary functions for non-parental care providers. Among primates, intensive allomaternal caregiving (e.g., feeding, carrying) is common in the callitrichids (e.g., Goldizen, 1987) and the colobines. Allomaternal care among the cercopithecines (e.g., Fairbanks, 1990; Maestripieri, 1994) and hominoids (e.g., Goodall, 1986; Nishida, 1990) is usually limited to protection from conspecifics and predators. Practice care is generally common among nulliparous females in social species (e.g., Hrdy, 1999). The prevalence of extensive alloparental care among humans (e.g., Flinn, 1989; Lahdenpera, Lummaa, Helle, Tremblay, & Russell, 2004; McKenna, 1982; Sear, Mace, & McGregor, 2000, 2003; Silk, 1990; Strassmann & Clarke, 1998; Tronick, Morelli, & Winn, 1987; Tronick, Morelli, & Ivey, 1992), particularly the importance of grandparents for direct care (Alexander, 1979; Hawkes, 2003), represents a strong divergence from our closest primate relatives.

The conditions responsible for the evolution of extensive alloparental care in humans are likely to include the importance of localized kin groups, altricial infants, prolonged childhood, extended generational overlap, and the cultural transmission of information (Alexander, 1989; Coe, 2003; Flinn & Ward, 2005; Geary & Flinn, 2001; Hrdy, 2005). Grandparents appear to be the most significant of potential alloparental caregivers (Hrdy, 2005).

The informational arms race that characterizes human social competition involves substantial novelty (Flinn, 2004, 2006a; Flinn & Alexander, 2006; Flinn & Coe, 2006) and hence requires unusual phenotypic plasticity. Although knowledge of the basic neuroanatomical structures involved with human social aptitudes has increased dramatically (e.g., Allman, 1999; Damasio, 2003; Gallese, 2005; Moll, Zahn, de OliveiraSouza, Krueger, & Grafman, 2005), the mechanisms that guide their ontogeny remain uncertain. Neuroendocrine stress response to stimuli in the social environment may provide important clues.

Stress Hormone Profiles as an Assessment of Caretaking Environment Changing, unpredictable environments require adjustment of priorities. Growth, immunity, digestion, and sex are irrelevant while being chased by a predator (Sapolsky 1994), or coping with a traumatic social event. Emergencies—large and small, good and bad—perceived by the brain stimulate a variety of neuroendocrine systems.

Hundreds of different endogenous chemicals—steroid and peptide hormones, neurotransmitters, cytokines, and so forth—are released from secretory glands and cells in response to information received and processed by the central nervous system (CNS).

The movement of these chemicals in plasma and other intercellular fluids communicates information among cells and tissues, helping the body to respond appropriately to varying environmental demands.

Physiological stress responses affect the allocation of energetic and other somatic resources to different bodily functions via a complex assortment of endocrine and neu-

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roendocrine mechanisms. Stress hormones help shunt blood, glucose, products of the immune system, and other resources to cells and tissues necessary for the task at hand.

Chronic and traumatic stress can diminish long-term health, evidently because resources are diverted away from important health functions, including cellular repair, building muscle mass, immune response, and neuromodulation (Korte, Koolhaas, Wingfield, & McEwen, 2005; Selye, 1976). Stress during childhood may be particularly harmful because of the additional demands of growth and development, especially of the CNS (Rutter, 1991).

During the first few years of life the human brain more than doubles in size via an extraordinary spurt of cell growth, migration, specialization, remodeling, and pruning.

The brain consumes almost half of the infant’s resting caloric requirements. The thymus and other parts of the immune system undergo a similarly dramatic transformation, preparing defenses against a nearly infinite variety of pathogens, while selecting out responses to the numerous molecular fingerprints of self-tissues. Even under the best of circumstances successful outcome of these complex ontogenetic trajectories would seem miraculous; the developing child, however, often faces a most imperfect environment. Emotional and physical stressors—such as abuse, neglect, parental divorce, strenuous work, exogenous toxins, inconsistent punishment, infectious disease, and malnutrition—are powerful stimulants of physiological stress response with potential effects on brain and immune development (e.g., Boyce, Adams, Tschann, Cohen, Wara, & Gunnar, 1995; Fukunaga, Mizoi, Yamashita, Yamada, Yamamoto, Tatsuno, & Nishi, 1992; Maccari et al., 2003; McEwen, 1995, 1998). But even common, everyday activities may be important.

Physiological responses to environmental stimuli that are cognitively perceived as “stressful” are modulated by the limbic system (amygdala and hippocampus) and basal ganglia that interact with the sympathetic and parasympathetic nervous systems and several neuroendocrine axes. Here we are primarily concerned with what has traditionally been termed the limbic hypothalamic-anterior pituitary-adrenal cortex system (HPA). The HPA system affects a wide range of physiological functions in concert with other neuroendocrine mechanisms and involves complex feedback regulation. The HPA system regulates glucocorticoids, primarily cortisol, which is normally released in seven to fifteen pulses during a 24-hour period (for reviews see: de Kloet, Sibug, Helmerhorst, & Schmidt, 2005; Ellis, Essex, & Boyce, 2005; Gold & Chrousos, 2002; Gray, 1982, 1987; McEwen, 1995; Sapolsky, 1992a, 1992b; Weiner, 1992).

Cortisol is a key hormone produced in response to physical and psychosocial stressors in humans. Cortisol modulates a wide range of somatic functions, including: (a) energy release (e.g., stimulation of hepatic gluconeogenesis in concert with glucagon and inhibition of some effects of insulin), (b) immune activity (e.g., control of inflammatory response and the cytokine cascade, particularly Il-2), (c) mental activity (e.g., alertness, memory, and learning), (d) neural modification, (e) growth (e.g., inhibition of growth hormone and somatomedins), and (f) reproductive function (e.g., inhibition of gonadal steroids, including testosterone). These complex multiple effects of cortisol muddle understanding of its adaptive functions. The demands of energy regulation must orchestrate with those of immune function, and so forth. Receptor differentiation, competition with mineralocorticoids for binding sites, and other mechanisms enable localized targeting (e.g., glucose uptake by active versus inactive

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muscle tissues, neuropeptide directed immune response, modulation by antiglucocorticoids, and cell-specific interactions with macrophages) of the above general physiological effects (e.g., de Kloet et al., 2005). Cortisol regulation allows the body to respond to changing environmental conditions by preparing for, and recovering from, specific short term demands (Mason, 1971; Munck, Guyre, & Holbrook, 1984).

These temporary beneficial effects of glucocorticoid stress response, however, are not without costs. Persistent activation of the HPA system is associated with immune deficiency, cognitive impairment, inhibited growth, delayed sexual maturity, damage to the hippocampus, enhanced sensitivity of amygdala fear circuits, and psychological maladjustment (Ader, 2001; Dunn, 1995; McEwen & Magarinos, 1997; Sapolsky, 1996). Deleterious effects of high cortisol to neurons in the hippocampus appear to occur after saturation of the high affinity mineralocorticoid receptors (MRs) and subsequent extensive binding of the glucocorticoid receptors (GRs) (de Kloet et al., 2005; Reul & de Kloet, 1985). Chronic stress may diminish cellular energy (Sapolsky, 1991; Sapolsky & Stein, 1989) and produce complications for autoimmune protection (Munck & Guyre, 1991). Stressful life events—such as divorce, death of a family member, change of residence, or loss of a job—are associated with infectious disease and other health problems during adulthood (Cohen et al., 2003; Maier et al., 1994; Marmot & Wilkinson, 1999).

Current psychosocial stress research suggests that cortisol response is stimulated by uncertainty that is perceived as significant and for which behavioral responses will have unknown effects (Dickerson & Kemeny, 2004; Kemeny, 2003; Kirschbaum & Hellhammer, 1994). In a child’s world, important events are going to happen. The child does not know how to react so as to achieve desired outcomes, but is highly motivated to figure out what should be done. Cortisol release is associated with unpredictable, uncontrollable events that require full alert readiness and mental anticipation.

In appropriate circumstances, temporary moderate increases in stress hormones (and associated neurotransmitters such as dopamine) may enhance mental activity for short periods in localized areas and prime memory storage, hence improving cognitive processes for responding to social challenges (Beylin & Shors, 2003; Boyce & Ellis, 2005; Domes, Heinrichs, Reichwals, & Hautzinger, 2002; LeDoux, 2000, 2003; cf.

McEwen & Sapolsky, 1995; McGaugh, 2004). Mental processes unnecessary for appropriate response may be inhibited, perhaps to reduce external and internal “noise” (Servan-Schreiber, Printz, & Cohen, 1990; cf. Kirschbaum, Wolf, May, Wippich, & Helhammer, 1996; Lupien et al., 2005).

Experimental studies that expose subjects to acute temporal stressors such as public speaking or parachute jumping reliably elevate stress hormones (Dickerson & Kemeny, 2004). Relations between cortisol production and emotional distress in natural settings, however, are difficult to assess because of temporal and interindividual variation in HPA response (Dabbs & Hopper, 1990; Ellis, Jackson, & Boyce, 2006; Kagan, 1992; Pollard, 1995; Nachmias, Gunnar, Mangelsdorf, Parritz, & Buss, 1996; Tennes & Mason, 1982). Habituation may occur to repeated events for which a child or adult acquires an effective mental model. Apparently “stressful” job environments may not stimulate increased levels of stress hormones if individuals have adjusted to them. Expressions of behavioral distress (e.g., crying) among children are not reliably associ-

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ated with elevated cortisol (Gunnar, 1992; cf. Ahnert, Gunnar, Lamb, & Barthel, 2004; Flinn, 2006c), and some studies suggest that phobic individuals exhibit only moderate rises in cortisol during clinical phobic episodes (Nesse, Curtis, Thyer, McCann, Huber-Smith, & Knopf, 1985). Attenuation and below-normal levels of cortisol may follow a day or more after emotionally charged events. Personality may affect HPA response (and vice versa), because children with inhibited, anxious, or fearful temperaments tend to have higher cortisol levels than extroverted children (Kagan, Resnick, & Snidman, 1988; cf. Suomi, 1991; Hart, Gunnar, & Cicchetti, 1995; Higley & Suomi, 1996; Nachmias et al., 1996).

Chronically stressed children may develop abnormal cortisol response, possibly via changes in binding globulin levels, and/or reduced affinity or density of glucocorticoid, CRH, oxytocin and vasopressin receptors in the brain (De Kloet, 1991; Fuchs & Flugge, 1995). Early experience—such as perinatal stimulation of rats (Meaney, Mitchell, Aitken, Bhat Agar, Bodnoff, Ivy, & Sarriev, 1991; Takahashi, 1992; Weaver et al., 2004), some types of prenatal stress of rhesus macaques (Schneider, Coe, & Lubach, 1992; Clarke 1993), maternal-infant attachment among humans (Spangler & Grossmann, 1993), and sexual abuse among humans (De Bellis, Chrousos, Dorn, Burke, Helmers, Kling, Trickett, & Putman, 1994; Heim et al., 2002)—may permanently alter HPA response.

Further complications arise from interaction between HPA stress response and a wide variety of other neuroendocrine and neuroimmune activities, including modulation of catecholamines, melatonin, testosterone, serotonin, ß-endorphins, cytokines, and enkephalins (de Kloet, 1991; Miller, Cohen, & Ritchey, 2002; Sapolsky, 1990b, 1992b). Changes in cortisol for energy allocation and modulation of immune function may be confused with effects of psychosocial stress. Cortisol may be a co-factor priming dopamine, oxytocin, and vasopressin intracerebral binding sites that are associated with the neuroplasticity of familial attachment in mammals (Carter, 2005; Fleming, Steiner, & Corter, 1997), and hence may influence distress involving caretaker-child relationships (see also Aragona, Liu, Yu, Curtis, Detwiler, Insel, & Wang, 2006; Carter, 2003; Cushing & Kramer, 2005; Porges, 1998; Tennes, 1982; Wismer Fries, Ziegler, Kurian, Jacoris, & Pollak, 2005). Synergistically, oxytocin has important effects on social cognition and fear (Heinrichs, Baumgartner, Kirschbaum, & Ehlert, 2003; Kirsch, Esslinger, Chen, Mier, Lis, Siddhanti, Gruppe, Mattay, Gallhofer, & Meyer-Lindenberg, 2005). Other components of the HPA axis, such as corticotropin releasing hormone (CRH) and melanocyte stimulating hormone, have additional stress-related effects that are distinct from cortisol. Finally, a variety of hormones such as estrogens and other endogenous chemicals—including “antiglucocorticoids”— mediate specific actions of cortisol (e.g., Kaufer, Ogle, Pincus, Clark, Nicholas, Dinkel, Dumas, Ferguson, Lee, Winters, & Sapolsky, 2004). Concurrent monitoring of all these neuroendocrine activities would provide important information about stress response, but is not possible in a non-clinical setting with current techniques.

Relations between stress-induced cortisol response and immunosuppression are perhaps even more complex and enigmatic (Coe & Lubach, 2005; McEwen, 1998; Sapolsky, 2005). Stress is associated with a variety of illness, including infectious disease, reactivation of latent herpes virus, cancer, and cardio-vascular problems. The

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wide range of health effects of stress suggests that a number of immune mechanisms are involved. Cortisol influences many functions of lymphocytes, macrophages, and leukocytes, and as with energy use, may direct their movement to specific locations and even modulate apoptosis (Costas et al., 1996). Cortisol also inhibits the production of some cytokines (e.g., interleukin-1) and mediates several components of the inflammatory response. In concert with the sympathetic system, which generally downmodulates lymphocyte and monocyte functions, HPA stress response affects all of the major components of the immune system. However, the effects of neuroendocrine stress response are not all inhibitory, and involve temporary up-regulation and/or localized enhancement of some immune functions (Dhabbar & McEwen, 2001; Jefferies, 1991; Coe & Lubach, 2005).

Stress response involves an optimal allocation problem (Sapolsky, 1990a, 1994). Energy resources are diverted to muscular and immediate immune functions and other short-term (stress emergency) functions, at cost to long-term functions of growth, development, and building immunity. Under normal conditions of temporary stress, there would be little effect on health. Indeed, there may be brief enhancement and directed trafficking of immune (Dhabbar & McEwen, 2001) and cognitive function. Persistent stress and associated hyper- or hypo-cortisolemia, however, is posited to result in pathological immunosuppression, depletion of energy reserves, and damage to or inhibition of neurogenesis in parts of the hippocampus (e.g., Gould & Tanapat, 1999; Santarelli, Saxe, Gross, Surget, Battaglia, Dulawa, Weistaub, Lee, Duman, Arancio, Belzung, & Hen, 2003; Sheline, Gado, & Kraemer, 2003). This perspective highlights the problems with a stress response system that evolved to cope with short-term emergencies. The chronic stress produced by modern human—or other primates with complex relationships— social environments may present novel challenges that the system is not designed to handle, hence potentially resulting in maladaptive pathology (Sapolsky, 1994, 2003).

This strict version of an environmental novelty hypothesis, however, is difficult to reconcile with the long evolutionary histories of complex sociality in primates, and especially humans, accompanied by dramatic changes in the brain. Why, given all the extensive modifications of the human brain over the past several million years, would selection not have weeded out this apparent big mistake? Modern human environments have many novelties that elicit stress response, but social challenges in general seem to have a much more ancient evolutionary depth, and may be a key selective pressure for the large human brain. One possibility is that the demands of preparing for potential dangers are an unavoidable costly insurance, akin to expensive febrile response to pathogens that are usually benign—the “smoke-detector” principle (Nesse & Young, 2000). The idea is that although physiological stress response to social challenges is costly, and most often wasteful, it may have helped our ancestors cope with rare and unpredictable serious conflicts often enough to be maintained by selection.

The benefit/cost ratio could be improved by fine-tuning stress mechanisms in response to environmental conditions during ontogeny.

A complementary approach suggests that neuroendocrine stress response may guide adaptive neural reorganization, such as enhancing predator detection and avoidance mechanisms (Buwalda, Kole, Veenema, Huininga, De Boer, Korte, & Koolhas, 2005; Dal Zatto, Marti, & Armario, 2003; LeDoux, 2000; Rodriguez Manzanares

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et al., 2005; Meaney, 2001; Wiedenmayer, 2004). Exposure to cats that elevates glucocorticoid levels can have long-term effects on the central amygdala (right side) in mice, resulting in increased fear sensitization (Ademec et al., 2005; see also Knight, Nguyen, & Bandettini, 2005). The potential evolutionary advantages of this neural phenotypic plasticity are apparent (Rodriguez Manzanares et al., 2005). Prey benefit from adjusting alertness to match the level of risk from predators in their environments. Post-Traumatic Stress Disorder (PTSD) appears analogous to these fear conditioning models, and involves similar effects of noradrenergic (Pitman et al., 2002) and glucocorticoid systems (Roozendaal, 2002; Roozendaal, Quirarte, & McGaugh, 2002) on associative long-term potentiation of the amygdala. Social defeat also affects the amygdala and hippocampus, but in different locations (Bartolomucci, Palanza, Sacerdote, Panerai, Sgoifo, Dantzar, Parmigiani, 2005; Buwalda, Felszhegy, Horvath, Nyakas, de Boer, & Bohus, 2001; Koolhaas, de Boer, de Ruiter, Meerlo, & Sgoifo, 1997), suggesting that neural remodeling and LTP is targeted and domain-specific (e.g., Pham, McEwen, Ledoux, & Nader, 2005; Rumpel, LeDoux, Zador, & Malinow, 2005). Glucocorticoids, perhaps in combination with peptide hormones and catecholamines, appear to facilitate the targeting of domain-specific remodeling and longterm potentiation (Huang & Herbert, 2006). The potentiating effects of cortisol on emotional memories and other socially salient information may be of special significance in humans (Fenker, Schott, Richardson-Klavehn, Heinze, & DĂźzel, 2005; Jackson, Payne, Nadel, & Jacobs, 2006; Lupien et al., 2005; Pitman, 1989). The neurological effects of stress response may underlie adaptation to both short-term contingencies and guide long-term ontogenetic adjustments of behavioral strategies.

If physiological stress response promotes adaptive modification of neural circuits in the limbic and higher associative centers that function to solve psychosocial problems (Huether et al., 1999), then the paradox of psychosocial stress would be partly resolved. Temporary elevations of cortisol in response to social challenges could have advantageous developmental effects involving synaptogenesis and neural reorganization (Buchanan & Lovallo, 2001; Huether, 1996, 1998) if such changes are useful and necessary for coping with the demands of an unpredictable and dynamic social environment. Elevating stress hormones in response to social challenges makes evolutionary sense if it enhances specific acute mental functions and helps guide cortical remodeling of â&#x20AC;&#x153;developmental exuberanceâ&#x20AC;? (Flinn, 2006b; Innocenti & Price, 2005; Sur & Rubenstein, 2005).

Chronic destabilization of neuronal networks in the hippocampus or cerebral cortex, combined with enhanced fear circuits in the amygdala (e.g., Bauer, LeDoux, & Nader, 2001; Phan, Fitzgerald, Nathan, & Tancer, 2006), however, could result in apparently pathological conditions such as PTSD (Tupler & DeBellis, 2006; Yehuda, 2002) and some types of depression (Preussner, Baldwin, Dedovic, Renwick, Khalili Mahani, Lord, Meaney, & Lupien, 2005). Even normal (but rather novel) everyday stressors in modern societies, such as social discordance between what we desire and what we have (Dressler & Bindon, 2000), might generate maladaptive HPA response.

Individual differences in perception, emotional control, rumination, reappraisal, selfesteem, and social support networks seem likely co-factors (see also Ellis, Jackson, & Boyce, 2006).

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Testing these ideas about relations between physiological stress response, neural remodeling, and adaptation to the social environment is not a simple or easy task (e.g., Pine, Fyer, Grun, Phelps, Szesko, & Koda, 2001). Cortisol can affect cognitive functioning, and cognitive processing can affect cortisol response, all in an ongoing ontogenetic dance. Teasing out the causes and effects in ontogenetic sequence requires sequential data on physiological response profiles, environmental context, and perception. Extensive research on hormonal stress response has been conducted in clinical, experimental, school, and work settings (Dickerson & Kemeny, 2004; Gunnar, Tout, de Haan, Pierce, & Stansbury, 1997; Panter-Brick & Pollard, 1999; Stansbury & Gunnar, 1994; Weiner, 1992). We know relatively little, however, about stress neuroendocrinology among children in normal everyday (“naturalistic”) environments, particularly in non-industrial societies (Panter-Brick, 1998). Investigation of childhood stress and its effects on development has been hampered by the lack of noninvasive techniques for measurement of stress hormones. Frequent collection of plasma samples in non-clinical settings is not feasible. The development of saliva immunoassay techniques, however, presents new opportunities for research on stress response to everyday life. Saliva is relatively easy to collect and store, especially under adverse field conditions faced by anthropologists and psychologists working in naturalistic research settings (Ellison, 1988). Longitudinal monitoring of a child’s daily activities, stress hormones, and psychological conditions provides a powerful research design for investigating naturally occurring stressors. Analyzing hormone levels from saliva can be a useful tool for examining the child’s imperfect world and its developmental consequences, especially when accompanied by detailed ethnographic, medical, and psychological information. Unfortunately, we do not yet have field techniques for assessment of corresponding ontogenetic changes in the relevant neurological mechanisms.

Social Worlds and the Ontogeny of Stress Response: The Dominica Study Assessment of relations among psychosocial stressors, hormonal stress response, family environment, and health during child development is complex, requiring (a) longitudinal monitoring of social environment, emotional states, hormone levels, immune measures, and health, (b) control of extraneous effects from physical activity, circadian rhythms, and food consumption, (c) knowledge of individual differences in temperament, experience, and perception, and (d) awareness of specific social and cultural contexts. Multi-disciplinary research that integrates human biology, psychology, and ethnography is particularly well suited to these demands (Bogin, 1999; Panter-Brick, 1998). Physiological and medical assessment in concert with ethnography and coresidence with children and their families in anthropological study populations can provide intimate, prospective, longitudinal, naturalistic information that is not feasible to collect in clinical studies. For the past eighteen years (1988–present) we have conducted such research with the help of many colleagues and students and the extraordinary cooperation of a wonderful study population.

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The Study Village “Bwa Mawego” is a rural community located on the east coast of Dominica. About 500 residents live in 160 structures/households that are loosely clumped into five “hamlets” or neighborhoods. The population is of mixed African, Carib, and European descent. The community is isolated because it sits at the dead-end of a rough road.

Part-time residence is common, with many individuals emigrating for temporary work to other parts of Dominica, other Caribbean islands, the United States, the United Kingdom, or Canada. Most residents cultivate bananas and/or bay leaves as cash crops, and plantains, dasheen, and a variety of fruits and vegetables as subsistence crops. Fish are caught by free-diving with spear-guns and from small boats (hand-built wooden “canoes” of Carib design) using lines and nets. Land is communally “owned” by kin groups, but parceled for long-term individual use.

Most village houses are strung close together along roads and tracks. Older homes are constructed of wooden planks and shingles hewn by hand from local forest trees; concrete block and galvanized roofing are more popular today. Most houses have one or two sleeping rooms, with the kitchen and toilet as outbuildings. Children usually sleep together on foam or rag mats. Wealthier households typically have “parlors” with sitting furniture. Electricity became available in 1988; during the summer of 1995 about 70% of homes had “current,” 41% had telephones, 11% had refrigerators, and 7% had televisions. Water is obtained from streams, spring catchments, and run-off from roofs; public piped water became available in June 1999, but few households are connected.

The community of Bwa Mawego is appropriate for the study of relations between a child’s social environment and physiological stress response for the following reasons: (1) there is substantial variability among individuals in the factors under study (i.e., family environments, social challenges, and stress response), (2) the village and housing are relatively open, hence behavior is easily observable, (3) kin tend to reside locally, (4) the number of economic variables is reduced relative to urban areas, (5) the language and culture are familiar to the investigator, (6) there are useful medical records, and (7) local residents welcome the research and are most helpful.

The study involved 282 children and their caregivers residing in 84 households.

This is a nearly complete sample (> 98%) of all children living in four of the five village hamlets during the period of fieldwork.

Methods and Field Techniques “. . . we finished getting the spit today! . . . maybe we should collect a couple more [duplicate] samples tomorrow from a few of the kids . . . just to make sure the lab measures are reliable . . . and to double-check that cortisol levels do not change much from day to day.”

(MVF field notes, July 18, 1989)

Our initial objective, back in 1989, was to assess what each child’s general stress level was, as determined by a single measure of the level of cortisol in their saliva. The idea was to see how this hormone was associated with a child’s family environment.

We assumed, rather naively, but in good academic company, that salivary cortisol

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levels were a fairly stable “trait” character. What seemed like an unnecessarily cautious decision at the time to collect and assay additional saliva samples from several of the children resulted in a rather more complex study. We were quite surprised when the results of the additional sample assays indicated that a child’s cortisol levels varied substantially from one day to the next. Serendipity provided samples from two siblings in good spirits one day, but sad and upset by a family quarrel the next, in concert with field notes detailing the events. This temporal link between cortisol levels and psychosocial states suggested a dramatic revision of research design. We also were fortunate to have saliva samples from different times of day in this initial collection, and quickly recognized that very precise control of circadian patterns—in particular sleep schedules and wake-up times—was critical to accurate assessment of HPA stress response (Flinn & England, 1992). More than 30,000 saliva samples later, it seems we have more questions than answers.

In this study, sequential longitudinal monitoring is used to assess physiological stress response to everyday events, including social challenges. Saliva is collected from children by members of the research team at least twice a day, wherever the children happen to be (usually at their household). This direct collection and observation procedure avoids errors that can occur with at-home self- or parent-collection and report protocols. The large sample size of cortisol measures for each child (>100 samples for most children) in a variety of naturalistic contexts provides a more extensive and complex picture of HPA stress response than small sample designs.

Data analyses examine both long term (ten+ years) and short term (day-to-day, hour-by-hour) associations among cortisol levels, family composition, socioeconomic conditions, behavioral activities, events, temperament, growth, medical history, immune measures, and illness. Physiological stress response is assessed by radioimmunoassay (RIA) of cortisol levels in saliva. Analyses include mean values, variation, and day-to-day and hour-by-hour profiles of standardized (circadian control by 5-minute intervals from wake-up time) cortisol data (Flinn & England, 2003; Flinn & Quinlan, in prep.). Family composition is assessed by age, sex, genealogical relationship, and number of individuals in the caretaking household. Socioeconomic conditions include household income, material possessions, land ownership, occupations, and educational attainment. Caretaking is assessed by (a) frequencies and types of behavioral interaction, (b) informant ratings of caretaking that children received, and (c) informant interviews. Here we use a dichotomous (above median, below median) composite measure of caretaking by grandparents (“GPC”). Immune response is assessed by turbidimetric immunoassay of secretory-immunoglobulin A from saliva; however, relatively few samples have been assayed (N = 212), and interpretation is uncertain so inferences are preliminary. Health is assessed by (a) observed type, frequency, and severity of medical problems (diarrhea, influenza, common cold, asthma, abrasions, rashes, etc.), (b) informant (parents, teachers, neighbors) ratings, (c) medical records, (d) growth (standard anthropometric measures, including height, weight, and skinfolds) and fluctuating asymmetry patterns (Flinn, Leone, & Quinlan, 1999; Leone, 2005) and (e) physical examination by a medical doctor. The primary measure of health used is percentage of days ill, the proportion of days that a child was observed (directly by researchers) with common benign temporary infectious disease

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(89% were common-cold upper respiratory tract infections with nasal discharge, cough, or myalgia—e.g., rhinovirus, adenovirus, parainfluenza, and influenza; 6% were diarrheal; 5% were miscellaneous indeterminate—e.g., febrile without other symptoms). Daily activities and emotional states are assessed from (a) caretaker and child self-report questionnaires, and (b) systematic behavioral observation (focal follow and instantaneous scan sampling). Multiple sources of information are crosschecked to assess reliability (Bernard, Killwoth, Kronenfield, & Sailer, 1984).

In the following section we briefly review some of the results from this study that may provide useful insights into the ontogeny of stress response to psychosocial challenges. We then turn to examining the effects that grandparents have in guiding this aspect of child development.

Cortisol Response to Naturally Occurring Social Challenges Our analyses of naturally occurring stressors in children’s lives in Bwa Mawego indicate that social challenges are important stressors, with the emphasis upon the family environment as both a primary source and mediator of stressful stimuli (Flinn & England, 1995, 2003; Flinn, Turner, Quinlan, Decker, & England, 1996; Turner, Flinn, & England, 1995). Temporary moderate increases in cortisol are associated with common activities such as eating meals, active play (e.g., cricket), and hard work (e.g., carrying loads of wood to bay oil stills) among healthy children. These moderate stressors—“arousers” might be a more appropriate term—usually have rapid attenuation, with cortisol levels diminished to normal within an hour or two (some stressors have characteristic temporal “signatures” of cortisol level and duration—see Figure 5 for an example).

High-stress events (cortisol increases from 100% to 2000%), however, most commonly involved trauma from family conflict or change (Flinn & England, 2003). Punishment, quarreling, and residence change substantially increased cortisol levels, whereas calm, affectionate contact is associated with diminished (–10% to –50%) cortisol levels. Of all cortisol values that are more than two standard deviations above mean levels (i.e., indicative of substantial stress), 19.2% are temporally associated with traumatic family events (residence change of child or parent/caretaker, punishment, “shame,” serious quarreling, and/or fighting) within a 24-hour period—for comparison, 12% are associated with minor family conflicts, 9.2% with peer conflicts or school problems, 7.9% with illness, and 6.4% with physical exertion, the next highest categories; 43.4% have no recorded abnormal event. In addition, 42.1% of traumatic family events are temporally associated with substantially elevated cortisol (i.e., at least one of the saliva samples collected within 24 hours is > 2 SD above mean levels)—other consistent predictors of elevated cortisol include illness with fever and high profile competitive sports events. Chronic elevations of cortisol levels, as in the example of the Franklin family (Figure 2), may also occur, but are more difficult to assess quantitatively.

There is considerable variability among children in cortisol response to family disturbances. Not all individuals have detectable changes in cortisol levels associated

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Cortisol (standardized)

3

family conflict

family returns

2

1

0

–1 June

24

25

26

27

28 29

July

19

20

21

22

FIGURE 2. On June 28, 1992, a serious marital conflict erupted in the “Franklin” household. “Amanda” was a 34-year-old mother of six children, five of whom (ages 2, 3, 5, 8, and 14) were living with her and their father/ stepfather, “Pierre Franklin.” Amanda was angry with Pierre for spending money on rum. Pierre was vexed with Amanda for “shaming” him in front of his friends. He left the village for several weeks, staying with a relative in town. His three genetic children (ages 2, 3, and 5) showed abnormal cortisol levels (in this case, elevated) for a prolonged period following their father’s departure. This pattern is typical: children usually became habituated to stressful events, but absence of a parent often resulted in abnormal patterns of elevated and/or subnormal cortisol levels. Following the return of their father, the Franklin children’s cortisol levels resumed a more normal profile. Again, this pattern is typical: children living in families with high levels of marital conflict (observed and reported serious quarreling, fighting, residence absence) were more likely to have abnormal cortisol profiles than children living in more amiable families were. Figure adapted from Flinn & England, 1997.

with family trauma. Some children had significantly elevated cortisol levels during some episodes of family trauma but not during others. Cortisol response is not a simple or uniform phenomenon. Numerous factors, including preceding events, habituation, specific individual histories, context, and temperament, might affect how children respond to particular situations.

Nonetheless, traumatic family events and social emotions such as guilt and shame (Flinn, 2006c) were associated with elevated cortisol levels for all ages of children more than any other factor that we examined. These results suggest that family interactions were a critical psychosocial stressor in most children’s lives, although the sample collection during periods of relatively intense family interaction (early morning and late afternoon) may have exaggerated this association.

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Cortisol (standardized)

1

.5

0

–.5 Nuclear Nuclear father abs > 50%

Single mother

Single mother + kin

Grand Grand mother parents

Step father

Step Distant father, relatives half-sibs

Household composition

FIGURE 3. Household composition and average cortisol levels of children. Vertical lines represent 95% confidence intervals (1.97 × SE). Figure adapted from Flinn, 1999.

Children residing in bi-parental, single mother with kin, and grandparental households have moderate cortisol levels (Figure 3), with a higher proportion of elevations occurring in the context of positive affect situations such as competitive play, physical work, and excitement regarding novel situations.

Although elevated cortisol levels are associated with traumatic events such as family conflict, long-term stress may result in diminished cortisol response. In some cases, chronically stressed children had blunted response to physical activities that normally evoked cortisol elevation. Comparison of cortisol levels during “nonstressful” periods (no reported or observed crying, punishment, anxiety, residence change, family conflict, or health problem during the 24-hour period before saliva collection) indicates a striking reduction and, in many cases, reversal of the family environmentstress association (Flinn & England, 2003). Chronically stressed children sometimes had subnormal cortisol levels when they were not in stressful situations. For example, cortisol levels immediately after school (walking home from school) and during noncompetitive play were lower among some chronically stressed children (cf. Long, Ungpakorn, & Harrison, 1993). Some chronically stressed children appeared socially “tough” or withdrawn and exhibited little or no arousal to the novelty of the first few days of the saliva collection procedure. These subnormal profiles may be similar in some respects to those of individuals with Post-Traumatic Stress Disorder (e.g., Yehuda, Engel, Brand, Seckl, Marcus, & Berkowitz, 2005).

Although elevated cortisol levels in children are usually associated with negative affect, events that involve excitement and positive affect can also stimulate stress response (Flinn, 2006c). For example, cortisol levels on the day before Christmas were more than one standard deviation above normal, with some of the children from twoparent households and those having the most positive expectations exhibiting the

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highest cortisol (Flinn, 2006e). Cortisol response appears sensitive to social challenges with different affective states. Other studies further suggest that the cognitive effects of cortisol may vary with affective states, such as perceived social support (Ahnert et al., 2004; Quas, Bauer, & Boyce, 2004).

There are some age and sex differences in cortisol profiles, but it is difficult to assess the extent to which this is a consequence of neurological differences (e.g., Butler, Pan, Epstein, Protopopescu, Tuescher, Goldstein, Cloitre, Yang, Phelps, Gorman, LeDoux, Stern & Silbersweig, 2005), physical maturation processes, or the different social environments experienced, for example, during adolescence as compared with early childhood (Flinn, Turner, Quinlan, Decker, & England, 1996; Flinn & Quinlan, in preparation). For instance, young adult women have a higher incidence of depression and associated abnormal cortisol profiles than children or young men in this community.

The emerging picture of HPA stress response in naturalistic context from the Dominica study is one of sensitivity to social challenges, consistent with clinical and experimental studies. The results further suggest that family environments are an especially important source and mediator of stressful social challenges for children. In the next section, data on the longitudinal effects of early traumatic experiences are examined to assess the domain-specificity of changes in stress response.

Ontogeny: The Early Trauma → HPA Dysfunction Hypothesis “. . . the development of individual differences in behavioral and neuroendocrine responses to stress can be influenced by events occurring at multiple stages in development . . .” (Francis, Diorio, Plotsky, & Meaney, 2002)

Early experiences can have profound and permanent effects on stress response.

Exposure to prenatal maternal stress, or prolonged separation from mother in rodents and non-human primates, can result in lifelong changes in HPA stress response (Maccari et al., 2003; Meaney 2001; Suomi, 1997; cf. Levine, 2005). Research on the developmental pathways has targeted the homeostatic mechanisms of the HPA system, which appear sensitive to exposure to high levels of glucocorticoids during ontogeny.

Glucocorticoid receptors (GRs) in the hippocampus that are part of the negative feedback loop regulating release of CRH and ACTH can be damaged by the neurotoxic levels of cortisol associated with traumatic events (Sapolsky, 1990b, 2005). Hence early trauma is posited to result in permanent HPA dysregulation and hypercortisolemia, with consequent deleterious effects on the hippocampus, thymus, and other key neural, metabolic, and immune system components (Mirescu et al., 2004; Zhang, Parent, Weaver, & Meaney, 2004). These effects have additional consequences resulting from high density of GRs in the pre-frontal cortex in primates (DeKloet, Oitzl, & Joels, 1999; Patel, Lopez, Lyons, Burke, Wallace, & Schatzberg, 2000; Sanchez, Young, Plotsky, & Insel, 2000).

Finer-grained analysis of the epigenetic mechanisms involved with maternal effects on glucocorticoid negative feedback on CRH release indicates that DNA methylation affects hippocampal GR exon 17 promoter activity (Weaver et al., 2004). The

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Cortisol (standardized)

1.0

18 24

9 0

57

No EFT

in utero

0–3

3–6

Age of first major trauma

FIGURE 4. Children exposed to early family trauma in utero or post-natal have higher average (means for each child) cortisol levels at ages ten and above than children who were not exposed to early trauma (no EFT). Sample sizes (# of children) are in bars.

Vertical lines represent 95% confidence intervals. Figure adapted from Flinn, 2006b.

permanence of DNA methylation, set during a sensitive period in the first week after birth in the rat, is a mechanism connecting diminished maternal care (e.g., licking, grooming, and arched-back nursing) with long-term elevations of HPA stress response.

The specific mechanisms affecting relations between exposure to trauma early in development and subsequent HPA system function in humans are not as well documented as in animal studies. Nonetheless, a similar causal linkage appears plausible (e.g., Essex, Klein, Cho, & Kalin, 2002; Heim et al., 2000; Lupien et al., 2005; O’Conner, Heron, Golding, Glover, & ALSPAC study team, 2003; Teicher, Andersen, Polcari, Anderson, Navalta, & Kim, 2003). Children in the Bwa Mawego study who were exposed to the stress of hurricanes and political upheavals during infancy or in utero do not have any apparent differences in cortisol profiles in comparison with children who were not exposed to such stressors. Children exposed to the stress of parental divorce, death, or abuse (hereafter “early family trauma” or EFT), however, have significantly higher cortisol (Figure 4) levels at age ten than other children. EFT children also have higher morbidity than non-EFT children (Flinn, 2006b). Based on analogy with the non-human research discussed previously, two key factors could be involved: (1) diminished hippocampal GR receptor functioning, resulting in less effective negative feedback regulation of cortisol levels; and (2) enhanced sensitivity to perceived social threats, perhaps as a consequence of lower social competencies. Children usually elevate cortisol in response to strenuous physical activity, but rapidly return to normal levels (Figure 5). If EFT has affected the negative feedback loop, then recovery to normal cortisol levels would be slower. Resumption of normal cortisol levels after physical stressors, however, appears similar regardless of early experience of family trauma (Flinn, 2006b). Cortisol profiles following social stressors, however,

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Cortisol (Âľg/dl)

.75

.50

.25

0 7:00 AM

12:00 PM

5:00 PM

FIGURE 5. Ten-hour cortisol profile of a 12-yearold boy. Note elevation of cortisol levels at 10:00â&#x20AC;&#x201C; 10:30 AM when he was helping his father carry wood.

indicate that EFT children sustain elevated cortisol levels longer than non-EFT children (Flinn, 2006b).

The enhanced HPA stress response of children in this community that were exposed to EFT appears primarily focused on social challenges, suggesting that the ontogenetic effects of early trauma on stress response may be domain-specific and even context-specific. These results are consistent with studies of the effects of social defeat with non-human models (e.g., Kaiser & Sachser, 2005). In the following section we examine the effects of close grandparental relationships on the stress response of EFT children.

Ameliorative Effects of Grandparental Care on the Ontogeny of Stress Response Review of analyses of data in the previous section indicate that early family trauma is associated with higher cortisol levels among children in this community. The different cortisol response patterns to social and physical stressors suggest that domainspecific mechanisms have been affected. In this section we examine whether close relationships with grandparents during early childhood are associated with individual differences among EFT children in several outcome measures. The general hypothesis is that grandparental care (GPC) reduces psychosocial stress for grandchildren. The negative effects of early family trauma on child development are therefore expected to be moderated by GPC, as measured by cortisol levels, growth, and morbidity.

EFT children with high (above median) levels of GPC have lower average cortisol levels (Figure 6a), lower morbidity (Figure 6b), and higher growth percentiles (Figure 6c), than EFT children with low GPC. EFT children that have high rates of grandparental care (GPC), however, do not have lower average fluctuating asymmetry (FA)

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Cortisol (standardized)

1.0

0

Controls (N = 57)

EFT children w/high GPC (N = 28)

EFT children w/low GPC (N = 23)

FIGURE 6a. EFT children with high grandparental care (GPC) have lower average cortisol levels than low GPC EFT children. Vertical lines represent 95% confidence intervals.

% days ill, (standardized)

10

1.0

0

Controls (N = 57)

EFT children w/high GPC (N = 28)

EFT children w/low GPC (N = 23)

FIGURE 6b. EFT children with high grandparental care (GPC) have lower average morbidity levels than low GPC EFT children. Vertical lines represent 95% confidence intervals.

(Figure 6d) or lower gastrointestinal parasite loads (Figure 6e) than EFT children with low GPC. These results suggest that grandparental care may substantially ameliorate some of the negative consequences of difficult family environments. These findings are generally consistent with our subjective impressions from watching these children over nearly two decades: that grandparental relationships are often of great importance

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Growth percentile

50

40

Controls (N = 57)

EFT children w/high GPC (N = 28)

EFT children w/low GPC (N = 23)

Fluctuating asymmetry (%)

FIGURE 6c. EFT children with high grandparental care (GPC) have higher average growth percentiles than low GPC EFT children. Vertical lines represent 95% confidence intervals.

2.5

2.0

Controls (N = 57)

EFT children w/high GPC (N = 28)

EFT children w/low GPC (N = 23)

FIGURE 6d. EFT children with high grandparental care (GPC) do not have lower levels of fluctuating asymmetry (FA) than low GPC EFT children. Vertical lines represent 95% confidence intervals.

for the development of emotional regulation, social skills, and self-confidence, especially for children in difficult family environments. What the specific mechanisms are, and whether the effects are direct or indirect via support to the childâ&#x20AC;&#x2122;s mother, are not discernable from these analyses.

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Parasite loads (%)

40

20

Controls (N = 57)

EFT children w/high GPC (N = 28)

EFT children w/low GPC (N = 23)

FIGURE 6e. EFT children with high grandparental care (GPC) do not have lower levels of parasite loads than low GPC EFT children.

Conclusions Grandparental care appears to be a significant mediator of HPA stress response and associated growth and health problems among children that have experienced early family trauma. Our observations suggest that maternal grandmothers are especially important mediators, (Quinlan & Flinn, 2005), although a variety of other kin (e.g., aunts, siblings, grandfathers) may also contribute, and in special cases, may be primary caregivers (Flinn & Leone, 2006). These results are likely to be specific to the context of the kin networks of this community (e.g., see Quinlan & Flinn, 2003), and are likely to vary contingent on the specific patterns of kinship, although grandparentgrandchild relationships appear to be broadly important (Lahdenpera et al., 2004; Sear et al., 2000; Voland & Biese, 2002). These results are consistent with the hypotheses that the importance of grandmothers in human evolution may involve their role as providers of social information (e.g., emotional comfort, social competencies, traditions) (Coe, 2003) in addition to providing calories and protection (Alexander, 1974; Hawkes, Oâ&#x20AC;&#x2122;Connell, Blurton Jones, Alvarez, & Charnov, 1998).

Returning to the paradox of why natural selection favored sensitivity of stress response to social stimuli in the human child, several points emerge. Human childhood is a life history stage that appears necessary and useful for acquiring the information and practice to build and refine the mental algorithms critical for negotiating the social coalitions that are key to success in our species. Mastering the social environment presents special challenges for the human child. Social competence is difficult because the target is constantly changing and similarly equipped with theory of mind and other cognitive abilities. Results from the Dominica study indicate that family environment, including care from grandparents, is a primary source and mediator of stressful events

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in a child’s world. The sensitivity of stress physiology to the social environment may facilitate adaptive responses to this most salient and dynamic puzzle, aided by information and security provided by effective parental and grandparental care.

Children lacking such care may be at a disadvantage in developing the social competencies necessary for coping with social challenges, and consequently may be at increased risk for problems ranging from dysregulation of emotional control and increased risk of psychopathology (Gilbert, 2001; Nesse, 1999), to broader health issues associated with social and economic disparities (Adler, Boyce, Chesney, Cohen, Folkman, Kahn, & Syme, 1994; Dressler et al., 2005; Marmot & Wilkerson, 1999). The potential for intergenerational cycles that perpetuate social relationships that affect stress (Belsky, 2005; Belsky, Jaffee, Sligo, Woodward, & Silva, 2005; Fleming, Kraemer, Gonzalez, Lovic, Rees, & Melo, 2002; Fleming, O’Day, & Kraemer, 1999; Francis, Diorio, Liu, & Meaney, 1999; Maestripieri, Lindell, Ayala, Gold, & Higley, 2005) and poor health are especially concerning. Under such circumstances, grandparents helping their grandchildren cope with difficult events involving their parents, intervening during times of critical need and stabilizing development, may be of critical importance (e.g., Lussier, Deater-Deckard, Dunn, & Davies, 2002).

We are still far from identifying the specific mechanisms linking stress response to the ontogenetic plasticity of components of the limbic system and pre-frontal cortex that are involved with the acquisition of social competencies. An evolutionary developmental perspective can be useful in these efforts to understand this critical aspect of a child’s world by integrating knowledge of physiological causes with the logic of adaptive design by natural selection (Worthman, 1999). It reminds us that our biology has been profoundly affected by our evolutionary history as fundamentally social creatures, including, perhaps, a special reliance upon grandparents. Indeed, the mind of the human child may have design features that enable its development as a group project, guided by the multitudinous informational contributions of its ancestors and co-descendants. Children without grandparental input may find themselves in worlds that are more stressful because they lack the advice, traditions, good humor, soft laps, and hugging arms by which to understand them.

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The Development of Spontaneous Gestures in Zoo-living Gorillas and Sign-taught Gorillas: From Action and Location to Object Representation Joanne E. Tanner Scottish Primate Research Group, and Collaborator, Centre for Social Learning & Cognitive Evolution, School of Psychology University of St. Andrews, Scotland

Francine G. Patterson The Gorilla Foundation/Koko.org Woodside, California

Richard W. Byrne Centre for Social Learning & Cognitive Evolution, Scottish Primate Research Group, School of Psychology University of St. Andrews, Scotland rwb@st-andrews.ac.uk

Abstract: We analyze the developmental sequence in which different types of representation appear in untaught signs in the repertoire of Koko, a signing gorilla, and in the gestures developed by zoo-living gorillas at different ages. There is a progression in all the subjects from pure action to iconic representation of action. The signing gorilla, in addition, depicts objects. This is done through hand shape, miming of an action related to the use of an object, or by tracing the outline of an object. The various spatial mediums (i.e., on the body versus in open space) in which signs are performed assist in understanding of the cognitive processes supporting ape representation and communication. The progression from ape “action mapping” to the level of representation found in human language is viewed as a series of stages that follow logically upon each other in a continuum of development, both in individuals and in possibly in the history of the hominoid family.

Introduction Research in recent decades has shown that zoo-living apes create gestures other than the obviously species-typical, and signing apes regularly employ signs that they have themselves created, in addition to taught signs. We explore the relationship of spontaneous gestures by zoo-living gorillas to those created by a sign language-taught gorilla.1 1. In this paper we will use the word “sign” for human sign language taught to apes, and also for gestural inventions by signing apes. “Gesture” refers to inventions by zoo gorillas.

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Particular attention is given to the development of iconic gestures because they require a type of understanding that can be linked to human representational abilities.

Here we define an iconic sign or gesture simply as one that depicts a physical aspect of its referent. Zoo-living gorillas use iconic gestures for actions anticipated or desired (Tanner & Byrne, 1996, 1999); in both species of chimpanzee as well, iconic gestures have been observed both in untaught captives (Kohler, 1925; Yerkes, 1943; Hayes, 1951; Savage-Rumbaugh, Wilkerson, & Bakeman, 1977) and chimpanzees trained in symbol systems other than sign language2 (Savage-Rumbaugh, 1986; Greenfield & Savage-Rumbaugh, 1990, Savage-Rumbaugh & Lewin, 1994). Signing apes also create novel iconic signs; unlike zoo captives, they spontaneously create signs to represent objects for which they have not been taught signs, and use such invented, untaught signs repeatedly and consistently (Gardner & Gardner, 1971; Patterson, 1980; Patterson & Cohn, 1990; Miles, 1978, 1993; Miles, Mitchell, & Harper, 1996). The usage of iconicity can be traced in the chronological development of gestures in individual gorillas, and the forms the iconicity takes and what it represents are important keys to understanding ape cognition.

We survey signs Patterson and Cohn (1990) list as invented by Koko during her first ten years of sign language instruction, with particular attention to those that appear to be iconic, and we note the types of iconicity that Koko uses and make comparisons with zoo gorillas’ gestures. We assess modes of representation in terms of their order of appearance in Koko’s individual development, and compare the developmental progression and age of appearance of similar gestures in zoo gorillas. We consider the spatial media in which gestures and signs are produced. We compare the usage of those gestures or signs that take the same form in both zoo gorillas’ and Koko’s usage to learn whether their “meanings” or functions are universal or variable. Though the gestures of gorillas have not been extensively studied by other researchers until very recently, where possible we incorporate any relevant data from other gorillas in zoos or the wild.

Subjects Only two gorillas have been extensively taught a human sign language: Koko (a zoo-born female lowland gorilla) and Michael (a wild-born male lowland gorilla, now deceased). Koko resides at the Gorilla Foundation in Woodside, California. Koko was born at the San Francisco Zoo on July 4th, 1971, and is the full sister of Kubie, a principal subject of the first author’s zoo observations. Koko’s exposure to American Sign Language (ASL) and constant interaction with human companions began at the age of one year under the tutelage of the second author, Francine Patterson, who was at the time a graduate student at Stanford University. Koko was simultaneously exposed to a variant of American Sign Language and human (English) speech. Further detail of the education of gorillas Koko and Michael and the entire ongoing project can be found in Patterson (1978, 1979, 1980), Patterson & Linden (1981), Patterson & Cohn (1990), Patterson & Gordon (1993, 2002), and Bonvillian & Patterson (1993, 1999).

2. Because the researchers working with these apes do not describe their gestures in physical detail, they cannot be compared with those of signing apes or apes not taught a symbol system.

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Information regarding the gestures of zoo-living gorillas is drawn primarily from Tanner & Byrne’s long-term study of the gorilla group at the San Francisco Zoo (Tanner 1998, 2004; Tanner & Byrne 1993, 1996, 1999). See www.gorillagestures.info for video examples of the San Francisco Zoo gorillas’ gestures and more about the research on the gorilla group there. From 1988 until 1997 observations were made outdoors at the San Francisco Zoo one morning each week for approximately three hours, conditions permitting. Further observations, on a less regular basis, have continued until this writing. The study team consisted of the first author and the camera operator, Charles L. Ernest. The general procedure was to videotape all social interaction continuously wherever it was possible to use the video camera. Later, videotape was analyzed and gestures were cataloged into a Filemaker™ database. As a working definition, the term “gesture” applied to all discrete, non-locomotor limb and head movements that appeared to be potentially communicative, regardless of receptive sensory modality.

The subjects, the gorillas at the San Francisco Zoo, are members of a stable social group; all of them have spent nearly all of their lives at this zoo. The San Francisco Zoo’s present gorilla enclosure has been this group’s home since 1980. It has an outdoors area of 2300 square meters, or 38 by 50 meters at maximum parameters. It is covered with grass and other vegetation and contains large, climbable live trees as well as several dead trees, large stumps, and two artificial rock hills including arches and cave-like areas.

The group at the time of the beginning of the study included first- and secondgeneration descendants of the wild-caught founder, Bwana, who had been at the zoo since 1958. A wild-caught female, Pogo, human-reared in her early years, grew up at the zoo with Bwana and is of about the same age. Two young females whose early rearing was by humans in zoo nurseries, Bawang and Zura, joined the group in 1981 and 1982 respectively, after the deaths of two older females. Bawang is the mother of Kubie’s offspring, Shango, Barney, and Nneka, who have all been mother-reared.

Bawang was always Kubie’s preferred mate, but when she was pregnant or involved in caring for her first infant, Kubie switched his attentions and play activity to the younger female, Zura. All of these gorillas have been subjects of the Tanner and Byrne studies, but the interaction between Kubie and Zura received the most intense analysis; by far the greatest amount of gesturing was done by these two gorillas.

Untaught Signs by Koko and Michael Most of Koko’s and Michael’s earliest taught sign language vocabulary that reached formal criteria3 of consistent usage was composed of iconic signs, in contrast to the vocabulary of deaf children. As the gorillas’ vocabularies increased, the proportion of 3. Two sets of criteria were used: the Emitted criterion accepted as a vocabulary item each use of a recognizable sign used spontaneously in an appropriate context; the Patterson criterion accepted a sign only if it was observed and recorded by two different observers to be used appropriately and spontaneously on at least half the days during a period of a month. By the end of ten years, Koko had acquired 876 words by the Emitted criterion, 290 words by the Patterson criterion. The spontaneously invented signs discussed in this paper all met the Emitted criterion.

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iconic signs decreased, though it remained higher than that of the human children studied by Bonvillian and Patterson (1993). Bonvillian and Patterson, however, acknowledge that the design of their study does not allow us to discern the influences from humans on the content of taught sign vocabulary. Also some taught iconic signs may represent aspects of the referent that would not be recognized by the learner as iconic.

Here we will look only at signs that were created by the gorillas that were not part of their taught American Sign Language vocabulary.

In summarizing the first ten years of Koko’s vocabulary development, Patterson and Cohn (1990) list Koko’s entire vocabulary during these ten years and indicate which of those signs were not taught, but used spontaneously by the gorilla. These spontaneous creations were not a result of deliberate human reinforcement of chance novelty; untaught signs were often not initially comprehended by Koko’s human companions and were ignored or misunderstood until repeated context made the meaning clear. Thus Koko’s untaught signs can be expected to be free from human influence in choice of referents. In some cases, the inventions were for actions, objects, or concepts for which Koko had not been taught a sign; others were for actions, objects, or concepts for which she had been taught a sign but for which she strongly seemed to prefer her own usage. Once acknowledged by humans as part of her vocabulary, untaught signs were neither discouraged nor encouraged, but simply accepted as part of Koko’s repertoire of signs. (It is, of course, possible that humans have failed to understand and interpret some of Koko’s signs. Also, because iconic signs are easier for us to attempt to translate, they might be over-represented in summarizing Koko’s vocabulary.)

We categorize, according to type of iconicity or other form of reference, fifty signs that Patterson and Cohn (1990) characterized as “invented” by Koko. This was done with the help of an unpublished, internal-use video created by Dr. Francine (Penny) Patterson and Darlene Chan for Gorilla Foundation employees, unpublished lists of Koko’s sign lexicon, published physical description of earliest signs (Patterson, 1978), as well as the first and second authors’ personal experience and knowledge of Koko’s signing. Not included are those listed as “natural” (Patterson & Cohn’s term for signs or gestures they suspected to be species-typical) or “modulated or compounded” (modulated means modifying the taught articulation of a sign; compounded means combining aspects of taught signs to form a new sign). The total corpus of 50 signs, with descriptions and categories, is included as an appendix. Table 1 summarizes the referential categories of Koko’s untaught signs, and Table 2 their types of iconicity or other modes of depiction. Plate 1 illustrates some of Koko’s untaught signs.

Table 1. Referents of Koko’s Untaught Signs (First 10 Years) Total invented signs Signs for objects Signs for actions Other signs

50 27 17 6 (2 for qualities, 2 for states of attention, 2 deictic [pointing])

54% 34% 12%

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Table 2. Types of Representation Used by Koko Note that the categories of iconic representation of object shape and action are not mutually exclusive: there were a few signs that involved elements of both.

Total signs using iconic mode of description

38

76% of total untaught signs

Signs depicting action iconically but not necessarily representing an action; may represent an object by depicting action on or with that object.

27

54% of total untaught signs

Signs depicting shape of an object iconically

15

70% of iconic untaught signs 30% of total untaught signs 40% of iconic untaught signs

Browse

Eye makeup

Frown

Unattention

Bite

Hair barrette

Plate 1. Some of Kokoâ&#x20AC;&#x2122;s untaught signs

Of Kokoâ&#x20AC;&#x2122;s untaught signs during the first ten years of her life, approximately half represented objects and another third, actions (Table 1). Three-quarters of her untaught signs involved an iconic mode of depiction (Table 2). Among these, approximately 70% involved depiction of action, either of an action itself or of a customary action upon an object. Though these untaught signs were predominantly signs for objects, more than half of these objects were not represented by depicting their shape, but by an action performed upon or with them. For instance, modeling clay was signed by a motion of rolling the palms together, as when rolling out clay; a hand puppet by

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the motion of putting the puppet on the hand. Some action mimes listed as representing objects might seem to be just as well translated as signs for actions, not for objects. However, Koko often used them to request the object in question (by accompanying pointing or reaching with eye contact), thus indicating that an object was the referent of the action.

In some cases the signs might be interpreted either way; in American Sign Language, many signs can represent either an object or an action depending on repetition and other differences in production. An action can refer to an object, and an object depiction may be part of an action request. Also, the categories of action and object depiction are not necessarily mutually exclusive because it is possible to indicate a shape and also an action in a single sign. An example is Koko’s sign for dental floss, where Koko picked her teeth with an index finger (untaught), and then made the taught sign for thread, which traces the shape of dental floss.

About 40% of Koko’s untaught iconic signs represented an object by depicting an element of the shape of the object. Since it is usually impossible to represent the entirety of an action or an object with the hands, a salient aspect must be chosen to represent it. Such condensation of depiction is an aspect of both ape and human signing.

Koko’s specific choices of forms of metonymy, i.e., representing an object or action by depicting just a part of it, will not be the focus here though well worthy of further study. (A description of the form of each untaught sign can be found in the Appendix.)

Here we consider metonymic signs simply as iconic. Because our primary interest here is the cognitive processes leading to the physical representation, we consider a sign that describes any part of the physical form of an action or object to be the result of some kind of process of iconic representation. Koko’s means of representation are discussed in detail later in the section entitled “Koko’s Modes of Invention.”

Some of Koko’s untaught signs were not iconic. One was a deictic (pointing) sign that indicated the location of an object (Koko’s early “notice” sign, glossed as bird at the time because she co-opted elements of this taught sign and used it in a deictic manner). Another sign simply located a referent on the self (e.g., body hair indicated by grasping hair between the fingers). Koko also created signs that involved cross-modal transfer of English sounds to a sign;4 for instance, blowing forcefully at someone to express that they “blew it,” that is, performed an action she wasn’t pleased with (she was quite familiar with the colloquial expression, frequently used in the spoken English of her companions, often to scold her). In this case, the “sign” is itself a sound, accompanied by characteristic body posture and facial expression. Some inventions were “blended” from several taught signs (e.g., apricot = the sign for peach made with an “A” hand shape like apple). A few were of unknown or indiscernible origin (like Koko’s lip in reference to human females, performed by rubbing an index finger horizontally on her lips).

4. A study of Koko’s response to alterations in vowels or consonants in spoken words illustrated that Koko can accurately perceive the sounds of human speech (Goodreau, Patterson & Tam, 1996; Patterson & Goodreau, 1987; Goodreau, 1987).

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Another frequent element of Koko’s untaught signs, as well as of taught signs she has altered to her personal preference, is locating them on her body as opposed to forming them in space away from the body. Of her untaught signs, 60% were placed on the body location of the referent.

Michael, Koko’s male gorilla companion, also used untaught signs, and Koko subsequently adopted some of these for her own use. Untaught signs originated by Michael but co-opted by Koko during the first ten years of the project were hit-inmouth, hit-in face, and pull-out-hair, all mimes of the described actions.

From Action to Object in the Creation of Gestures and Signs: Zoo Gorillas and a Signing Gorilla Compared Action and location, the preferred ways of depiction in Koko’s untaught signs, are also frequently used in gestures of the gorillas observed at the San Francisco Zoo (Tanner & Byrne, 1993, 1996, 1999) to communicate about features of behavior and the environment. For both signing and non-signing gorillas, action and location (as the beginning or ending point of action) seem to be the basic building blocks for expression. It is a short journey from describing an action or indicating a location to describing an object, because the action and location of an object can be employed in describing it gesturally, as in many of Koko’s inventions; and the outlining of action is not far from the action of outlining an object.

Zoo gorillas have been observed to create depictions of action of the self or another gorilla, and gestures of similar types have, though very rarely, been observed in the wild (Schaller, 1963). Gorillas in the wild have been observed to enact actions anticipated of the self or desired of others; zoo gorillas have been observed to trace the trajectory of such actions on another’s body or in space.5 Captive studies (Tanner 1998; Tanner & Byrne 1999) give the approximate ages at which different classes of gestures appear (see Table 3).

Table 3 illustrates the progression in taught and untaught gorillas from depiction purely of action, to object depiction with signs or gestures. The developmental progression of sign invention by Koko can be found in records of her first untaught signs (Patterson, 1980); Table 3 is thus ordered chronologically. The chronology for zooliving gorillas and gorillas in the wild is less precise because of more limited observation. Only one earliest example is given for each class of depiction in Table 3; in most cases there were other examples of each class, and in the discussion following, some of these are mentioned. Additional signs for each classification can also be found in the descriptions in the Appendix. For some categories “invented” signs by Koko are not found in available records but instead are listed as “natural” gestures in an earlier study. The dividing line between “natural” gesture and “invented” sign cannot be a

5. There have also been some observations in the wild, such as those found in Schaller (1963) and Robert Campbell’s unpublished film for Dian Fossey at the National Geographic Society (viewed in entirety by the first author), that can give us an idea of at what stage mountain gorillas in their native environment make certain kinds of gestures.

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Table 3. From Actions to Objects in Gesture and Sign Invention: First Appearances of Different Kinds of Representation.

What sign or gesture describes or indicates

How produced

location touch indicated to location other

Where formed

on an object (other than self or other gorilla)

Example (English gloss)

Physical description

knock

fist contacts object such as rock or tree; eye contact and response waiting to other gorilla

that

index finger or fingers contact object

Zoo, wild gorillas, earliest age observed to be used

Signing gorilla, age in years and months when first used or invented

zoo age 7

knocks, age 1 but not to indicate location to other

not seen

1.0

location extend indicated to finger other toward location

in space

that, there

index finger extended from hand toward location

not seen

1.0

action upon enacted self desired from other

in space

up

arms raised to request or anticipate being picked up by adult

zoo age 1; wild infant

1.0

action desired of other

enacted non- on other’s forcefully body

move away

light push to other’s body

zoo age 2; wild adults

1.0

action desired of other

mimed

on own body

tickle

index strokes underarm or sole of foot

not seen

1.2

action desired of other

traced

on body of other

turn around

on other’s waist, arm zoo age 7 moves from one side of body to other

1.11

object

hand shape, location

on own body

bracelet, hand puppet

cupped hand pats wrist

not seen

2.8

action desired of other

traced

in space

away, go

arm swept toward other

zoo age 6; 2.9 wild all ages

action upon enacted other anticipated

on own body

bite

biting self on hand or wrist

zoo age 7; wild juvenile

object

action on or of an object mimed

with hands in space in front of body

clay

flat hands, top hand not seen moves back and forth over other palm

3.8

negation

altering facial expression

on own body

Frown (KOKO)

manipulate face

zoo age 7

4

tracing of shape of object

on own body

eyeglasses

index fingers trace lines from eyes to back of ears

not seen

6.1

object

2.10

cover up face with hide playhands face (ZURA)

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Table 3. (Continued)

What sign or gesture describes or indicates

How produced

Where formed

Example (English gloss)

Physical description

Zoo, wild gorillas, earliest age observed to be used

Signing gorilla, age in years and months when first used or invented

location on touch self location indicated to other

move arm in space, to location on own body

armswing under (walk up bottom)

arm swings from zoo age 7 space in front of body to between legs

6.4

object

formed by static hand shape only

in space

pickle

thumb and index extended from both fists held in space in front of body

not seen

7+

object

tracing of shape of object

in space

thread

two little fingers touch then move apart horizontally

not seen

(used only when taught by humans)

Observations of gestures in the wild come from the following sources, but primarily the publications of George Schaller and Dian Fossey: Baumgartel, 1976; Burbridge, 1928; Campbell unpublished film; Denis, 1963; Fay, 1989; Fossey, 1979, 1983; Mori, 1983; Schaller 1963/1976, 1964.

Sources: Patterson (1980); Patterson, Tanner & Mayer (1987); Patterson & Cohn (1990); Tanner (1998) Arranged chronologically by order of appearance in signing gorilla.

firm one, as learning and genetics are so entwined for any behavior and further, since we do not have good observations of behavior for all groups of gorillas, especially in the wild. A better designation, which we use throughout, is simply between humantaught and untaught signs.

Koko’s earliest recorded untaught signs were listed as “natural” signs, though her standard deictic sign, pointing with the index finger, has not been reported in untaught gorillas. Further untaught signs seen early in the first year of instruction (age 12–24 months) were up, requesting an action upon the self by another; and tactile signs such as a light push to another, indicating move away. By the end of the year a tactile sign using a tracing motion on another’s body appeared, requesting a companion to turn around.

Gorillas at the San Francisco Zoo have been observed to use all the “natural” untaught gestures performed by Koko in her first year of sign instruction, except for pointing with the index finger. Later in development knock or pound (using the fist) and slap (open hand) are used by zoo gorillas to touch objects in a clearly deictic fashion, with eye contact and waiting for response from the partner gorilla.6 Such usage was observed repeatedly in a 7-year-old gorilla and her older play partner but may appear earlier; Tanner’s zoo observations began when the younger of her principal subjects was already age 7. Subsequent observations of younger zoo gorillas by Tanner and others 6. See Leavens, Hopkins, & Bard, (1996), Leavens & Hopkins (1998, 1999), for discussions of variability of form in pointing by chimpanzees. The development of pointing in human children and the criteria for social pointing have been discussed by many scholars, for instance Butterworth (1996) and Bates, Benigni, Bretherton, Camaioni, & Volterra (1979).

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(Pika, Liebal, & Tomasello, 2003) did not find such referencing, however. Likewise, tactile gestures on another’s body, requesting directional movement of the other gorilla, were rarely seen in zoo gorillas until age 7.7 Miming on the gesturer’s own body of the specific action desired of another was not observed at all in zoo gorillas.

The earliest untaught signs recorded as invented by Koko are blow and tickle, which depicted actions desired of another and appeared during her second and third months of sign instruction, when she was just over a year old. The earliest appearance of blow was putting her index finger to another’s mouth when the person stopped blowing, perhaps simply pointing; Koko appeared to want the person to continue blowing.

Koko then began to request the action “blow” by holding a finger up to her own mouth, transferring the features of another’s body to her own. Tickle was likewise indicated by miming the action desired of another on her own body. Her next sign was a deictic sign, performed with two index fingers held together at the tips. This sign was directed toward interesting objects out of reach, but was glossed bird because it incorporated elements of a bird sign a teacher first used. Subsequently, however, Koko employed it for many referents other than the bird the teacher had originally been pointing out.

Koko’s next type of untaught sign did not appear until over a year later, during which time her taught ASL signing progressed rapidly. This sign, at age 2 years 8 months, was bracelet, performed by a cupped hand patting the wrist, first used requesting a new bracelet she was shown. This was her first sign created for an object, and involved an iconic hand shape depiction as well as contacting the part of her own body where the object usually was worn, thus perhaps involving a tactile element as in earlier signs such as tickle. She later extended the use of the bracelet sign, referring to a hand puppet on a companion’s hand as well as using the sign for bracelets. This seems to be an extension of the ability to point out location to another, which Koko did at the age of just one year. It is requesting “something on my body, wrapped around this location.” A zoo gorilla (Kubie) comes close to this in a unique observation when he pats his shoulders, with eye contact, in interaction with another gorilla (Zura), resulting in her approaching Kubie and placing her hands on his shoulders (Tanner & Ernest, 1989).

Koko’s next untaught sign, bite, appeared at age 2 years 10 months (see Plate 1).

She placed the side of her hand or index finger in her mouth to request biting play from a companion. A similar gesture has been observed in both free-living and zoo juvenile gorillas and the first author has observed it in captive monkeys where a play partner was not physically available. Like Koko’s earliest untaught signs, bite reproduced the action desired of another, on her own body. Around the same time, another untaught sign, away or go, appeared. It differed from the earlier sign, up, in that it depicted in space motion desired from another, not motion anticipated for the self. A similar gesture was used by zoo gorillas from age 6, and has been seen in the wild.

At age 3 years, 8 months, a new type of depiction appeared: Koko’s sign for clay.

Koko requested clay by miming the customary action performed on the object, rolling a

7. Tactile gestures consisting of reaching, stretching and touching are seen early on (also in gorillas studied

by King, 2004) but not tracing a path of action or suggesting motion in a certain direction as found in older gorillas by Tanner and Byrne (1999).

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ball of clay between the hands. This could be interpreted as depicting the activity of playing with clay rather than the object itself, but Koko used such signs to request objects.

During Koko’s first five years, all her iconic inventions reproduced action of or upon an object, or objects were indicated by simply placing an appropriate hand shape on her body. No signs depicting an object or its action have been observed in zoo gorillas.

At age 6 years a new mode of depiction appeared for Koko: tracing the shape of an object. Koko created a sign for eyeglasses where index fingers traced a line from the eye to the back of the ears. Eventually, Koko produced a total of 15 inventions describing objects that involved depicting the shape rather than the action of an object (see Appendix). A form of active “tracing” of the form of an object was used in five cases; in ten cases, her depictions of shape were produced instead by a descriptive hand shape (e.g., extended finger for a straight or narrow object, cupped hand for a rounded object, index and thumb extended for a small rectangular object) placed on an appropriate body location. Among Koko’s 50 inventions from her first 10 years (listed in Appendix), all signs that depicted an action were performed on appropriate body locations, and nearly all that depicted a shape were also performed touching her body. An exception was her later invention at age 7 of a sign for pickle (described in Table 3), with appropriate hand shapes in the space in front of the body. The only category of object representation not found among Koko’s untaught signs during her first ten years is the tracing of an object in space away from the body, though she uses such signs when taught. (Thread, a taught sign used in her untaught compound sign for dental floss, is such a sign).

Also between age 6 and 7, Koko produced a sign glossed walk-up-bottom, requesting her male gorilla companion to touch or tickle her bottom. A similar gesture was frequently observed in zoo gorillas, described as armswing under. For the zoo gorillas as for Koko, this gesture appeared in adolescence. For the zoo gorilla Kubie, this often included a tap to the other gorilla, and then swinging the arm to a location between the legs. His version actually was a phrase that can be glossed as “you come under,” that is, a request to make contact with the gesturer gorilla’s genital area.8 To summarize, the chronological development of modes of representation in Koko’s spontaneously created signs is as follows: 1) (from age 1–2 years) depicting actions on her own body, another’s body, or in space, to represent activity desired of another; and pointing to objects or locations desired or noted 2) (from age 2.8) placing the hand-shape of an object on an appropriate body location, to represent an object or action 3) (from age 3.8) miming an action performed with or on an object in order to represent an object 4) (from age 6) tracing on her body the outline of an object to describe the object 5) (from age 7) tracing a shape in space away from the body or using a hand shape held in space away from the body to describe an object

8. For more about gesture phrases, see Tanner 2004.

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These last two were the rarest of Koko’s means of representing objects, though these methods of depiction are common in American Sign Language and are employed in many of her taught signs.

Development of Gesture in Zoo Gorillas In zoo gorillas, gestures were utilized to depict action or indicate location, as described above for Koko at age 1–2 years onward, but appeared later in the zoo gorillas. Tanner’s zoo observations began when the two principal subjects, Kubie and Zura, were already young adults. The earliest information available on Kubie showed that nearly all his adult repertoire of gestures at age 13 was already present at age 8, in the context of sexual positioning and sexual play with an older and uncooperative female (Keller, 1984). Some play gestures were present at age 2 years. Sue Parker (1999), in a study when Kubie was an infant, lists Kubie’s play “enticements” which include “slapping surface, arm waving, chest beating, foot stamping, tagging, hand clapping, head waggling.” These gestures at age 2 do not appear to include gestures that indicate location or depict directional motion, tactile or otherwise.

A gesture used as a “negative” was seen in the zoo gorilla Zura from age 7; this was hide playface, used to suppress the urge to play and understood by her male play partner, who responded by not approaching (Tanner & Byrne, 1993); other gestures were used as negatives also (Tanner, 2004). Koko at age 4 used a facial alteration, frown, to show annoyance, disgust or negativity toward activities or objects. Later she used an unattention sign, hands covering face, to avoid things she did not want to see or participate in.

Because it was impossible to know whether gestures observed in the adult zoo subjects might originally have appeared earlier, the question of when different kinds of gestures develop was addressed later through observation of two male infants, Shango and Barney, born into the group during the course of the study (Tanner & Byrne, 1999).

Their earliest discrete gestures were audible ones produced by contact with a surface (e.g., ground, rock, tree or own body), actions that were also included in Kubie’s early gestures listed by Parker (1999). They used reaches and arm extensions toward their mother or other gorillas or toward objects of interest that another gorilla possessed, but without the eye contact and response waiting that are hallmarks of real indication.

(However, responses from older gorillas to arm extensions may eventually lead to awareness of their efficacy and establish them as indicating gestures.) New gestures gradually appeared in the older brother, Shango; he began to use a few tactile gestures, but at age 6 still used neither the silent gestures in space nor self-indicating gestures that the young adults used. Barney, the younger brother, began at age 2 to frequently use the armshake gesture observed in his father, but older brother Shango almost never used it. Armshake, by iconically depicting action, may show desire for another gorilla to approach and take play action. Other gestures by adult Kubie indicated approach was desired to various body locations; examples are head nod, armswing under, slap shoulders, and extended palm. Some gestures indicated locations in the environment; such indicating gestures were all observed in gorillas aged 6 years and above. Repre-

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sentation of objects or individuals found in the gorillas’ environment seemed to be absent. In summary, the zoo gorillas, without any human instruction, would depict on their own body, on another’s body, or in space, actions desired from another, and would manually indicate objects or locations of concern, but mostly after age 6. These kinds of gestures were produced by Koko by age 2.

Discussion: Koko’s Modes of Invention Whether the tracing of a shape or use of a “frozen” hand shape is the more abstract method of depiction is an open question, but depiction of an object with hand shape appeared earliest for Koko. The hand shape was placed on the relevant body location, a development that seems to follow on from pointing to locations by touching them.

Tracing would seem to be a more precise or detailed way of mapping a shape. Koko used both tracing and hand shape modes of depiction in taught signs before using similar modes in untaught signs. In both types of signs, the concept of one’s own body as a mirror of something “out there” is necessary. Consistent with this, Koko has shown the ability to use mirrors appropriately (Patterson & Cohn, 1994).

Another aspect of Koko’s untaught signs for objects is that nearly all of her 27 object signs were for referents that she could, and presumably did, touch and handle. The motion, previously experienced, of rolling clay is easily performed when the clay is not in the hands. Another invention, barrette, (see plate) reproduces the motion of touching the length of a barrette (hair clip). Thermometer places a finger under the arm, just like the real thermometer touches the underarm when Koko is given veterinary treatment. The early invention, stethoscope, combines the learned sign necklace with the placing of fingers in the ears, a mirror reproduction of the doctor’s action, also a tactile reproduction when allowed to handle the stethoscope herself. Active tactile experience with objects appears to play a part in eliciting manual expressions representing absent objects.

“Tracing” untaught signs were the latest to appear in Koko’s repertoire, only created after 6 years of age. Long-hair refers to long-haired humans, and traces the hairline of a human’s long hair on her own body, again a mirroring of something seen outside of herself. Filmers/reporters is likewise a tracing sign on her body, delineating the straps of camera equipment on news reporters who visited her.

Koko had two frequent signs that also appeared after age 6, woman (lip) and man (foot), that are not clearly iconic. They did, however, perhaps draw upon characteristics of men and of women that were particularly salient for Koko, thus employing metonymy, the representation of an object or concept by depiction of only a part of the object. Like many signs in human sign languages, lip and foot are opaque and arbitrary to anyone without an intimate knowledge of their origins (Kendon, 1988; Armstrong, Stokoe, & Wilcox, 1995). “Woman” (lip) is an index finger rubbed horizontally back and forth across the lips. Perhaps this is related to lipstick, a similar motion performed with the thumb. However, lip is similar to another earlier sign of unknown origin, glossed note, which Koko used before pointing to something of interest; this note sign dropped out of her vocabulary after early years. “Man” (foot) appeared after

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she began to take sexual interest in a human visitor not amongst her caretakers, a laboratory worker who wore heavy boots, and it has been speculated that Koko was using the boots as a point of reference; this visitor also sometimes played a game tickling Koko’s foot, and she may have extended her foot to him then. There is another possible derivation, however. A gesture observed several times in the zoo female Zura (see Table 4), consisted of turning the rear toward and extending a foot back to another gorilla, a mounting reference possibly derived during development from a signal commonly used by a mother for a youngster to get on her back. Zura sometimes tapped the sole of her extended foot with her index finger as part of this signal, sometimes only tapping the foot without presenting the rear, in the context of sexual play. This tap foot is identical to Koko’s “man” (foot) sign, which Koko used frequently in the context of human men, but not, for instance, for a “family” member such as her “surrogate father” Ronald Cohn. If the derivation suggested is correct, it would be an example of an adaptation of a “natural” behavior to a new context.

Untaught signs created by Koko after her first ten years have not been formally described in academic publications but many are described in articles in the Gorilla Foundation’s semi-annual Journal. Signs now regularly glossed as above and below, whose meaning at first eluded researchers, have become a standard part of Koko’s repertoire (Patterson & Tanner, 1988). These depict spatial location by moving a flat palm forward off the top of the head (above) or moving a flat palm from between the legs when seated (below).9 Another sign noted only in recent years has been glossed as take-off, referring to removal of clothing, lifting both flat hands quickly off the top of the head. Koko has also continued to transfer sounds of human speech into signed form, as in her frequent sign for vegetable browse (see Plate), a term for which she was not given a sign. The spoken word was not used until a change in diet when browse items of leafy green vegetables began to be distributed to Koko at intervals throughout the day. Koko makes the browse sign by placing a fist (“S”-hand) on her brow, with the tapping motion of the sign for “lettuce” from American Sign Language (Menendez & Patterson, 1994).

As well as inventing signs for referents for which she had not been provided with an ASL sign, Koko replaces some of her taught signs with untaught ones for the same referent, perhaps because her own versions are more meaningful to her when clearly iconically related to a referent or touching her body. Also, as previously noted, she seems to prefer signs without intricate hand configurations, substituting signs easier for gorilla hands to articulate, and signs that touch her body. An example is her usage (a cross-modal transfer) of knee (tapping a finger on her knee) for “need,” for which she had a taught sign; the ASL version of need is performed with a crooked index finger moving downward in the open space in front of the body. Another untaught sign that makes use of gorilla anatomy is Koko’s exaggerated version of frown, using her hands to pull her lower lip down rather than simply tracing downward lines at the corner of the mouth as in the ASL sign. In many ASL signs she retains the motion and place of a sign but changes or simplifies hand shape; in some she retains motion and 9. This depiction of the concept that something is located below something else seems to be a directional reversal of Koko’s walk-up-bottom sign and Kubie’s frequent armswing under gesture.

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hand shape but changes the place, usually to her body or a surface in her environment such as wall or floor.

Gestures Found in Both Signing Gorillas and Zoo Gorillas The number of communicative gestures shared by taught and untaught gorillas may be underestimated. Patterson and Tanner (1988) list untaught signs of Koko’s that duplicate gestures described for one or more of the gorillas at the San Francisco Zoo. Table 4 lists gestures of Koko’s that have also been observed in zoo gorillas or in the wild. A few gestures listed here overlap with those listed among Koko’s “invented” signs from Patterson and Cohn (1990); at the time of observation, these were not known to be used by other gorillas. Though not all have been seen in all gorillas, most have been observed in more than one zoo gorilla. Some of the gestures have not been reported in gorillas other than Koko and the San Francisco Zoo gorillas and may be similar because of a capacity of gorillas (and other apes) to form iconic gestures, rather than the gestures themselves being genetically predetermined. Similar gestures have been observed in other ape species (Fouts, 1997; Miles, 1978, 1993), and often have different functions both in different species and for individuals within a species (Tanner, 1998). Functions of many gestures are similar for both Koko and the zoo gorillas, but there are also some differences. All these shared gestures are social in function, used in interaction with other individuals to regulate actions and locations of activity. For Koko, such gestures were incorporated into her signed discourses and thus were used linguistically regardless of their origin. Non-sign-taught apes, who have been trained with lexigrams or computers, also incorporate “species-typical” gestures into their communications (Savage-Rumbaugh, 1986; Greenfield & SavageRumbaugh, 1990). For the zoo gorillas too, gestures often did not stand alone but were incorporated into strings of other gestures (Tanner, 2004).

General Discussion A gorilla tutored in sign language and gorillas living in a zoo both create signs or gestures that depict and invite action and point out objects and locations, but signs that refer to objects themselves are invented only by the signing gorilla. Many of the untaught signs of signing apes and the gestures of non-signing apes have iconic characteristics. Iconic descriptions can be formed in several different ways, depending on what aspect of an action or object is chosen as salient, i.e., what kind of metonymy is employed. Gestures describing similar actions or objects, therefore, may vary within and between different groups of apes (Tanner, 1998). On the other hand, some gestures or signs that are physically very similar are shared between signing and non-signing apes but may not have the same functions; these may be iconic gestures that are similar in appearance because they describe similar material, or may be hitherto little known species-typical gestures elicited by a relevant social environment (see Table 4).

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Table 4. Koko’s Untaught Gestures Seen in Other Gorillas Koko’s untaught signs also observed in other gorillas

Koko’s usage with Gorilla Foundation gloss

Usage at San Francisco Zoo

Where observed (zoo, wild)

armcross

(glossed as catch) used in activities involving tossing and catching of objects; chase games, playing hard to get; also requesting embrace or desirable objects

play contexts; function otherwise unknown

zoos and wild

armshake

(glossed as play or hurry) invitation to play; also expression of excitement or impatience

play invitation, readiness for activity; sometimes warning or threat (only used this way by one individual)

SF Zoo, not in wild

armswing under

(glossed as walk-up-bottom) sexual solicitation or request for tickling of bottom

invitation for contact in sexual play

SF Zoo, not in wild

away

(glossed as stop) to stop advance of another individual

agonistic contexts, avoidance of contact

zoos and wild

backhand

(glossed as darn) expresses annoyance or frustration

gaining attention in play situations, also used in agonistic display or protest

zoos and wild

bite

in playful excitement, referring to biting

in play, before or after biting play

zoos and wild

chestbeat

excitement, agitation, but also in a more controlled form glossed as gorilla

excitement, agitation, attention getting

zoos and wild

circle hands

(glossed as gentle) request for gentle behavior

unknown, but seen in play contexts

zoos and wild

clap

playfulness or excitement

in play, often solitary and before performing a physical action like jumping or balancing

zoos and wild

deictic (pointing) gestures

(glossed as me, you, that, there, your) designating numerous referents and locations; Koko performs points with extended index finger. Your is performed with outstretched palm, may designate another’s property or turn for action.

designating other or self as object or zoos and agent of action; also designating loca- wild tions. Performed with open hand, knuckles or fist. Glossed as chest fist pat, tap other, pound, extended palm

(glossed as come-gimme) extended palm requesting objects or the (could be included with deictic gestures) approach of other individuals

invitation to contact or request for food

facewipe

(glossed as toilet, b.s.) expression annoyance, avoidance of disbelief, uncertainty or annoyance

foot

designating the body part, also referring to human males

hand between legs

(glossed as below) performed play, sexual invitation (usually patting seated; hand moving out from motion) under body designates location below or under another object.

When forceful slapping motion, a masturbation activity.

zoos and wild SF Zoo

seen in a zoo gorilla, a variation of one SF foot back sexual invitation performed Zoo by tapping the foot with the hand gorilla SF Zoo, Rio Grande Zoo

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Table 4. (Continued) Koko’s untaught signs also observed in other gorillas

Koko’s usage with Gorilla Foundation gloss

Usage at San Francisco Zoo

Where observed (zoo, wild)

hands behind back

(glossed as walk-up-back) requesting companions fingers walked up back, tickling

inviting play activity or approach from companion seated behind self

zoos

head nod

(glossed as yes) agreement, assent

inviting approach or visual attention of other gorilla

one SF Zoo gorilla, wild

head shake, head turn

(glossed as no) dissent

head shake used in playful contexts; head turn sometimes avoidance or possible request for change of direction

zoos and wild

knock, pound (fist hand shape)

attention getting, or cross-modal transfer of English “obnoxious”

get visual attention in playful context; zoos and wild indicate location or direction

slap surface (flat hand)

(for Koko, glossed as pound) play invitation of challenge; referential use to request pounding on her back

play or chase invitation

tactile gestures

indicate movement desired from another by non-forceful contact or motion upon other’s body; can take many different forms: can take many different forms: moving hand down back vertically or across horizontally, patting, gentle pulling of hand, light push away, and others

indicate movement desired from another by non-forceful contact or motion upon other’s body; can take many different forms: moving hand down back vertically or across horizontally, patting, gentle pulling of hand, light push away, and others

zoos and wild

up

for movement upward; request to be picked up

request or intention to move upward

zoos and wild

attention getter

zoos and wild

Observations of gestures in the wild come from the following sources, but primarily the publications of George Schaller and Dian Fossey: Baumgartel, 1976; Burbridge, 1928; Campbell unpublished film; Denis, 1963; Fay, 1989; Fossey, 1979, 1983; Mori, 1983; Schaller 1963/1976, 1964.

(Koko’s usages from Patterson, 1980; Patterson & Tanner, 1988; zoo data from Tanner, 1998)

The fact that some of the gestures performed by signing apes resemble those of apes in the wild has been seized upon by some as evidence that apes do not really learn human sign languages, but only perform gestures that they would “naturally” use anyway (Pinker, 1994; Wallman, 1992). The accumulation of evidence does not support contentions that signing apes do not really use sign language but only adapt their species-typical gestures. “Natural” or species-typical gestures are indeed used by symbol-taught apes, but they may often elaborate upon them and have opportunities to use them in a greater variety of contexts than do apes in the zoo or in the wild. In addition to such species-typical gestures, apes with different upbringings are likely to invent gestures similar to each other’s, given a common ability for iconic representation, similar anatomies, and similar material to describe. In addition, signing apes, of course, use a large vocabulary of taught standard sign language in addition to speciestypical gestures and untaught signs. Even when modified by anatomy of the ape hand,

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much of this signing is nothing like their “natural” gestures. Few gestures resembling American Sign Language signs are spontaneously formed by untaught apes, who use a limited number of hand shapes compared to apes taught ASL.10 The iconic gestures a signing gorilla creates are more numerous and elaborate than those of zoo captives, probably because of intensive exposure to symbolic modes of communication and interaction with humans. Early input may alter brain utilization in humans (for instance, a heightened sense of pitch in humans blind since infancy, Gougoux, Lepore, Lassonde, Voss, Zatorre, & Belin, 2004) and no doubt in apes (Bard & Vauclair, 1984; Povinelli, 1994). A recent experiment with marmosets (South American monkeys) showed that in only one month, those monkeys housed in larger and more enriched environments actually developed denser neuron growth and had more of the synaptic proteins the brain uses in relaying messages between neurons, in contrast to control subjects housed in minimal caged situations (Kozorovitskiy, Gross, Kopil, Battaglia, McBreen, Stranahan, & Gould, 2005).

Where great apes have been shown to possess capacities once reserved for humans, such as the ability to imitate goal-directed actions and understand their reflection in mirrors and employ referential pointing, the apes have often been individuals raised by humans (discussions of the strong claim that human-rearing “enculturates” apes, giving them human capacities they do not naturally develop, are found in several chapters in Parker, Mitchell, & Boccia, 1994). Skills salient in humans would be likely to be more utilized in apes with a good deal of exposure to humans (Povinelli, 1994; Gomez, 2004). Iconic representation is, after all, related to imitation in that it is a form of mime, and requires the taking of another’s perspective when depicting an action or object outside the self as well as kinesthetic/visual matching (Mitchell, 1994; Byrne, 1995). Expressing, in iconic fashion, action desired from another appears relatively late in Koko’s inventions (age 2) and even later in zoo gorillas’ development (age 6–7). Request for another’s action upon the gesturer’s own body appears earlier.

Gestures requesting action of another require understanding of the other as an independent agent and also an understanding of the other’s point of view. For instance, the gorilla must have an awareness that the visual attention of the partner is necessary for communicating with gestures; such understanding was present in the adolescent zoo gorillas studied by Tanner and Byrne (and in younger gorillas; see Gomez, 1990, 1991, 1994, 1996).

Koko moves further than zoo subjects with her untaught signs: from depicting social action, to use of a “still” image to represent an object, to reproduction of customary behavioral action upon an object to represent that object, then to tracing the outline of an object. Thus there is a transition from pure behavior and “intention movements” to representation of proposed action from others (rather than one’s own action), and finally to non-action representation of objects.

Signing apes and zoo captives have in common action and location as the most prevalent descriptive elements used in forming their gestural creations, even those un10. American Sign Language has nineteen primary hand shapes plus twice as many variations; a deaf human child untutored in sign language created nine hand shapes (Goldin-Meadow, 1984). Untutored gorillas seem perhaps to have three: open palm, fist, and knuckle hand.

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taught signs of the gorilla Koko that represent objects. This may be because of the gorilla’s limited comfort with the intricate hand shapes utilized in human sign language that would more precisely describe object shape, but are not suited to gorilla anatomy.

Alternatively, however, preference for action as a descriptive mode may be related to cognitive processing. The brain has specialized cells for visual reception of hand and limb movement that respond strongly to hand-object interactions (Perrett et al., 1989).

More recently neurons termed mirror neurons have been found to react to actions performed on objects, but do not react to an object alone, or to the same action performed without an object involved (Gallese, Fadiga, Fogassi, & Rizzolatti, 1996; Rizzolatti, Fadiga, Fogassi, & Gallese, 1996; Rizzolatti & Arbib, 1998; see Rizzolatti & Craighero, 2004, for a review of mirror neuron research, and Roy & Arbib, 2005; Arbib, 2002, 2005, regarding implications for language production and perception). Most recently, research has shown that the understanding of others’ manual actions is influenced by context (objects nearby) that implies what the subject’s intention might be (Iacoboni, Molnar-Szakzac, Gallese, Buccioni, Mazziotta, & Rizzolatti, 2005). The implication that actions are understood through their context and that objects are understood through the actions performed on or with them aligns well with the fact that the majority of Koko’s untaught signs for objects were made by portraying a customary action associated with the object.

Within the framework of the function of mirror neurons, Arbib provides a scenario that neatly parallels the progression we have found in moving from zoo gorillas’ spontaneous gestures depicting action, to Koko’s inventions for objects. Demonstrating how bridging from action to language could take place, Arbib (2002) provides a hypothetical sequence for development of gesture in evolutionary history that moves from pragmatic action towards a goal object, to imitation of such actions (required in order for Koko to establish an iconic sign for new objects/actions), to pantomime produced away from the goal object (what Koko does when establishing a new sign in her vocabulary, getting the observer to focus on a specific action, or an object associated with it). The next stages Arbib posits are: abstracting gestures from their pragmatic origins, which is what happens when Koko makes a (metonymic) choice of what aspect of action to use to henceforth represent the target action or object; then using the new sign in compounds with other previously established taught or untaught signs, as she does. Koko presumably jumps up to the latter phases, not found in zoo gorillas or other untaught apes, because her enculturation with human communication enhances her understanding of shared attention and conventions of language.

The predominance of descriptive action in untaught signs may be biologically facilitated by the mirror neuron system; proximately, it may be due to the fact that it is through shared action that social discourse takes place between gorilla and gorilla, or gorilla and human companion in Koko’s case. For Koko, the introduction of a new and unfamiliar object like a stethoscope or modeling clay would be meaningless without a demonstration of the usage of that object, and it is that usage that makes the object come alive as a part of the shared interaction involving it.

In Koko’s development, actions were depicted earlier than hand-shape object descriptions, and tracing of outlines of objects was latest to appear. Tracing a shape is

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cognitively very close to drawing or writing (as noted by Edwards, 1979). Koko is able to paint depictions of objects that are correctly placed in their relative spatial and size locations and to select appropriate paint colors, but her paintings are not always detailed in reproduction of shape (for a photograph of a painting and its model see Patterson, 1985).11 Because the tracing of shapes for Koko seems to be most comfortably and extensively performed on the surface of her own body, there might also be a tactile element involved in some of her signs; the hand shape for glasses, for instance, might involve a tactile memory of touching the frames of glasses on one’s head, or for scarf, the feeling of a scarf covering her head. Koko, in her learned ASL signs, was taught numerous signs for objects that were not touchable, or could not be touched by her: examples might be clouds, sun, tree, and house. These signs, however, are not among her most frequent spontaneously used vocabulary items.

Though a tactile element is part of many of Koko’s untaught gestures, some of these signs apparently originate from transfer of a visual feature observed on someone else onto herself, as in her sign for filmers/reporters (tracing the outline of the straps seen on camera bags). Transferring features observed on someone else to one’s own body is rather like touching oneself on a location observed in a mirror. For humans, feeling that one is actually tracing the outline of an object in a tactile manner when putting it on paper has been shown to produce accurate and natural artistic depictions, even by those with no artistic training; most people, however, instead perform the intermediary step of mentally representing, or visualizing, an object to oneself and only after this drawing it on paper (Edwards, 1979). In the zoo gorillas, tracing of motion on another gorilla’s body is a frequent medium of requests for action. This tactile propensity, born from physical interaction, may underlie many of the inventions of both the zoo gorillas and Koko. The model object was present when Koko first created her “shape tracing” signs, but she also used them later in the absence of the original model, implying memory of either the shape of the object or her previous actions.

Gorilla gestures, both of zoo and signing gorillas, seem to arise from an understanding of paths of action that can be tactile, visual or locomotor. Underlying the gestural abilities of all great apes is the anatomical characteristic of rotational movement of the joints, a characteristic that humans share, derived originally as an adaptation to brachiation under tree limbs and arboreal “clambering.” The locomotor adaptations permitting brachiation in apes allow a much greater flexibility of limb control than possessed by monkeys, which potentially has consequences for all manual activities (Morbeck, 1994). Several theories have been put forward that specifically relate ape cognition to demands of the physical environment (reviewed in Byrne, 1997). Parker and Gibson (1977, 1979; see also Bard, 1990) propose that seasonal foraging, on foods that require extraction from a matrix, selected for tool-using propensities and abilities.

Povinelli and Cant (1995) (see also Chevalier-Skolnikoff, Galdikas, & Skolnikoff, 1982, p. 643) propose that arboreal clambering, by an animal too large to risk a fall, selected for the ability to imagine itself in a detached, objective way and thus plan safe routes through the canopy, dealing with constantly changing conditions in transferring 11. Chimpanzees and other apes have also painted; for a most extensive illustrated discussion, see Morris, 1961, and Hoyt’s (1941) early description for the gorilla Toto.

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from tree to tree. Orangutans use supports that are flimsy relative to their weight much more often than do monkeys in the same habitat, and use multiple supports, whereas monkeys prefer single supports. On this theory, viewing the self as an object led to the ability in apes to recognize their own selves reflected in a mirror.

Both the extractive foraging and complex locomotion accounts focus on a single modern species (the tool-using chimpanzee, the arboreal clambering orangutan) as models of the common ape ancestor, making them difficult to test against comparative data. Byrne (1997, 1998, 2000, in press) proposes that feeding competition from sympatric monkeys—smaller animals with lower metabolic needs, more efficient longrange travel, and ability to eat less ripe fruit—selected for skills in manual foraging, allowing apes to exploit foods unavailable to their competitors, such as insects within mounds or trees, and plants defended by spines or stings. All modern apes feed in ways that are manually skillful compared with monkeys, involving complex, hierarchically organized techniques that are unlikely to be invented by a solitary individual (Byrne, 2002). Critical to skill acquisition, then, is the ape’s ability to decipher the skilled manual actions of others and thereby learn novel techniques (Byrne & Russon,1998; Byrne, 2003; Whiten, Horner, de Waal, 2005). Behavior parsing and hierarchical program-building abilities, functioning to allow apes to exploit a wider range of foods by allowing traditions of skill to accumulate by social learning, have been explicitly related to the origins of gestural communication (Byrne, 2000, in press).

Building up hierarchically structured action-plans, from simpler building blocks of actions in the ape’s extensive manual repertoire, is seen as the evolutionary origin of the syntactic structuring of language components. However, none of these theories deals specifically with the iconic abilities that have been a prominent focus of the present analysis. Iconic gestures are anticipations of action, including actions of others as well as anticipated or previously experienced actions of the agent itself, that the gesturing gorilla must be able to represent mentally and then express through a kind of mime. Moreover, the gorilla is apparently able to translate between different scales, expressing desired large-scale body movements of others by using the smaller compass of its own hand gestures.

We propose that action mapping in three-dimensional space is an important capability of all great apes. Action mapping can be defined as the mental ability to picture motion in space, predict its results before performing it, and translate from the largescale of real world motions of bodies (whether observed, remembered, or anticipated) into the smaller scale of hand movements that iconically describe them. The capacity to map seamlessly from observed bodily motions to corresponding actions of the self appears closely related to the “active intermodal matching” theory, proposed by Meltzoff & Moore (1977) (Meltzoff, 1996) to underlie the ability of very young children to copy the facial gestures of adults. They suggest that humans are born equipped with the ability to match their own muscular movements with the movements they see others make, a 1:1 system of correspondence that bridges across modalities. The action mapping concept also is supported by the existence of mirror neurons and their functions, as discussed earlier. In a communicative context, as in gorilla gesturing, action mapping would mean mentally picturing motion in space and its possible results (either on the basis of memory or anticipatory planning) and then performing it, without

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the need for any step-by-step shaping process. In communication, action in real space can be “miniaturized,” mapped in hands or arms.12 Though it seems that many gestures may be mapped directly to the hands from action in the real world, some form of imitative process is often posited as a way in which novel communication might be propagated. Let us look at the evidence for imitation, or any kind of social learning, of gestures. Frans de Waal describes the spread of a behavioral tradition in captive chimpanzees (de Waal & Seres, 1997). The capacity to reproduce nonfunctional limb motions demonstrated by a human in a “do as I do” task has been shown in captive chimpanzees (Custance et al., 1995) and also in gorillas (Byrne & Tanner, 2006 in press). Orangutans imitate elaborate human activities, sometimes involving a series of several actions (Russon & Galdikas, 1993), and imitation at a program level seems to be the best explanation for the complex, hierarchically-organized, and highly plant-specific feeding techniques seen in mountain gorillas (Byrne & Byrne, 1993; Byrne & Russon, 1998). For gorillas raised in a signing environment, imitation of a human’s signs is a frequent way of learning new signs, even in a gorilla not formally taught signs. Ndume, an adult male gorilla brought to the Gorilla Foundation to be a companion to Koko, was never formally taught any sign language, but began gradually to use some of the same signs that Koko and her gorilla companion Michael had been taught, and to compound signs (Patterson & Gordon, 2002; Patterson, 2005).

At the zoo, some evidence speaks against imitation as a way of learning gestures.

Many of the gestures shared by all the gorillas in the San Francisco group are generally accepted as species-typical. The use of a few gestures by some but not all members of the group remains unexplained. The gesture armshake, for instance, is not seen in all gorillas, though it has been recorded at several zoos and was used by several members of the San Francisco Zoo group. Kubie’s son, Shango, who at an early age watched many of the play sessions between Kubie and Zura during which armshake was frequent, never developed armshake as a part of his gestural repertoire, and it has only very rarely been observed in his mother, Bawang. On the other hand, Shango’s younger brother Barney armshakes frequently and seemed to move from, in earliest observations, using armshake in a solitary way, to using it socially. Pika et al. (2003) found some gestures that were widespread among members of one zoo group studied, but not found at all in another group elsewhere. Stoinski (2006) in a survey of gorillas in different zoos found that numerous behaviors, including gestures, varied considerably from zoo to zoo, indicating each zoo had its own set of potentially cultural behaviors.

Another indication of gorillas’ capacity to remember and reproduce actions comes from the observation of repeated sequences of actions, gestural and otherwise, by gorillas in the San Francisco Zoo group (Tanner, 1998), in contexts of play and display.

Though they involved the reproduction of a gorilla’s own previous actions, not those of another, these sequences show that the memory capacity necessary for reproduction of complex activities is available for the gorilla. Ability to reproduce complex sequences of functional activities makes sense in the action mapping context.

12. Gestures in adults are miniaturized in comparison to those of young children (McNeill, 1992).

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The work of Tomasello and colleagues posits ontogenetic ritualization, a process of fading or shaping frequently performed actions in repeated interactions with another individual, as the main process through which ape gesture is created (Tomasello, Kruger, Farrar, & Evans,1985; Tomasello, Gust, &, Frost, 1989; Tomasello, SavageRumbaugh, & Kruger, 1993; Tomasello, Call, Nagell, Olguin, & Carpenter, 1994; Tomasello, 1999 for an overview). The adaptive explanation of action mapping is a simpler one than ontogenetic ritualization, which as a process has been deduced but never actually observed in full. In the experience of the present authors, ontogenetic ritualization is not a completely satisfying explanation of all inventions by zoo gorillas or by signing gorillas. Instead, much invention appears to begin not with shaping of a functional action directed toward another gorilla, but with one of these two processes: (1) a spontaneous natural body movement (perhaps a sign or gesture such as armshake) is expanded or altered when re-used in varying situations of social interaction, eventually gaining meaning through repeated interactions, or (2), an iconic movement is produced by putting into manual motion an action mentally anticipated or desired. For Koko, this, with manual reproduction of shapes of objects as well as actions, was the primary method of invention. Such gestures or signs, generated by either process, may vary in scope, size, and dynamic according to context, as do signs in human sign languages. Type (1) invention is not entirely removed from the idea of ontogenetic ritualization though it need not begin with a functional action; type (2), however, would be generated by action mapping without any need for a ritualization process. Koko’s gestures, above, below and browse, discussed earlier in this paper were all spontaneously used by the gorilla well before human companions understood them, thus no shaping process could exist. In the zoo, Barney’s usage of armshake appeared to develop from spontaneous use of an idiosyncratic, but anatomically feasible movement, used at first in a solitary context and only later developed in social contexts. It is also not impossible that the two kinds of gesture creation described above could both be used in forming one meaningful gestural motion, though an example has not been found at present.

Pointing and other deictic gesture is not well explained by ontogenetic ritualization. There are too many variations in size, scope, location, and orientation of gestures indicating locations for each gesture to be likely to be individually ritualized. Likewise, though zoo gorillas’ tactile iconic gestures may appear to be “faded” from forceful actions, new gestures constantly appear in different directions and dimensions, with no two exactly alike. It is unlikely that each gesture would be individually faded.

Many untaught gorilla gestures combine action mapping with the deictic principle of locating a sign appropriately in a certain location, on one’s own body or on another’s body. An example from zoo gorilla Kubie, come shoulders, involved patting both his shoulders with his palms, to which play partner Zura responded by approaching and placing her hands on his shoulders (Tanner & Ernest, 1989). Koko also early generated an untaught “pointing” sign. The taught sign “bird,” used by her instructor to point out a bird seen through the window was co-opted by Koko as a sign for various animals and novel objects on the other side of the window. Koko used both index fingers to point in a configuration similar to the original sign performed by the instructor, an extended thumb and index finger.

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At the San Francisco Zoo, Kubie used his established repertoire of gestures with several gorillas and was later understood by new individuals. He used most of the same repertoire of gestures he used with Zura in his interactions with two other females in the group during other time periods years apart. His most frequent gestures were all used regularly over a period of more than seven years, though proportions of the different gesture types used with each female varied. Apparently different recipients were able to interpret his actions and the resulting interactions were favorable often enough that it benefited each new pair to establish such communication. Action mapping as a cognitive ability shared by apes explains this mutual understanding of iconic gesture between different partners without any need for re-shaping.

Thus, though gorillas in the zoo group varied in their repertoires of gestures, with some gestures being shared with other gorillas, and others unique to individuals, the gorillas still seemed to have developed a mutually understood system of communication. This was particularly striking in Kubie and Zura’s interactions; their gestures often alternated in a turn-taking conversational manner and seemed to be used to make decisions about type, timing, and location of play as well as simply promoting contact (Tanner, 2004).

Koko’s untaught signs for objects are unlikely to be explained as “faded” from action, but they can be understood as formed by an ability to map and mirror visual input with the hands. Ontogenetic ritualization “takes two” to shape gestures for mutual interaction, but originating a sign for an object does not require interaction for its invention, only to establish it as a mutual communicative element. Shared cognition and shared backgrounds along with shared interaction with objects, make understanding of such signs possible. Koko’s newly untaught iconic signs thus eventually make good sense, once decoded by human companions.

Because anatomy and behavior evolve in interaction with the environment, the contexts in which gestures most frequently take place are important in understanding what their ultimate function might be. The gestures observed in zoo gorillas were at their highest frequencies in play and quasi-sexual situations, and pygmy chimpanzees (also known as bonobos) in captivity used iconic gestures to settle on copulatory positioning (Savage & Rumbaugh, 1977). Further, Crawford (1937) saw the spontaneous emergence of much gesturing in an artificial context where two chimpanzees had to cooperate and coordinate their movements in order to receive food rewards. Signing chimpanzees, when observed through remote videotaping with no humans present, conversed with signs and gestures about play, grooming, and other social matters but hardly at all about food and eating or discipline and dominance (Fouts & Fouts, 1989).

What all these situations of rich communication have in common is the necessity of coordination of movement around the environment, or cooperation in movement. The term co-regulation in the manner of Alan Fogel’s mothers and children could just as well be applied (Fogel, 1993). Visual and tactile gestures proliferate when maintenance of close contact with another, or closely coordinated movement, is necessary for interaction to be successful (King, 2004).

Gestures and signs also obviously thrive when an environment is vested with conspecifics and objects with which interaction is desirable and pleasurable; Greenspan

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and Shanker (2004) describe the importance of function and emotion and how complementary they are in the development of communication. In a study of the pragmatic functions of Kokoâ&#x20AC;&#x2122;s signing during her first year of instruction (between age 1 and 2 years), the categories found to be used by human children were all used by Koko; these included labeling, repeating, answering, requesting action, requesting an answer, calling, greeting, and protesting (Patterson, Tanner, & Mayer, 1988). A glance at the list of Kokoâ&#x20AC;&#x2122;s inventions (Appendix) shows that her untaught signs were for things and activities in her environment that Koko was interested in, but for which she had not been taught a sign. She needed signs in order to maintain shared attention with her companions, and so generated ones of her own invention. In some cases, her signs were emotional comments, such as her unlisten, unattention, frown, and blew-it signs.

Koko and her gorilla companion Michaelâ&#x20AC;&#x2122;s sign acquisition has been compared to that of signing human children in several studies by Bonvillian and Patterson (1993, 1999). Similarities were found in type of vocabulary content, acquisition of referential signing, and in the generation of various non-sign gestures. Differences were found in rates and patterns of early language and gestural milestones, with gorillas reaching many of these milestones but at a slower rate than children. The same could be said for the zoo gorillas in comparison to the sign-instructed gorillas. Comparison of the untaught signs of Koko, a signing gorilla, and gestures of zoo gorillas shows a continuum of representation, where a signing gorilla moves further than the zoo gorillas along a line that proceeds from behavior directed at immediate goals, to representation of desired action, to representation of objects.

Gesture may well be the structural foundation upon which language is built, and we can find in gesture the thread of evolutionary continuity between animal action and human language (King, 1999; Byrne, in press). The present study shows that it is likely that in the history of our hominoid ancestors, the earliest iconic depictions were of action rather than objects, just as we find in apes. Because such iconic capacity is present in gorillas, and surely in orangutans, given their related ability to imitate and to use human sign language (Russon & Galdikas, 1993; Miles & Harper, 1994; Miles et al., 1996; Shapiro & Galdikas, 1995), it was most likely present 10 million years ago in the common ancestor of hominoids. New means of communication, when they occurred in our ape ancestors, would certainly have achieved increased success for individuals in social, and ultimately, sexual relationships. Such behavior would surely have selective value, and over generations result in gestures becoming increasingly frequent and complex. Through the condensation of real activity to something representing it, in forms progressively more removed from the original, hominid communication have, over millions of years, reached the arbitrariness that is a characteristic of human language. But not all of human language even today is purely arbitrary. We can still see glimpses, particularly in sign languages, of the development of language from the raw materials of action (Armstrong et al., 1995). The creation and usage by gorillas of special repertoires of gestures gives us a window into the developmental processes and environmental pressures that might have led an ancestor ape to further refinement of iconic communication, and its eventual expansion to human gestures of the mouth.

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Credits: The authors wish to thank Barbara King, Christa Nunes, and two anonymous reviewers for their time spent reading this paper and for their helpful suggestions. The first author wishes to thank Charles L. Ernest, her husband, for his video documentation since 1988 of the San Francisco Zoo gorillas and their gestures, as well as continual technical support of all kinds.

Appendix Koko’s untaught signs: first 10 years (Signs from Patterson & Cohn, 1990, analysis of iconic characteristics by first author) Key: O: object A: action D: deictic IS: iconic for shape of object IA: iconic for an action BL: indicates (self) body location of referent BLO: on body of other person or gorilla CMT: cross-modal transfer from English sounds D: deictic; pointing U: unknown derivation FA: functional action Gloss in English and classification

Physical form of untaught sign

Type of iconicity or other type of reference

Kind of representation

CMT

apricot O

“A” hand shape with motion like cross-modal transfer from English sound as well as “peach” sign (hand brushed compounding signs down cheek)

barrette O

index finger draws line forward above ear where barrette is usually placed

draws shape of object, also places on body location

IS, BL

bird (notice) D

index fingers, held together at tips, point to location of object of interest that is out of reach

deictic

D

bite A

teeth bite index finger side of hand

iconic for action

IA

blew-it A

loud exhalation: blowing sound directed at offending person

cross-modal transfer from English sound

CMT

blow A

blows on index finger held vertically in front of mouth

iconic for action

IA

body hair O

fluffing up hair on the body by rubbing both hands up and down on body

indicating part of body

BL

bracelet O

cupped hand encircles and pats wrist

iconic for shape of object, placed on body location

IS, BL

The Development of Spontaneous Gestures in Zoo-living Gorillas and Sign-taught Gorillas Gloss in English and classification

Physical form of untaught sign

Type of iconicity or other type of reference

95

Kind of representation

clay O

palms together, move back and forth in circular rolling motion

iconic for action, on customary body location

IA, BL

dental floss O

pick index on teeth plus thread sign (two little fingers touch then move apart horizontally)

iconic for shape and action, on body location

IA, IS, BL

drip-chin A

mime with index the action of liquid rolling down chin

iconic for action, on body location

IA, BL

dripping A

index imitates motion of dripping liquid on cheek

iconic for action

IA

earphones O

thumb and index of both hands move down body from ears

iconic for shape of object, placed on body location

IS, BL

eye makeup O

index finger strokes horizontally across eyelid

iconic for action, placed on body location

IA, BL

fake-sneeze A

imitates sound and motion of sneezing

iconic for action

IA

fake-tooth O

taps upper or lower rear tooth with index

body location

BL

fang (Halloween toy)

tap lower canine teeth with hooked index fingers

iconic for shape of object, placed on body location

IS, BL

O filmers, reporters O

thumb and index of both hands move down body where camera straps are located

iconic for shape of object, placed on body location

IS, BL

frown O

lower lip pulled down over chin with fingers

iconic for shape, placed on body location

IS, BL

glasses O

thumb and index pinch at temples

iconic for shape of object, placed on body location

IS, BL

grate A

imitating motion of grating a vegetable; fist moves across palm of other hand

iconic for action

IA

hair bow O

index and thumb of both hands placed on head

iconic for shape of object, placed on body location

IS, BL

inhale A

index from mouth down to stomach

iconic for internal path of an action in body

IA, BL

kiss-hand A

kiss on hand

iconic for action

IA

long hair O

index fingers trace hairline from ears to below shoulder

iconic for shape of object, placed on body location

IS, BL

man, male (foot) O

taps bottom of foot with index

unknown

U

nail file O

tip of bent index moves back and forth across finger of other hand

iconic for action, placed on body location

IA, BL

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Gloss in English and classification

Physical form of untaught sign

Type of iconicity or other type of reference

Kind of representation

note (something in environment) D

moves index horizontally across lips before pointing to something

unknown

U

obnoxious QUALITY

knock sharply on wall or floor

cross-modal transfer from English sound “nox” in obnoxious

CMT

pickle O

thumb and index extended from both fists held in space in front of body

outlining shape of object

IS

poke A

jab with index

iconic for action

IA

poke-stomach A

poke stomach with index

iconic for action on body location

IA, BL

puppet O

open hand moves down over fist of other hand

iconic for action (putting hand puppet over hand), placed on body location

IA, BL

runny nose O

index traces path of liquid running from nose

iconic for action

IA, BL

scarf O

palms of open hands down sides of head

iconic for shape, body location

IS, BL

scraper O

fingers of open hand make scrap- iconic for action ing motion across other hand

sip A

tips of index and thumb touch lips

smooth QUALITY

smoothing motion of open palms iconic for action up legs

stethoscope O

index fingers in ears

iconic for shape, body location

IS, BL

strangle A

hands grasp neck

iconic for action, on body location

IA, BL

thermometer O

puts extended index finger under arm

iconic for shape, on body location

IS, BL

tickle A

index makes tickling motion under arm

iconic for action, on body location

IA, BL

turn-around A

open hand brought around from one side of waist to other on other’s body

iconic for action

IA, BLO

unattention STATE

palms of both open hands placed over face

functional action

FA

iconic for action, body location

IA IA, BL IA

The Development of Spontaneous Gestures in Zoo-living Gorillas and Sign-taught Gorillas Gloss in English and classification

Physical form of untaught sign

Type of iconicity or other type of reference

Kind of representation

under-eye makeup O

index moved horizontally under eye

iconic for action, on body location

IA, BL

unlisten STATE

palms cover ears

functional action

FA

Viewmaster O

one hand open palm like mask, other hand thumb and index at eye like camera

compound sign at body location

BL, IS

iconic for action, on body location

IA, BL

walk-up-my-back in seated position, hands placed behind back, palms A up, and bounced

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walk-up-mybottom A

arm with open hand swings under body between legs

iconic for action, on body location

IA, BL

woman (lip) O

rubs index horizontally back and forth across lips

iconic for action (applying lipstick) on body location

IA, BLO

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The Kids Are Alright: Maternal Behavioral Interactions and Stress Reactivity in Infants of Differentially Reared Rhesus Monkeys Peter G. Roma Department of Psychology American University

Angela M. Ruggiero National Institute of Child Health and Human Development

Melanie L. Schwandt and J. Dee Higley National Institute on Alcohol Abuse and Alcoholism

Stephen J. Suomi National Institute of Child Health and Human Development

Abstract: Behavioral interactions and infant stress reactivity were investigated in 120 mother-infant pairs of rhesus monkeys (Macaca mulatta). The mothers themselves were either mother-reared (MR), surrogate-peer reared (SPR), or peer-reared (PR). Focal observations and isolation stress tests were conducted throughout post-natal months 1–6 of the infants’ lives, followed by a standardized 4-week social separation regimen. PR mothers engaged in more grooming than MR mothers during months 4 and 6, and more rejections than both other groups during months 3 and 5. Although all infants were mother-reared, D 14 and 30 cortisol responses in infants of MR and SPR mothers resembled their mother’s responses at that age, a pattern that corresponded inversely with levels of mother-infant mutual ventral contact during month 1. Despite observed differences in maternal behavior and evidence of non-genomic cross-generational transmission of early cortisol reactivity, infant stress responses throughout later infancy did not vary as a function of the mother’s rearing condition.

Maternal Behavioral Interactions and Stress Reactivity in Infants of Differentially Reared Rhesus Monkeys The impact of early adverse experience on biobehavioral development in humans and other animals is well documented. Extensive evidence from the human literature

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indicates heightened vulnerability to psychopathology stemming from early childhood loss and trauma (e.g., Agid, Kohn, & Lerer, 2000; Heim, Plotsky, & Nemeroff, 2004), with the resulting alterations in stress physiology exacerbating this and other health risks (e.g., Christoffel & Forsyth, 1989; Goeders, 2003; Vanitallie, 2002). Analogous findings have also been observed in correlational and experimental animal models (e.g., Brake, Zhang, Diorio, Meaney, & Gratton, 2004; McIntosh, Anisman, & Merali, 1999; Sánchez, Ladd, & Plotsky, 2001).

One particular topic that has attracted considerable attention is the effects of early experience on social development, and in this context, nonhuman primate models have generated a compelling body of research. In virtually all primate species, including humans, some of the most salient early environmental experiences are social in nature, particularly within the domain of the mother-infant relationship. Among the most poignant demonstrations of this are the classic studies of “motherless-mother” monkeys conducted by Harlow and colleagues at the University of Wisconsin Primate Laboratory (see Ruppenthal, Arling, Harlow, Sackett, & Suomi, 1976 and Suomi & Ripp, 1983, for thorough reviews). In this work, infant rhesus monkeys (Macaca mulatta) were reared for at least the first six months of life devoid of contact with any conspecifics. When later introduced to socially reared peers, the isolate-reared monkeys appeared overwhelmed and typically remained socially inept unless “rehabilitated” by interaction with younger monkeys of equal social sophistication. When some of these isolate-reared females subsequently became mothers (“motherless mothers,” according to Harlow) most were grossly incompetent and often abusive in caring for their infants. Somewhat less severe deficits were exhibited by most motherless mothers who had been reared in increasingly complex social environments, such as peeronly rearing (see Novak & Sackett, 2006).

These studies are often cited as clear examples of how socially impoverished rearing can produce deficits in subsequent maternal care, with devastating cross-generational results for the infants. However, in their 10-year follow-up survey of motherless mothers, Ruppenthal et al. (1976) described some remarkable trends underscoring the robustness of species-appropriate maternal behavior in females reared without a real monkey mother. The most striking effect was that of parity. Without any human intervention, motherless mothers were well more than twice as likely to provide adequate care for their second and third infants versus their first, and more than three times as likely to adequately care for their fourth and fifth infants.

In addition to parity, a number of other variables were also shown to increase the likelihood of adequate parenting among motherless-mother monkeys, and ever since then active efforts have been made to integrate these factors into primate nurseryrearing paradigms (Suomi & Ripp, 1983), including those employed in the Laboratory of Comparative Ethology (LCE) at the National Institute of Child Health and Human Development (NICHD). Perhaps the most important variable has been the opportunity to engage in species-typical social interactions throughout development. At LCE, mother-reared (MR) infants are reared by their mothers in groups with other adults and their offspring, an arrangement that provides ample opportunity for relatively normal biobehavioral development. Nursery-reared infants are either peer-reared (PR) or surrogate-peer reared (SPR). The former condition is essentially identical to that used

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in the Harlow laboratory, where age-matched infants live exclusively with each other in groups of four. Surrogate-peer rearing involves individual housing with an inanimate surrogate, but includes daily socialization sessions with other SPR infants beginning after the first month of life.

Although the original motherless-mother work identified sometimes dramatic rearing effects on maternal behavior, contemporary nursery-rearing conditions have received relatively little attention in this regard; moreover, few investigations have extended analyses of rearing effects to developmental outcomes in the mothers’ infants, with the obvious exception of the abusive and infanticidal primiparous isolate-reared mothers. Champoux, Byrne, DeLizio, and Suomi (1992) did show that despite some differences in rejection rates and social contact, multiparous peer- and isolate-reared rhesus mothers were largely indistinguishable from their mother-reared counterparts in most other aspects of their maternal behavior. Also, Sackett, Ruppenthal, and Davis (2002) recently compared health and reproductive data from nearly 1,200 MR and over 500 SPR pigtailed macaques (Macaca nemestrina), but found virtually no differences between rearing conditions in terms of growth, injury, survival probability, or reproductive success. Taken together, these results suggest that some modern laboratory rearing practices may be successful in ensuring infant health in the absence of care by the biological mother. However, Sackett, Ruppenthal, and Davis’ data did not specifically address maternal behavior of their differentially reared monkeys, whereas Champoux, Byrne, DeLizio, and Suomi’s did not include SPR mothers or assess effects of maternal rearing on any aspect of infant biobehavioral development. The purpose of the present study is to address these issues.

In addition to extensive mother-infant behavioral observations, the LCE research program investigating biobehavioral development in rhesus monkeys is unique because it includes standardized longitudinal assessments of stress reactivity throughout infancy, namely activation of the hypothalamic-pituitary-adrenal (HPA) axis in response to psychosocial stressors. This combination provides numerous opportunities to assess early environmental influences on biobehavioral development across generations. As such, the specific goals for the present study were to determine 1) if and how contemporary laboratory rearing affects subsequent mother-infant behavioral interactions, 2) if and how a mother’s own rearing history influences her infant’s HPA axis reactivity, and 3) if direct relationships exist between individual differences in maternal care and infant stress reactivity within groups of differentially reared rhesus monkey mothers.

Method Subjects Data were analyzed from a total of 120 mother-infant pairs of rhesus monkeys (Macaca mulatta) collected over eight consecutive birth-year cohorts; the infant subject pool was composed of 74 males and 46 females. All mothers and their infants were group housed in combined indoor-outdoor pens with another 6–8 adult females from the same cohort as each other and with their infants from the same cohort as each other.

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Each group also included two adult males who sired their respective group’s infants.

All animals had ad libitum access to water and monkey chow with regular supplements of fresh fruit and grains. All procedures described in this report were in compliance with the Animal Welfare Act (1966) and Public Health Service Policy, and all protocols were approved by the NICHD and NIAAA Animal Care and Use Committees.

Mothers’ Rearing Conditions All of the infants included in this study were reared by their mothers (biological or adoptive); however, the mothers themselves were reared as infants under one of three conditions: Mother-Reared (MR, n = 40), Surrogate-Peer Reared (SPR, n = 20), or Peer-Reared (PR, n = 18). Each of these rearing conditions was described in detail by Shannon, Champoux, and Suomi (1998) and is summarized briefly here.

MR mothers were reared in the same conditions as their own infants (described above). The SPR and PR females were removed from their mothers 1–3 days post-partum and assigned to their respective nursery-rearing groups. All nursery-reared infants were housed in clear plastic cages with constant access to a polypropylene surrogate outfitted with a heating pad and covered with fleece cloth until post-natal day 15. On day 15, each individual infant was moved with her surrogate (minus the heating pad) to a larger wire mesh cage.

Nursery-reared infants were assigned to mixed-sex groups of four; when the youngest group member reached 37 days of age, the SPR infants began regular socialization sessions in a separate large play cage. SPR socialization took place each weekday for two hours, after which the infants were returned to their respective individual home cages. When the youngest member of a PR group reached 37 days of age, all of the infants from that group began permanent social housing in a large primate cage.

The SPR infants had access to their surrogates for the duration of their stay in the nursery while the PR groups’ surrogates were removed when the infants reached 4 months of age.

At approximately 7 months of age, all subjects were moved into large peer groups, each containing several MR, PR, and SPR age-mates of both sexes. All of the subjects remained in these or subsequently reconstituted peer groups until adulthood.

Mother-Infant Behavioral Observations Although the mothers described in this report were initially reared under systematically different conditions, all of their infants included in this study were motherreared. In order to assess rearing effects on subsequent maternal care, a subset of behaviors from an extensive mother-infant ethogram were analyzed. Each mother-infant pair was observed twice a week from week 1 to week 24 of the infant’s life. Observation sessions consisted of a 5-minute focal observation period of the infant followed immediately by a 5 minute focal observation period of the mother. Observation sessions were conducted by trained observers on various weekdays and at various times

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Table 1. Operational Definitions and Scoring Criteria for Mother-Infant Behavioral Interactions Behavior

Description

Grooming

Cleaning/grooming of infant by mother or vice-versa; includes scratching, biting, licking, or rubbing. Must be scored simultaneously with either Mutual Ventral or Social Contact.

Recorded as duration (seconds).

Mutual Ventral

Infant is belly-to-belly with mother and/or on the nipple. Infant cannot be in Social Contact with any other animal or engage in locomotion, but mother can. Recorded as duration (seconds).

Social Contact

Sitting, standing, locomoting, or lying within arms reach of mother or infant, depending on which is the focal animal. Social Contact is superseded by Mutual Ventral. Recorded as duration (seconds).

Reject/Withdrawal

Mother or infant rejects approaches made by the other for mutual ventral contact. Also scored if there is mutual ventral contact and one of the animals attempts to break but the other does not want to.

Recorded as frequency (number of occurrences).

between 0900 hr and 1600 hr. The behaviors of interest for our study were: Grooming between mother and infant, Mutual Ventral contact between mother and infant, Social Contact between mother and infant, and Reject/Withdrawal between mother and infant. The operational definitions and scoring criteria for these behaviors are outlined in Table 1 (the entire mother-infant ethogram is available upon request).

Infant Stress Reactivity Blood samples were obtained from each infant via femoral venipuncture on day (D) 14 and 30 and month (M) 2, M3, M4, and M5 of life. In all cases, the infants were hand-caught from their home groups. The D14 and D30 samples were obtained after the infants underwent a 30-minute neurobehavioral assessment that required handling, restraint, and gentle physical manipulation by a human experimenter (Schneider, Champoux, & Moore, 2006). The M2 samples were taken immediately after the infants were retrieved from their groups, and served as a relative baseline. The M3, M4, and M5 samples were obtained after a 30-minute period where each infant was isolated in a wire cage in a room out of tactile, visual, and auditory contact with all other animals and experimenters. Since blood sampling coincided with cerebrospinal fluid (CSF) sampling (blood was obtained before CSF), the infants were anesthetized with ketamine hydrochloride (10 mg/kg, IM) before any samples were taken.

Between months 6 and 8 of age, each infant underwent a 4-week social separation regimen. On D1 of this procedure, mother-infant pairs were hand-caught, physically separated from each other, and blood samples were taken immediately from the infants (baseline). Each infant was then individually held in a quadrant of a large primate cage along with three other maternally-separated infants with whom they shared auditory

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and olfactory, but limited visual and no tactile contact. At one hour post-separation, each infant was removed from its holding cage and another blood sample was taken (H1); after this sampling, the infants were returned to their respective holding cages.

Finally, a third blood sample was taken two hours post-separation (H2) in the same fashion as the H1 sampling. The Baseline, H1, and H2 blood samples were taken while the monkeys were fully awake, and provided the opportunity to assess acute stress effects on HPA axis activity. Following the H2 sampling, the infants were returned to their holding cages where they remained for three days. On day 4, each infant was anesthetized (15 mg/kg ketamine, IM) followed by blood and CSF sampling (H96); the H96 sampling provided the opportunity to assess the impact of a chronic stressor on HPA axis output. On D5, the infants were reunited with their mothers in their respective home groups, where they remained for three days. Following the 3-day reunion period, the 4-day separation and 3-day reunion sequence was repeated until a total of four full cycles was completed over the course of 28 days.

All blood samples were kept on ice until centrifugation (within three hours after extraction), after which the plasma was transferred to cyrotubes and immediately flash-frozen in liquid nitrogen. Samples were then stored in a –80° C freezer until shipped for assay. Levels of plasma adrenocorticotropic hormone (ACTH) and total cortisol were determined via radioimmunoassay by a commercial assay facility; interand intra-assay coefficients of variation were ≤ 10%. ACTH values were expressed in picograms per milliliter (pg/ml) and cortisol values were expressed in micrograms per deciliter (µg/dl).

Data Analyses Most of the infants studied were reared by multiparous mothers over successive years; specifically, the 120 infant subjects were reared by 78 different mothers. Of the 120 infants, a total of 57 (47.5%) were reared by primiparous mothers, whereas a total of 75 infants (62.5%) were reared by females who were or would later become multiparous. Maternal parity notwithstanding, the data from each mother-infant pair were considered independent of each other; therefore, each dyad was treated as an independent case for analyses. Data were analyzed using Analyses of Variance (ANOVA), paired-samples t-tests, planned least-significant difference (LSD) between-groups comparisons, and Pearson product-moment correlations as described in detail below.

Statistical significance was set at α = .05 for all analyses (2-tailed when applicable).

Mother-Infant Behavioral Interactions Since all of the behaviors analyzed involved interaction between mother and infant, and both members of each mother-infant pair were observed in immediate succession, the values for each behavior at each week were the sum of the combined 10-minute mother-infant scoring episode. The behavioral data were analyzed by post-natal month

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of the infant’s life, with the mean value per session during weeks 1–4 serving as the single data point for month 1, followed by the mean of weeks 5–8 representing M2, weeks 9–12 for M3, weeks 13–16 for M4, weeks 17–20 for M5, and weeks 21–24 for M6. Each behavior was analyzed via 3 × 6 mixed ANOVA with a between-groups factor of Mother’s Rearing (MR, SPR, or PR) and a within-group factor of Infant’s Age (1, 2, 3, 4, 5, and 6 months). Main effects of age were followed by paired-samples t-tests comparing overall means of consecutive months. All ANOVAs were then followed by planned LSD comparisons at each month to identify differences in maternal behavior as a function of how the mothers were reared.

Infant Stress Reactivity Separate one-way ANOVAs with a between-groups factor of Mother’s Rearing were performed on the ACTH and cortisol values at D14, D30, M2, M3, M4, and M5.

All ANOVAs were followed by planned LSD comparisons. For the social separations, the average of each infant’s ACTH and cortisol during Baseline, H1, H2, and H96 across all four separation cycles served as the data points for analyses (cf. Barr, Newman, Shannon, Parker, Dvoskin, & Becker, 2004). The ACTH and cortisol data were each analyzed via 3 × 4 mixed ANOVA with a between-groups factor of Mother’s Rearing and a within-group factor of Phase of separation procedure (Baseline, H1, H2, and H96). Main effects of Phase were followed by paired-samples t-tests comparing overall means of consecutive phases. Both ANOVAs were then followed by planned LSD comparisons at each phase.

Individual Differences A number of studies from the animal literature have demonstrated clear relationships between individual differences in early maternal behavior and subsequent stress reactivity in offspring. The best known and most widely reproduced relationship is the negative one between licking/grooming behavior in rat dams (Rattus norvegicus) and subsequent neuroendocrine responses to stress in their pups (see Meaney, 2001). However, individual differences in maternal care among nonhuman primates are regularly observed (Fairbanks, 1996; Maestripieri, Lindell, Ayala, Gold, & Higley, 2005), and in order to determine if analogous relationships existed in differentially-reared rhesus monkey mothers and their infants, a series of correlational analyses was conducted via Pearson product-moment correlations. Specifically, mean mother-infant grooming behavior during each month of each infant’s life was plotted against the infants’ corresponding ACTH and cortisol values for that month. Also, to assess whether early maternal care can predict stress reactivity in later infancy, month 1 grooming behavior was correlated with mean ACTH and cortisol responses to each phase of the separation procedure. All of the above mentioned correlational analyses were performed separately for infants of MR, SPR, and PR mothers.

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Results Mother-Infant Behavioral Interactions No significant main or interaction effects were produced by the grooming ANOVA (Fs < .376, ps > .222); however, the planned LSD comparisons showed the PR motherinfant pairs engaging in significantly more grooming behavior than the MR group during months 4 and 6 (ps < .044).

The Mutual Ventral ANOVA only yielded significant main effects of Infant’s Age and Mother’s Rearing (Fs > 3.375, ps < .039). Paired-samples t-tests revealed significant overall decreases in Mutual Ventral from months 1–2 and 2-3 (ts > 7.000, ps < .001), but no differences after M3 (absolute ts < .825, ps > .410). LSD comparisons revealed that the SPR mother-infant pairs spent more time in mutual ventral contact versus the MR group during M1 and versus the MR and PR groups during M4 (ps < .019).

The only significant term in the Social Contact ANOVA was Infant’s Age (F(5,535) = 23.317, p < .0000000001; all other Fs < .801, ps > .630). Paired-samples t-tests revealed a significant overall increase from M1–2 (t(119) = –10.455, p < .001), but no differences after M2 (absolute ts < 1.276, ps > .060). LSD comparisons showed no between-groups differences in Social Contact during any month.

As with Social Contact, the only significant term in the Rejections ANOVA was Infant’s Age (F(5,545) = 7.177, p < .000002; all other Fs < 1.681, ps > .104). Pairedsamples t-tests revealed significant overall increases from M2-M3 and M3-M4 (absolute t(199)s > 2.017, ps < .047), but no differences between M1-M2 or after M4 (absolute ts < 1.455, ps > .148). However, LSD comparisons showed that the PR mother-infant pairs engaged in more rejections than both the MR and SPR groups during months 3 and 5 (ps < .029). These and all other mother-infant behavioral interactions and group comparisons are summarized in Figure 1.

Infant Stress Reactivity The one-way ANOVAs for ACTH produced no significant main effects of Mother’s Rearing at D14, D30, M2, M3, M4, or M5 (Fs < 1.675, ps > .191); these findings were confirmed by the planned LSD comparisons (ps > .078). However, similar analyses of cortisol yielded a significant main effect at D14 (F(2,108) = 4.909, p = .009) and a trend at D30 (F(2,108) = 2.371, p = .098), but no effects at any other time point (Fs < 2.242, ps > .110). As illustrated in Figure 2, LSD comparisons showed that the infants of SPR mothers had significantly lower cortisol output versus infants of MR and PR mothers on D14 and versus infants of MR mothers on D30 (ps < .030; SPR vs. PR at D30 p = .059).

The mixed ANOVA on ACTH during the separation regimen generated only a significant main effect of Phase (F(3,345) = 136.823, p < .0000000001; all other Fs < 1.764, ps > .122). Paired-samples t-tests revealed a significant overall increase in ACTH output from Baseline-H1, and decreases from H1-H2 and from H2-H96; H96 was also significantly lower than Baseline (absolute ts > 4.334, ps < .001). LSD

Time Spent per Session (mean secs + SEM)

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Peer-Reared

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*†

Rejections

3

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*#

Mutual Ventral

5

*†

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FIGURE 1. Mother-infant behavioral interactions as a function of mother’s rearing condition. Overall mean levels of Grooming did not vary as a function of infant’s age; however, Mutual Ventral significantly decreased from M1-M2 and M2-M3, Social Contact increased from M1-M2, and Rejections increased from M2-M3 and M3-M4. Each MR, SPR, and PR bar represents the respective mean of 56–57, 23, and 31–32 mother-infant pairs. Within each month, significant difference versus the MR group is indicated by *, significant difference versus the SPR group is indicated by †, and significant difference versus the PR group is indicated by #.

Time Spent per Session (mean secs + SEM)

Grooming Time Spent per Session (mean secs + SEM) Number per Session (mean + SEM)

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PETER G. ROMA, ET AL. Infants’ ACTH

450

Mean pg/ml + SEM

370 290 210 130 50 D14

D30

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Infants’ Cortisol 60

Mean µg/dl + SEM

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† †

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44

36

*

28

20 D14

D20

M2 (Baseline)

Infants’ Age in Months Mother’s Rearing Condition Mother-Reared

Surrogate-Peer Reared

Peer-Reared

FIGURE 2. Physiological stress reactivity across infancy as a function of mother’s rearing condition. The top panel represents mean plasma ACTH values, the bottom panel represents mean plasma cortisol values. The D14 and D30 samples were taken after an experimenter-administered 30-minute neurobehavioral assessment, the M2 Baseline sample was taken immediately after capture, and the M3, M4, and M5 samples were taken after a 20-minute isolation stress challenge. Each MR, SPR, and PR bar represents the respective mean of 56–62, 23–26, and 29–32 infants. Within each time point, significant difference versus the MR group is indicated by *, significant difference versus the SPR group is indicated by †, and significant difference versus the PR group is indicated by #.

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comparisons showed that the infants of SPR mothers had significantly lower ACTH versus infants of MR mothers at H2 only (p = .016; other ps > .054).

The mixed ANOVA of separation-induced cortisol also only yielded a significant main effect of Phase (F(3,351) = 555.648, p < .0000000001; all other Fs < .706, ps > .645). Paired-samples t-tests revealed significant increases from Baseline-H1 and H1H2 as well as a significant decrease from H2-H96; H96 was also significantly higher than Baseline (absolute ts > 5.631, ps < .001). LSD comparisons revealed no betweengroups differences in cortisol output at any phase of the separation procedure (ps > .232). The results of the separation analyses are depicted in Figure 3.

Individual Differences The results of the correlational analyses are summarized in Tables 2 and 3. Monthly grooming rates were generally not associated with infant HPA axis activity at each month; however, grooming during the first month of life was positively correlated with D30 cortisol output among infants of MR females (r (59) = .530, p = .000016) and negatively correlated with D30 ACTH output among infants of PR females (r (29) = –.491, p = .007; all other absolute rs < .305, ps > .138). A dissociation between grooming during the 1st month of life and infants’ subsequent responses to separation stress was also observed, except for a modest but significant positive relationship with H2 ACTH levels among the infants of SPR mothers (r (26) = .444, p = .023; all other rs < .317, ps > .077). The statistically significant relationships between maternal care and infant stress reactivity are presented in Figure 4.

Discussion The purpose of this study was to explore the influence of contemporary laboratory rearing conditions on maternal behavior in adult rhesus monkeys and to determine how rearing effects may impact biobehavioral development in these mothers’ infants.

Given the fairly comprehensive collection of variables and the relatively large sample size, perhaps the most striking result was the general lack of differences in maternal behavior or infant stress reactivity as a function of maternal rearing condition. Especially in light of the original motherless-monkey work and more recent investigations of potentially detrimental effects of nursery rearing (e.g., Barr et al., 2004; Bastian, Sponberg, Suomi, & Higley, 2003; Higley, Suomi, & Linnoila, 1992), it is somewhat surprising that even the mother-reared mothers failed to emerge as superior caretakers, if not producers of infants with superior coping skills.

The behavioral data showed that all three groups of mothers engaged in generally species-normative patterns of interaction with their infants, exhibiting high levels of mutual ventral contact in early infancy, giving way to increasing levels of social contact, and culminating in increased rejections as weaning approached. The most patent deviation from the overall pattern among these behaviors was in the PR mothers’ tendency to reject their 3–5-month old infants with a frequency reserved by the other two

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Hr 1

Phase of Separation Mother’s Rearing Condition Mother-Reared

Surrogate-Peer Reared

Peer-Reared

FIGURE 3. Infants’ physiological stress reactivity to a social separation procedure as a function of mother’s rearing condition. The top panel represents mean plasma ACTH values while the bottom panel represents mean plasma cortisol values from blood sampled immediately after capture (Baseline) and 1, 2, and 96 hours post-separation.

Each MR, SPR, and PR bar represents the respective mean of 56–62, 23–26, and 29– 32 infants. Within each time point, significant difference versus the MR group is indicated by *, significant difference versus the SPR group is indicated by †, and significant difference versus the PR group is indicated by #.

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Infants’ HPA Axis Responses at Corresponding Month of Life Infants of MR Mothers

Grooming During Infants’ Month of Life

ACTH

1 2 (Baseline) 3 4 5

.023 –.207 –.146 –.080 –.105

Infants of SPR Mothers

Cortisol .530*** .001 –.022 .211 .148

ACTH

Cortisol

–.041 .304 .002 .065 –.081

.129 .091 .144 –.174 .179

Infants of PR Mothers ACTH –.491** –.124 –.252 .291 .291

Cortisol .164 –.157 .138 –.024 .093

Note: Each value represents Pearson r correlation coefficient. Significant correlations are in bold: **p = .007, ***p = .000016.

Table 3. Relationships between M1 grooming and infant HPA axis responses to separation stress.

Relationship with M1 Grooming Infants of MR Mothers

Infants of SPR Mothers

Infants of PR Mothers

Phase of Separation Procedure

ACTH

Cortisol

ACTH

Cortisol

ACTH

Cortisol

Baseline Hour 1 Hour 2 Hour 96

.089 .123 .048 –.050

.119 .177 .013 .126

.046 .266 .444* –.023

–.044 .098 .294 .255

.182 .143 .172 –.070

.316 .307 .243 .277

Note: Each value represents Pearson r correlation coefficient. Significant correlation is bolded (p = .023).

groups for month 6. However, and somewhat paradoxically, the PR mothers also engaged in more grooming behavior than their MR counterparts during the latter half of their infants’ rearing. It is uncertain why this pattern appeared—one possibility is that the PR monkeys’ propensity for physical contact could have provoked more rejection responses from their MR infants as the infants grew increasingly independent—but perhaps a more relevant question than “why?” is “did it matter?”, and at least in terms of infant stress reactivity, our physiological data suggest that it did not.

The HPA axis data were concordant with the behavioral data in that no one group of infants appeared particularly well- or ill-suited to cope with the isolation and separation stress challenges. The infants of PR mothers did not differ from their MR or SPR counterparts in HPA axis reactivity during the later months when PR mothers rejected their infants more frequently. In fact, infants of PR mothers involved in relatively high levels of grooming during the first month of life showed relatively low ACTH levels that month, whereas infants of high-grooming MR mothers actually showed increased cortisol levels (see Figure 4). The former result echoes the rodent literature if one assumes linear causality between maternal grooming and infant HPA

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Individual Differences in Maternal Care and Infant Stress Reactivity Infants’ Day 30 ACTH Mother-Reared Mothers

1050 900 750 600 450 300 150 0

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FIGURE 4. Individual differences in maternal care and infant stress reactivity. Individual differences in mother-infant Grooming during the infant’s first month of life served as the predictor variable for these graphs. Each column of graphs corresponds to a different outcome variable among the infants of MR (●, n = 56–62), SPR (▲, n = 23–26), or PR (■, n = 29–32) mothers, respectively. Statistically significant correlations within any combination of outcome variable and mother’s rearing condition are indicated by an underlined graph title.

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Individual Differences in Maternal Care and Infant Stress Reactivity Infantsâ&#x20AC;&#x2122; Day 30 Cortisol Mother-Reared Mothers

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r (59) = .530, p = .000016

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Mean Grooming per Session During Infantsâ&#x20AC;&#x2122; 1st Month of Life

FIGURE 4. (Continued)

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Individual Differences in Maternal Care and Infant Stress Reactivity Infants’ Hr 2 ACTH During Separations Mother-Reared Mothers

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FIGURE 4. (Continued)

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axis reactivity (cf. Francis, Diorio, Liu, & Meaney, 1999); however, the latter result is less readily explained, unless already high-reactive infants of MR mothers tended to elicit more maternal grooming than their low-reactive peers (cf. Stern, 1997). This interpretation is difficult to verify with our existing dataset, but seems reasonable given the fact that infants of MR and PR mothers did not actually differ at the group level in their mean D14 or D30 HPA measures.

In addition to the early grooming correlations, perhaps the most intriguing result of the HPA analyses was the relationship between infants of MR and SPR mothers at the D14 and D30 samplings. In their 1998 study employing the same procedures as those we used, Shannon et al. reported significantly higher cortisol values in MR versus nursery-reared infants that were virtually identical (within 5 µg/dl) to those seen in our infants of MR and SPR mothers (see their Figure 1 and our Figure 2 bottom panel). The critical point here is that all of the infants in our study were mother-reared, yet the infants of MR and SPR mothers exhibited cortisol patterns resembling those produced by their mothers’ rearing conditions.

Since the patterns of early cortisol reactivity Shannon et al. reported were produced by the rearing conditions to which the monkeys were assigned, they cannot be primarily attributed to genetic factors. To account for their findings, Shannon et al. argued quite sensibly that MR infants were not only subjected to the stress of the neonatal assessment procedure, but to the stress of capture and maternal separation, whereas the nursery-reared infants were more acclimated to human handling and did not experience disruptive capture and separation. However, the infants in our study were all assigned to the same mother-reared environment, so there were no differences in procedure that could account for our findings. Nonetheless, the pattern of early cortisol reactivity in infants of SPR mothers was still identical to their own mothers and different from the infants of MR mothers. Taken together, these results suggest a crossgenerational transmission of early stress reactivity, but by different non-genomic means for both acquisition in SPR mother and transmission to her MR infant.

The patterns of early stress reactivity in MR and SPR mothers can be explained by their own differential rearing, but the identical patterns seen in their mother-reared infants cannot. This point coupled with the fact that the first month of a rhesus infant’s life is spent almost exclusively on or in very close proximity to mother leaves maternal behavior as the most likely means of cross-generational transmission. Although mother-infant grooming behavior did not vary as a function of mother’s rearing, the SPR mothers did engage in more mutual ventral contact with their infants during the first month of life compared to their MR and PR counterparts—a pattern that corresponds inversely with the D14 and D30 cortisol data. More conclusive verification of this relationship would, of course, require further study, but as conceptually intriguing as these findings might be, there still remains the issue of functional consequences. As with the behavioral tendencies produced by the mothers’ differential rearing, the apparent cross-generational alterations in their infants’ early HPA axis regulation were inconsequential when challenged later in infancy.

So overall, what can we conclude about modern laboratory-rearing effects on maternal behavior and infant stress reactivity in rhesus monkeys? Generally, it appears that the mother-rearing, surrogate-peer rearing, and peer-rearing conditions utilized

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at LCE do not produce aberrant patterns of maternal care in socially-housed adult females, or enduring effects on stress reactivity in their offspring. Whether or not this news is surprising, it is certainly welcome, especially to those with more than a principled interest in nonhuman primate health and well-being. This conclusion is all the more persuasive considering the purposely liberal statistical approach used to analyze the data. That is, the planned comparisons all sought the least significant difference between means; however, none of the ANOVAs actually yielded significant interaction terms involving Mother’s Rearing. Moreover, the only ANOVAs with significant main effects of Mother’s Rearing that would have warranted unplanned post-hoc comparisons were Mutual Ventral and D14 cortisol, and of those analyses the only differences to survive even Tukey type I error correction are the SPR mothers engaging in more mutual ventral than MR at M1 and both other groups at M4, as well as infants of MR mothers producing higher D14 cortisol than infants of SPR mothers.

Although our data indicate reproductively successful outcomes in differentially reared monkey mothers and relatively normal development in their infants, it is important to note that these data do not suggest that nursery-rearing is superior to motherrearing. Among other reasons, the use of nursery-reared monkeys continues to prove valuable for the study of development as well as gene-environment interaction effects on behavior and physiology (Barr, Newman, Becker, Parker, Champoux, & Lesch, 2003). However, nursery-rearing got its start and is still often employed as a model of early-life stress through compromised attachment relationships and unguided early socialization. Although the days of isolate rearing have long since passed, compared to mother-rearing, even modern nursery-rearing has been shown to produce deficits in central nervous system function and HPA axis regulation (Higley, Suomi, & Linnoila, 1992), as well as increasing adult risk of low social dominance, aggressive behavior, and excessive alcohol consumption (Bastian et al., 2003; Higley, Hasert, Suomi, & Linnoila, 1991; Newman et al., 2005). However, like Harlow’s motherless-mother studies from so many years ago, what our study of rhesus monkey mothers demonstrated is that despite the potential risks conferred by contemporary nursery-rearing in other biobehavioral domains, a stable, species-appropriate social environment may facilitate competent reproductive and maternal function—arguably the most important constellation of behaviors for any animal—with no apparent detrimental long-term consequences for the infants, at least over their first six months of life.

Indeed, it is a rather complex process to determine if laboratory rearing conditions affect later maternal behavioral interactions and if, in turn, maternal behavior in differentially reared animals affects their infants’ biobehavioral responses to stress. Nevertheless, in the case of mother-reared, surrogate-peer-reared, and peer-reared rhesus monkey mothers, we can take comfort in the simple fact that normal maternal behavior appears to be surprisingly resilient, and that ultimately, the kids are alright.

References Agid, O., Kohn, Y., & Lerer, B. (2000). Environmental stress and psychiatric illness. Biomedicine & Pharmacotherapy, 20, 135–141.

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Barr. C. S., Newman, T. K., Becker, M. L., Parker, C. C., Champoux, M., Lesch, K. P., et al. (2003).

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Barr, C. S., Newman, T. K., Shannon, C., Parker, C., Dvoskin, R. L., Becker, M. L., et al. (2004).

Rearing condition and rh5-HTTLPR interact to influence limbic-hypothalamic-pituitaryadrenal axis response to stress in infant macaques. Biological Psychiatry, 55, 733–738.

Bastian, M. L., Sponberg, A. C., Suomi, S. J., & Higley, J. D. (2003). Long-term effects of infant rearing condition on the acquisition of dominance rank in juvenile and adult rhesus macaques (Macaca mulatta). Developmental Psychobiology, 42, 44–51.

Brake, W. G., Zhang, T. Y., Diorio, J., Meaney, M. J., & Gratton, A. (2004). Influence of early postnatal rearing conditions on mesocorticolimbic dopamine and behavioural responses to psychostimulants and stressors in adult rats. European Journal of Neuroscience, 19, 1863–1874.

Champoux, M., Byrne, E., DeLizio, & Suomi, S. J. (1992). Motherless mothers revisited: Rhesus maternal behavior and rearing history. Primates, 33(2), 251–255.

Christoffel, K. K., & Forsyth, B. W. (1989). Mirror image of environmental deprivation: Severe childhood obesity of psychosocial origin. Child Abuse & Neglect, 13(2), 249–256.

Fairbanks, L. A. (1996). Individual differences in maternal styles: Causes and consequences for mothers and offspring. Advances in the Study of Behavior, 25, 579–611.

Francis, D., Diorio, J., Liu, D., & Meaney, M. J. (1999). Nongenomic transmission across generations of maternal behavior and stress responses in the rat. Science, 286, 1155–1158.

Goeders, N. E. (2003). The impact of stress on addiction. European Neuropsychopharmacology, 13(6), 435–441.

Heim, C., Plotsky, P. M., & Nemeroff, C. B. (2004). Importance of studying the contributions of early adverse experience on neurobiological findings in depression. Neuropsychopharmacology, 29, 641–648.

Higley, J. D., Hasert, M. F., Suomi, S. J., & Linnoila, M. (1991). Nonhuman primate model of alcohol abuse: Effects of early experience, personality, and stress on alcohol consumption.

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Higley, J. D., Suomi, S. J., & Linnoila, M. (1992). A longitudinal assessment of CSF monoamine metabolite and plasma cortisol concentrations in young rhesus monkeys. Biological Psychiatry, 32, 127–145.

Maestripieri, D., Lindell, S. G., Ayala, A., Gold, P. W., & Higley, J. D. (2005). Neurobiological characteristics of rhesus macaque abusive mothers and their relation to social and maternal behavior. Neuroscience and Biobehavioral Reviews, 29, 51–57.

McIntosh, J., Anisman, H., & Merali, Z. (1999). Short- and long-periods of neonatal maternal separation differentially affect anxiety and feeding in adult rats: Gender-dependent effects. Brain Research: Developmental Brain Research, 113(1-2), 97–106.

Meaney, M. J. (2001). Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generation. Annual Review of Neuroscience, 24, 1161–1192.

Newman, T. K., Syagailo, Y. V., Barr, C. S., Wendland, J. R., Champoux, M., Graessle, M., et al.

(2005). Monoamine oxidase A gene promoter variation and rearing experience influences aggressive behavior in rhesus monkeys. Biological Psychiatry, 57, 167–172.

Novak, M. A., & Sackett, G. P. (2006). The effects of rearing experience: The early years. In G. P. Sackett, G. C. Ruppenthal, & K. Elias (Eds.), Developments in primatology: Progress and prospects: Vol. 2. Nursery rearing of nonhuman primates in the 21st century (pp. 5–19). New York: Springer-Verlag.

Ruppenthal, G. C., Arling, G. L., Harlow, H. F., Sackett, G. P., & Suomi, S. J. (1976). A 10-year perspective of motherless-mother monkey behavior. Journal of Abnormal Psychology, 85(4), 341–349.

Sackett, G. P., Ruppenthal, G. C., & Davis, A. E. (2002). Survival, growth, health, and reproduction following nursery rearing compared with mother rearing in pigtailed monkeys (Macaca nemestrina). American Journal of Primatology, 56, 165–183.

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Sánchez, M. M., Ladd, C. O., & Plotsky, P. M. (2001). Early adverse experience as a developmental risk factor for later psychopathology: Evidence from rodent and primate models. Development and Psychopathology, 13, 419–449.

Schneider, M. L., Champoux, M., & Moore, C. F. (2006). Neurobehavioral assessment of nonhuman primate neonates. In G. P. Sackett, G. C. Ruppenthal, & K. Elias (Eds.), Developments in primatology: Progress and prospects: Vol. 2. Nursery rearing of nonhuman primates in the 21st century (pp. 215–247). New York: Springer-Verlag.

Shannon, C., Champoux, M., & Suomi, S. J. (1998). Rearing condition and plasma cortisol in rhesus monkey infants. American Journal of Primatology, 46, 311–321.

Stern, J. M. (1997). Offspring-induced nurturance: Animal-human parallels. Developmental Psychobiology, 31, 19–37.

Suomi, S. J., & Ripp, C. (1983). A history of motherless mother monkey mothering at the University of Wisconsin Primate Laboratory. In M. Reite, & N. G. Caine (Eds.), Child abuse: The nonhuman primate data. New York: Alan Liss.

Vanitallie, T. B. (2002). Stress: A risk factor for serious illness. Metabolism, 51(6, Supplement 1), 40–45.

Author Note We are grateful to Courtney Shannon, Stephen Lindell, and our many other colleagues and friends for their tireless efforts in data collection and management, veterinary and animal care, and facilities maintenance throughout the years.

This project was supported by intramural funds from the National Institute of Child Health and Human Development and the National Institute on Alcohol Abuse and Alcoholism/National Institutes of Health/Public Health Service/US Department of Health and Human Services.

Correspondence concerning this article should be addressed to Pete Roma, Department of Psychology, American University, 4400 Massachusetts Ave. NW, Washington, DC 20016. Email: PeteRoma@gmail.com.

The Literacy of Interaction: Are Infants and Young Children Receiving a “Mental Diet” Conducive for Future Learning?

Pnina S. Klein School of Education Bar-Ilan University Ramat-Gan, Israel

Abstract: There is a plethora of research on environmental effects on the development of infants and young children, and a general consensus regarding several basic requirements for quality of early education and care. However, there are still many questions that remain relatively unanswered, particularly in relation to parental teaching behavior, which is one of the major objectives of adult-child interactions. Three main types of such questions are as follows: 1. What are the specific processes within adults’ teaching (mediation) behavior in interactions with young children that may have an effect on their potential to learn from new experiences?

2. How do these processes affect children’s flexibility of mind (readiness to learn)?

3. What are the differential expressions and potential effects of these components on children with special needs and with populations of children and families in different cultures?

Possible answers to these questions are suggested in this paper from the theoretical perspective of a developmental mediation approach, focusing on the quality of adult-child interaction and on ways to understand and enhance it. Implications for early education policy are discussed in light of current research.

Are Infants and Young Children Receiving a “Mental Diet” Conducive for Future Learning?

One of the central challenges of education in the 21st century is to prepare children to live in a rapidly changing world, requiring constant adjustment and flexibility of mind. The latter may be defined as the capacity to benefit from new learning experiences, or as readiness to learn. There is a general consensus, based on extensive research documentation, that adult-child interactions are of central importance and that quality care of young children should consist of a mental diet including warmth, nurturance, and stability (for example, see the review by Shonkoff & Phillips, 2000). This

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generalization can be made despite marked heterogeneity of children, their families and the education and care service they receive. In light of all the latter, it seems highly important to focus on variables that represent the quality of that interaction including variables of adults’ teaching behavior (mediation), which constitute a universal major component of adult-child interactions. Despite the consensus in child development literature regarding the important role played by adult-child interactions, research on adults’ teaching behavior in interactions with young children is still scarce.

This paper focuses on adult-child interactions, particularly on adults’ teaching behavior in their interactions with very young children and on the potential effects of these behaviors on children’s readiness to learn. There is a theory-based model and research supporting the assumption of causal relationships between certain types of behavior or characteristics of adult-child interaction that affect children’s socialemotional and cognitive behavior and that create learning experiences that are potentially contributive to children’s flexibility of mind (Feurstein, 1980; Vygotzky, 1978).

The role of these factors has been studied in various cultures and with different populations of children and families with special needs (Klein, Wieder, & Greenspan, 1987, Klein, 1996; Klein & Alony, 1993; Klein, 2001b; Klein & Rye, 2004; Chiswanda, 1997). In these studies, mediational behaviors of parents (teachers or other adults) were defined, and their frequency and manner or style of appearance were identified. The identified mediational behaviors were found to be significantly related to children’s learning processes and consequently to their cognitive and socialemotional behavior (Feuerstein, 1979, 1980; Tzuriel, 1999; Klein, 1996; Klein, Feldman, & Zarur, 2003; Klein & Rye, 2004). This effect was explained as a consequence of changes occurring in children’s need systems, including, for example, the need to focus and perceive things clearly; the need to investigate things and to ask questions; to make associations between things; to compare and contrast; to complete a task or an action; to please others; to succeed at an objective; and to organize and to plan activities. How does such a need system develop?

From Theory to Research and Practical Implications There is a theoretical base (Feuerstein, 1979, 1980) and empirical data (Klein, Wieder, & Greenspan, 1987; Klein, 1988, 1991; Tzuriel, 1999) suggesting that specific characteristics of adult interaction with children constitute mediational behavior and may affect children’s predisposition to learn from new experiences. Mediated learning, as distinct from direct learning through the senses, occurs when the environment is interpreted for the child by another person who understands the child’s needs, interests, and capacities, and who takes an active role in making components of that environment, as well as past and future experiences, compatible with the child. Mediation affects the individual’s present learning and may improve his or her opportunity to learn from future experiences.

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Elements of Mediation Basic elements of what constitutes a teaching mediational interaction between a caregiver and a young child have been identified (Feuerstein, 1979, 1980). The most salient of these factors are empirically defined (Klein, Raziel, Brish, & Birenbaum, 1987; Klein, Wieder, & Greenspan, 1987; Klein, 1988, 1991) and are presented in Table 1.

It was found that the factors of quality mediation predicted cognitive outcome measures up to four years of age better than the children’s own cognitive test scores in infancy, or other presage variables related to pregnancy, birth histories, and mothers’ education (Klein, Wieder, et al. 1987). Similar findings were reported for a sample of very low birth weight infants (Klein, Raziel et al. 1987).

Intercorrelations between mothers’ mediational behaviors over time (when their children were 6, 12, 24, and 36 months old), were moderate to high. The average interjudge reliability for assessing these behaviors was considerably high in studies of American families of low socioeconomic status (Klein, Wieder et al. 1987) and Israeli mother-infant samples (Klein & Alony, 1993).

Similar studies were carried out in Ethiopia, Sri Lanka, Indonesia, USA, Sweden, and Israel (Klein, 1996). A study designed to examine the sustained effects of modifying the mother-infant mediational interaction on infants’ cognitive test performance and behavior was carried out in Israel. This study will be referred to as the Israeli follow-up study.

The research design of the Israeli follow-up study included random assignment to the experimental and control groups; an observational assessment of maternal mediation; a baseline assessment of the infants’ developmental status, using Bayley’s Mental Development Scales, prior to training mothers in mediational strategies; and a follow-up evaluation of experimental versus control mothers and children one year and three years after the termination of training.

The total study sample consisted of 68 families in a small, low income status urban community in Israel, who were randomly assigned to an experimental and control group. This community was singled out for intervention by the Ministry of Education and the Office of Welfare due to the high proportion of children who had poor schoolreadiness skills and a significant high school dropout rate.

Activities developed for the experimental group were based on the Mediational Intervention for Sensitizing Caregivers (MISC) process, which is described in detail later in this article. These activities were designed to improve mothers’ mediation to their children. The level of mediation was defined by the frequency of appearance, sequence and synchrony of maternal mediating behaviors, and their children’s responsiveness. Mothers were trained at home by paraprofessional “mediators” and supervised by professional developmental psychologists. Mothers were actually helped to “read” their interactions with their children, to understand their own behavior and their children’s responses, as well as the potential consequences of these interactions.

Intervention was terminated when mothers improved their mediation and could verbally define the basic components of the parental behaviors targeted by the intervention.

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Table 1. Definitions and Examples of Basic Criteria of Parental Mediation and Affected Needs Mediation Processes

Examples of the Process

Intellectual Needs

Social-Emotional Needs

1. Focusing Any act or sequence of acts of an adult that appear to be directed toward affecting a child’s perception or behavior.

These behaviors are considered reciprocal when the infant or child in the intervention responds, vocally, verbally, or nonverbally.

Making the environmental stimuli compatible to the child’s needs, e.g., bringing closer, covering distractions, repeating, sequencing, grouping, helping the child focus, see, hear and feel clearly.

Need for precision in perception (vs. scanning exploration).

Need to focus on and decode facial and body expressions of emotion.

Need for precision in expression.

Need to modify one’s own behavior or the environment in order to mediate to others (to make the other person see or understand).

2. Exciting Behavior that expresses verbal or nonverbal excitement, appreciation, or affect in relation to objects, animals, concepts, or values.

Expressing excitement Need to search for meaningful new experiences vocally, verbally or non(i.e., listen, look, taste, things that remind one of past verbally over experiences, experiences). objects, people, etc.

Need to respond in a way that conveys meaning and Naming, identifying. excitement (sound, look and feel excited) and meaningful activities.

3. Expanding Behavior directed toward the expansion of a child’s cognitive awareness, beyond what is necessary to satisfy the immediate need that triggered the interaction.

Explaining, elaborating, associating and raising awareness to metacognitive aspects of thinking.

Need to go beyond what meets the senses. Seek out further information through exploration

Relating past present and future experiences.

Request information from other people and from other sources.

Relating to physical, logical, or social rules and Need to seek framework. generalizations.

Need to link, to associate, to recall past information and anticipate future experiences.

4. Encouraging Verbal or nonverbal behavior that expresses satisfaction with a child’s behavior and that identifies a specific component or components of the child’s behavior which contribute to the experience of success.

Praise in a way that is meaningful to the child.

Need to seek more success experiences.

Clear isolation and identification of the reasons for success.

Need to summarize one’s own activities and determine what led to success.

5. Regulating Behavior Behaviors that model, demonstrate, and/or verbally suggest to the child regulation of behavior in relation to the specific requirements of a task, or to any other cognitive process required prior to overt action.

Regulation with regard to speed, precision, force, and preferred sequence of activities.

Well timed in relation to the experience.

Need to think about one’s own feelings and the feeling of others Need cause and effect sequences in social interaction.

Need to associate between experiences, to recall past information and anticipate future experiences.

Need to please others and gain more mediated feelings of competence.

Need to identify what pleases different people.

Need to provide others with mediated feelings of competence.

Need to plan before acting, e.g., need to consider possible solutions prior to responding.

Need to control one’s impulses in social situations.

Learn acceptable ways of expressing one’s emotions (i.e., regulate Need to pace one’s activities. the pace and intensity of one’s social responses to Need to regulate the level anger and joy). of energy invested in any given task.

Clarifying goals, meeting subgoals.

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In the experimental group, these behaviors were represented by the criteria of mediation, and in the control group, by basic aspects of a stimulating, responsive, non-punitive environment.

Since mediation was found to affect children’s cognitive functioning (including perception, elaboration, and expressive processes), it was expected that maternal mediation behaviors (e.g., focusing, showing affect, and expanding) would affect children’s vocabulary and abstract reasoning and, in general, prepare children to perform better in situations requiring “new learning,” such as tasks requiring immediate sequential memory. Thus, children’s cognitive performance was assessed using the following measures: Peabody Picture Vocabulary Test (PPVT), the auditory reception, visual reception, visual association, auditory association, and auditory sequential memory of the Illinois Tests of Psycholinguistic Abilities (ITPA), as well as the Beery and Bucktanika test of visual motor integration. In addition, children’s behavior during the play interactions with their mothers’ was video recorded and analyzed.

Comparison of the two groups on the separate components of each mediation factor, three years following the intervention, revealed that the mothers who participated in the intervention, (i.e., learned to “read” their interactions with their children), showed significantly more mediation behaviors (Klein & Alony, 1993).

Significant differences in favor of the children in this group were found on the PPVT, auditory reception and auditory association measures. The average PPVT IQ for the experimental group was 101 (SD = 15.5), and for the control group, 84 (SD = 14.1).

Of all factors of maternal mediation, mothers’ expanding and rewarding behaviors were most frequently related to children’s cognitive performance. Within these two types of behavior, maternal request for expansion of ideas (i.e., “Does it remind you of anything?”, “What is it like?”) and mediation of competence with explanation (rather than simply saying “Good,” “Fine,” etc.) were singled out as most significantly related to the children’s cognitive performance at age four. These findings coincide with those reported by Collins (1984), identifying the variable of “demandingness” as one of the most essential determinants of the quality of “good” family environments.

Similarly, Heath (1983) suggests that demanding from children that they reconstruct experiences verbally, (i.e., asking young children to tell about their experiences) may enhance their thinking and language development. Children’s expressions of affect were most significantly related to all criteria of maternal mediation, but mostly to maternal rewarding behaviors, maternal expansion of ideas, and maternal request for “affect,” that is, attempts to arouse signs of excitement in relation to anything or anyone.

Focusing behavior in isolation from the other mediational behaviors (e.g., only catching of attention) was not significantly related to any of the cognitive outcome measures. A noteworthy relationship was found between the children’s performance and the mothers’ nonverbal expression of feelings. Mothers’ expressions of feelings were also found to be related to children’s spontaneous provision of rewards to others.

The mediational approach applied in the follow-up study was not designed to improve children’s performance on specific cognitive tasks. Yet, three years following the termination of the intervention, children in the experimental group outscored the children in the control group with regard to language performance as measured by the PPVT and two measures of verbal reasoning. These findings suggest that children from poor families who participated in the intervention were brought well within the

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normal range of verbal performance. Mothers in the intervention group expressed higher aspirations for their children’s intellectual growth, as well as a more flexible and balanced view of the factors they thought were important for their children’s future development. Provision of external rewards was traditionally criticized in educational literature (e.g., LeVine, 1980; Lepper, 1981). In the Klein and Alony (1993) follow-up study, verbal or gestural praise contributed favorably to children’s cognitive and social-emotional development, but only when it was accompanied by explanations relating “success” to its causes or associating it with other experiences. Young children depend on adults for mediation of competence. Quality mediation requires recognition of children’s individual needs, including those related to the frequency, intensity, and type of reward they may require.

It has been well established in psycho-educational literature that children from poor families generally score lower on a variety of cognitive measures related to intelligence and academic performance as compared to middle-class children. Mothers’ intelligence or years of schooling were repeatedly pointed out as powerful predictors of children’s cognitive performance. The following finding from the mediational intervention and follow-up study is of special interest in view of the preceding facts. The correlation between mothers’ years of schooling and their mediation to their infants and young children prior to the intervention was almost identical to that found in the intervention and the comparison group (for the intervention groups, r = .43, and for the control group, r = .45). Three years following the intervention, the correlation between mothers’ years of schooling and the mothers’ mediation went down (to .21) in the intervention group, while remaining almost constant (r = .42) for the comparison group. Furthermore, the correlation between mothers’ years of schooling and children’s Bayley’s Mental Development Scales for both groups prior to the intervention was .36. Following the intervention, the correlation between mothers’ years of schooling and children’s PPVT scores was .23 for the intervention group and .41 for the comparison group. These findings suggest that the quality of maternal mediation can be modified. Once modified, the link between mothers’ schooling and their behavior in interactions with their children can be modified as well, resulting in blocking of the commonly found link between mothers’ education and children’s cognitive achievements. Poor mothers (and other caregivers and educators) can improve their mediation and contribute to their children’s cognitive development as well as middle-class mothers. The effectiveness of the mediational approach with populations of very poor children was demonstrated in Sri Lanka (Fugelsang & Chandler, 1996), in Indonesia (Hundeide, 1996) and recently, following a 12-year intervention project, in Ethiopia (Klein, 2001a; Klein & Rye, 2004).

Typical Profiles of Mediation in Special Populations The mediational approach was used with populations of children with special needs, including children born at very low birth weight (Klein, Raziel et al., 1987), children with Down Syndrome, and very young gifted children (Klein, 1996). A specific pattern of mediation was frequently noted for parents who believed in their abil-

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ity to help their children overcome their developmental problems and who were highly motivated to act toward achieving that goal. For example, parents of very low birth weight (VLBW) children showed disproportionately high frequencies of focusing behaviors which were unmatched by high frequencies of other mediational behaviors, i.e., showing affect, expanding, encouraging, and regulation of behavior. It was as though those parents were highly motivated to interact with their children but were not aware of the need to associate meaning to whatever was focused on. As a result, they did not provide them with meaningful sequences of mediation. Instead, they focused and refocused their children’s attention on objects or people in their environment, but did not enable them to use the focused attention in order to obtain meaning, expand experiences, and experience success. Even brief mediational interventions with populations of VLBW children and their parents led to significant improvement in parental mediation and consequently to the enhancement of cognitive performance of the children (Klein, Raziel et al. 1987).

In a study on the development of pre-verbal communication, 80 dyads of parents and infants, including 40 infants with Down Syndrome and 40 infants who were developing normally, the infants were followed from the age of 7 months to 22 months (Klein & Rosenthal, 2002). The developmental patterns of pre-verbal communication of the babies were matched with the profiles of mediation provided by their mothers.

Children with Down Syndrome were found to be jeopardized twice, once due to the syndrome causing a slower rate of development, and again due to poor mediation provided by the mothers. Major differences between interactions of mothers with typically developing infants and the interactions of mothers with Down Syndrome infants emerged around the age of 14–16 months. At that age, significant gaps were found in the development of Down Syndrome infants as compared to typically developing infants. Mothers of Down Syndrome infants showed an excess of focusing behavior and regulation of behavior with minimal affecting and expansion (e.g., expressing meaning, explaining, and making associations).

Modifications of the mediational approach are introduced to meet the special needs of young children with PDD (Pervasive Developmental Disorders). For example, their parents are guided to mediate affect frequently and in an exaggerated manner in order to open and close circles of communication with their children. In addition, they are helped to mediate affect by associating meaning with whatever the child does, even if the child’s behavior seems unrelated to any intent or lacking in meaning.

These patterns of mediation are meant to create associations between actions and their purpose and lead to the development of the spontaneous formation of such associations in the future (Greenspan & Wieder, 1996).

Parents of young gifted children appear to use a mediational style that is characterized by higher frequencies of mediation in the form of questions rather than giving of information. It appears that these parents repeatedly ask their children to verbally reconstruct experiences they have had or to reply to questions about them. In other words, parents of gifted children actively demand the “exercising” of their children’s thinking (Moss, 1992).

Extreme poverty has been found to result in a general decrease in mediation, particularly in mediation of affect and expansion. Parents preoccupied with daily worries

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about the mere survival of their family may not have enough mental energy to invest in expressions of excitement related to objects or events in the environment or to associate those experiences with others in the child’s past or future. Thus, it is possible that the cycle of poverty is perpetuated, since one of the types of mediation most conducive to cognitive development as well as school achievement, is missing in parental mediation to these young children.

Cross-Cultural Differences in Styles of Mediation: Analytical and Holistic Styles of Mediation Two general styles of mediation, a Western, analytic style and a traditional, holistic style, were identified following studies of mediational experiences in six cultures (Klein, 1996). The analytical style is frequently used by parents in Western cultures and is guided primarily by the objective of teaching the infant about objects available in his or her environment. The holistic approach is typically used in the so-called “traditional societies” in developing countries (Hundeide, 1996). Parents do not attempt to fragment experiences in an analytical way for the child. The child learns through participation in the life experiences of the family and acquires the meaning of things holistically. There are very few experiences of expansion; most interactions with adults are not decontexualized (i.e., not explored beyond the immediate context).

These children may be well equipped to adjust to life in their traditional native community, but they are not ready to cope with the Western style of education that requires experiences of analytic mediation. Western children are equally unprepared to live in traditional societies, but their parents are generally less interested in this sort of crosscultural learning.

Interpersonal Variability in Mediation In order to assess the type of mental diet received by young children in their daily interactions with the adults around them, it is necessary to assess the characteristics of a child’s day, the people he or she interacts with, and the kinds of toys or objects used in those interactions. Different people may provide different profiles of mediation. It is also possible that the same adult may provide a different type of mediation to one child as compared to another. Thus, it is of interest to assess a child’s mental diet by summing up all the experiences he or she has with adults. Some of the causes for variability in a child’s mental diet have been found to be related to the adult’s perception of the child and of his or her own educational objectives in relation to that child. In addition, different toys, objects, games or activities typically invite various profiles of mediation. For example, reading a book frequently includes higher frequencies of affecting and expanding, whereas playing “rough and tumble” may include more regulation of behavior.

Children’s interactions with other children may also contribute to a child’s mental diet. For example, 5-year-olds were found to mediate to their 3-year-old siblings using

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focusing, affecting, regulation of behavior, and encouragement. However, their mediation typically lacked expansion and encouragement with explanation (Klein, Feldman et al. 2003). Both of these types of mediational behaviors were found as determinants of children’s future learning. Thus, children who spend most of their time interacting with their siblings or other children may lack these important components of their mental diet.

Current research on the application of developmental mediation focuses on matching specific developmental profiles of infants and young children with the profile of mediation that may be best suited to their needs within the context of their family, community, and culture. In a sense, this is an attempt to plan a mental diet appropriate for the changing needs of infants and young children as they develop.

Summary Infants and young children require adult mediation in order to develop the potential to benefit from new experiences. Various patterns of mediation have been found to be related to characteristic behaviors of infants and young children, reflecting the needs to seek clarity in perception, to search for meaning, to seek information beyond what could be perceived directly through the senses, to link between experiences (spontaneous associations), to experience success, especially in social contexts, and others. It is possible to enhance parents’ or teachers’ mediation through intervention, and consequently to affect the mental development of infants and young children. Specific patterns of mediation were identified cross-culturally and in populations of children with special needs. Learning to “read” these patterns (i.e., learning to use the literacy of interaction) may be helpful in planning suitable mental diets through quality educational programs for young children. “Literacy of interaction” refers to sensitization and consciousness-raising regarding key issues in the adult-child (parent-child, caregiver-child, or teacher-child) interaction. In practice this means trying to raise the adult’s awareness regarding his or her own basic philosophy of childrearing, perceptions of the child; of himself or herself as parent or teacher; of the child’s emotional and cognitive needs; and how all these affect the interaction with the child, especially the mediational interactions, namely the attempts to teach the child. The representation of all these components is referred to as the literacy of interaction representing a child’s mental diet.

Most of the decisions of educational policymakers focus on what is done, rather than on how it is done in the teaching-learning interaction. The developmental appropriateness of educational programs for young children is frequently assessed in terms of outcome measures, primarily including measures of achievement, skills and abilities, and rarely involving a focus on how the process of adult-child interactions potentially affect children’s readiness to learn in the future. This paper suggests that answers to the “How” question may explain much of the variability in children’s readiness to learn, through the effects on children’s need systems, motivation, and self-regulation.

The following is an example of an educational approach exemplifying the use of the basic ideas discussed here.

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The Developmental Mediation Approach The MISC is presented here as a model educational approach, which is based on attempts to analyze or read interactions and use them to enhance early education. The acronym MISC stands for both the process and the objective of this approach. The objective of this approach is More involved, interested, insightful (Intelligent) and Sensitive Children (MISC). Intelligence is referred to as the ability and need to learn readily and easily from one’s experiences, also referred to as flexibility of mind. Sensitivity is defined as the ability to understand one’s self and others’ emotions expressed in adult-child interactions and to respond in a way that promotes the quality of the interaction, including positive affect, synchrony between partners, and optimal duration of the interaction. The process through which this objective is achieved is represented by the same acronym MISC—a Mediational Intervention for Sensitizing Caregivers, including parents and teachers.

The MISC approach is based integrating three major frameworks, two of which, the eco-cultural and the developmental approach, are frequently mentioned in current early intervention approaches. The integration of the first two components with the third, the mediational one, is unique and is proposed as a necessary combination for effective early childhood education in general and for early intervention in particular.

The three components of the MISC are as follows: 1. The eco-cultural approach relates to the necessity to raise the awareness of the adults interacting with young children of their own deep objectives of childrearing, their long-term educational goals, their perception of the ideal child, ideal parent, etc., vis-à-vis their actions toward achieving immediate goals, such as teaching specific content matter. This is particularly important when teachers and children come from different cultural backgrounds.

2. Growth and development are viewed as a dynamic process in which both child and adult are partners affecting each other and the environment. Based on this framework, programs for infants and young children must take into consideration young children’s basic emotional needs for stable affectionate relations with one adult as the basis for any future learning.

3. A developmental mediation approach combines basic elements from the developmental approach and the mediational approach. Based on the theory of cognitive modifiability (Feurstein, 1979, 1980) and Vygotzky (1978), several basic characteristics of adults’ behavior that are necessary to create experiences of mediated learning for young children were empirically defined and identified. Empirical evidence (Klein & Alony, 1993; Klein, 1996; Tzuriel, 1999) suggests that these experiences may consequently promote the chances for cognitive and emotional development of young children by affecting their needs systems. These mediational processes (see Table 1) include the following behaviors by adult caregivers: • Focusing—attempts to get a child’s attention.

• Affecting—attempts to raise the child’s awareness of the affect or significance associated with objects, people, and actions in the environment, i.e., expressing the meaning and significance of things, people, or processes.

• Encouraging—mediates feelings of competence to the child.

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• Expanding—transcends verbally or nonverbally the concrete immediate context of the interaction (also known in the educational literature as “distancing”).

• Regulating behavior—attempts to mediate planning behaviors, including considerations that precede actions, as well as actually demonstrating to a child how to do things.

Typical Features of the Developmental Mediation Approach The objective of the developmental mediation approach is to promote a sound, facilitative adult-child relationship with a special focus on adults’ teaching behavior— enhancing and improving the literacy of interaction representing a child’s mental diet.

One approach using the MISC is based on videotaping and providing video feedback of adult-child interactions. Adults view themselves interacting with their children and are helped to analyze their interactions in relation to their own views and perceptions of their child, themselves, their educational objectives, and the child’s actual sensory profile and developmental status (Klein, 1996). A profile of mediation represents the frequencies and sequences of mediational behaviors in the observed interaction. Initially, the most frequent or the best mediational behaviors are pointed out and discussed, followed by the others. In addition, the synchrony of the interaction, and the adult’s sensitivity and responsiveness to the child’s initiatives are highlighted. This process helps parents, caregivers, and teachers sharpen their awareness regarding what they bring to the interaction vis-à-vis what their child contributes to it, and how those contributions interplay and modify the interaction. Following this process, parents, teachers, and caregivers frequently become more motivated and interested in the interactions with their children as they gain competence in their own behavior as caregivers. The latter is most important for sustaining long-term effects of the mediational approach.

Poor Mediation and Difficulties in Learning?

In line with Feuerstein’s theory of cognitive modifiability (Feuerstein, 1980), much of the variability in children’s capacity to benefit from new experiences (namely, flexibility of mind) is linked to the type of mediational interactions they have had with the adults who cared for them. These differences are apparent in the way these children approach new experiences, in the way they integrate them with other experiences, and in the way they express themselves. Many children lack the enthusiasm or need to explore their environment, to search for meaning, to think of connections between things, to seek newness. They are satisfied with a blurred, undifferentiated picture of their environment. Their eyes and ears (although functioning normally) are not tuned to detect fine differences between various things they perceive. They do not have the need to form a link between cause and effect, between past, present, and future experiences, and are less inclined to seek an adult’s assistance in order to solve problems or obtain more interesting information or objects. It is clear that children with undifferentiated, blurred perceptions, lack of enthusiasm, and absence of the

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drive to explore and opportunities to do so, experience things in an isolated, fragmented manner, which limits their capacity to benefit from future experiences. Children who have these limitations may be considered as lacking flexibility of mind or as having difficulties in benefiting from new experiences. Most of these behaviors have been identified by Feuerstein (1979, 1980) as reflecting deficient cognitive processes related to poor mediational experiences.

Differences between the MISC and Other Early Interventions The MISC was designed to overcome some of the difficulties that were inherent in ongoing early intervention projects in various countries in Africa, Asia, Europe, and in the United States (Klein, 1996). Although different programs were implemented in different countries, the following problems were reported repeatedly in many of them: 1. Whereas many early education programs aim to promote the development of cognitive skills or abilities, the prime objective of the mediational approach is to affect the children’s need system, to create new, more differentiated needs that could promote their future appetite and capacity for learning (see Table 1).

It is a misleading notion to assume that merely bringing people into contact with new experiences helps them to develop a differentiated taste or need for them. We can take children to the theater, to the library, or to a concert, but does it affect their need to seek cultural experiences of this kind in the future?

An infant or young child experiencing pleasant feelings in the presence of an adult wants to be with him or her even after basic needs have been fulfilled.

Hearing the adult, pointing to things, explaining them, associating, comparing, contrasting, becomes desirable as well, and thus develops the need for more such “educational” interactions. Fredrickson (2001) has suggested that positive feelings have an effect on cognitive dispositions and processes, and that as the links between them persist, these processes become a permanent part of one’s repertoire of behavior. It is through pleasurable human interaction and mediation that an infant or young child learns to need and seek clear information, beyond what is directly perceived by his or her senses and all the other needs listed earlier, which are associated with better reception, organization, and application of learned experiences.

2. Parents from various ethnic backgrounds, especially poor parents, were led by education professionals to believe that there is one ideal model, a “better way” of raising and educating young children, better than the traditional way they brought with them from their old homes. The transition from the old to the new frequently led to a feeling of alienation. Parents felt that what they had to transmit to their children would not sufficiently promote later development.

They felt that they could only contribute the little they had been taught by their child’s kindergarten teacher, nurse, or visiting specialist in the ongoing programs. This misperception limited all forms of cultural transmission and minimized the chance to capitalize on the best learning opportunities for the chil-

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dren. The application of structured, content-oriented programs using specific materials tended to create a dependency on these materials (e.g., toys, booklets, etc.) and limited transfer to other situations or other children within the family, daycare, or educational setting.

There are differences between stimulating and mediating children. Stimulation is a concept that most people, including professionals, parents, and caregivers seem to view as a positive educational process. Yet, as is clarified here, it may be a relatively useless or even a developmentally harmful process, far from the original intent of those who are encouraging its use. In a modern competitive society, parents are pressured to provide their children with everything possible to insure that they are not left developmentally behind other children. Many parents or caregivers are misled to believe that stimulating young children, (i.e., merely catching their attention or focusing it on fragmented stimuli, without using this attention to convey meaning or relate experiences), promotes their development. Such experiences may be perceived by children as a bombardment of their senses and as inappropriate for them and their specific needs at a particular moment. Such experiences may minimize the child’s chances of developing the appetite and dispositions for learning.

As the MISC is focused on the quality of the adult-child interaction, and not on the content of the material used in this interaction, it is not a program in the traditional sense. It is more a method for sensitizing mothers (and other caregivers) to the positive aspects of their existing interaction and childrearing practices. As such, it can never be in conflict with the mothers’ own traditional way of childrearing and stands a better chance of sustaining long-term effects on parental behaviors.

Note: The research presented here was supported in part by WHO, UNICEF, UNESCO, NORAD, and Red Barnna, supporting the implementation of the MISC in Ethiopia, Sri Lanka, Indonesia, Norway, Sweden, the Unites States, and Israel. Preparation of this manuscript was supported by the Machado Chair for Research on Cognitive Modifiability, Bar-Ilan University, Israel.

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Bryant, D. M. & Ramey, C. T. (1987). An analysis of the effectiveness of early intervention programs for environmentally at-risk children. In M. J. Guralnick & F. C. Bennett (Eds.), The effectiveness of early intervention for at-risk and handicapped children (pp. 33–78). New York: Prentice-Hall.

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Feuerstein, R. (1980). Instrumental enrichment: Redevelopment of cognitive functions of retarded performers. New York: University Park Press.

Fredrickson, B. L. (2001). The role of positive emotions in positive psychology—The broaden and build theory of positive emotions. American Psychologist, 56(3), 218–226.

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Klein, P. S. (1992). Mediating the cognitive, social and aesthetic development of precocious young children. In P. S. Klein & A. J. Tannenbaum (Eds.), To be young and gifted. (pp.245–277).

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Klein, P. S. (2001b). A mediational approach to early intervention in Israel: Mediational intervention for sensitizing caregiver (MISC) of typically developing and hard to reach children. In S. Odam, M. Hanson, & J. Blackman (Eds.), International perspectives on early intervention (pp. 69–90). Baltimore, MD: Paul H. Brookes Publishing Company.

Klein, P. S., & Alony, S. (1993). Immediate and sustained effects of maternal mediation behaviors in infancy. Journal of Early Intervention, 71(2), 177–193.

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Toward a Behavior of Reciprocity Morton Ann Gernsbacher Department of Psychology University of Wisconsin-Madison MAGernsb@wisc.edu

Abstract: It is frequently believed that autism is characterized by a lack of social or emotional reciprocity. In this article, I question that assumption by demonstrating how many professionals—researchers and clinicians—and likewise many parents, have neglected the true meaning of reciprocity. Reciprocity is “a relation of mutual dependence or action or influence,” or “a mode of exchange in which transactions take place between individuals who are symmetrically placed.” Assumptions by clinicians and researchers suggest that they have forgotten that reciprocity needs to be mutual and symmetrical—that reciprocity is a two-way street. Research is reviewed to illustrate that when professionals, peers, and parents are taught to act reciprocally, autistic children become more responsive. In one randomized clinical trial of “reciprocity training” to parents, their autistic children’s language developed rapidly and their social engagement increased markedly. Other demonstrations of how parents and professionals can increase their behavior of reciprocity are provided.

Toward a Behavior of Reciprocity Worldnet Dictionary (thefreedictionary.com) defines reciprocity as “a relation of mutual dependence or action or influence.” Hyperdictionary (hyperdictionary.com) defines it as “a mode of exchange in which transactions take place between individuals who are symmetrically placed, that is, they are exchanging as equals, neither being in a dominant position.” The connotation of reciprocal as actions given or done in return permeates many of our political and societal coinages; we use expressions such as reciprocal aid, reciprocal trade, and reciprocal privileges (e.g., reciprocal membership privileges at health clubs or reciprocal borrowing privileges at lending libraries).

Indeed, a primary association to the word reciprocity for the author is the agreement between the University of Minnesota and the University of Wisconsin that allows Wisconsin state residents to attend the University of Minnesota, paying only in-state tuition, rather than the more expensive out-of-state tuition, and similarly Minnesota state residents can attend the University of Wisconsin, paying only in-state tuition. This agreement between the Universities of Wisconsin and Minnesota epitomizes reciprocity: It is mutual, it is symmetrical, and the exchange occurs with neither party being in a dominant position.

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Now, consider reciprocity with regard to autism. The thesis of this article is that many professionals—researchers and clinicians—and likewise many parents, have neglected the reciprocal nature of reciprocity. They have forgotten that reciprocity needs to be mutual and symmetrical—that reciprocity is a two-way street. Thus, the purpose of this article is to move us toward a behavior of reciprocity, genuine reciprocity.

Reciprocity and Autism It has become a truism that autism is characterized by a lack of social or emotional reciprocity. So accepted is this assumption that, for example, in a recent research article examining a hypothesized autism susceptibility gene, the opening line simply claimed that “impaired reciprocal social interaction is a core feature of autism” (Wassink et al., 2004, p. 968). No scientific citations were needed, no supporting data were required; the statement was assumed to be fact. Interestingly, however, none of the initial descriptions of autism mentioned reciprocity and its assumed lack. For example, the seminal diagnostic criteria for autism published in 1980 in the DSM-III did not mention one word about reciprocity (APA, 1980). The more recent 1994 published DSM-IV criteria for autism do mention reciprocity (APA, 1994); more specifically, “a lack of social or emotional reciprocity” is listed as one of the 16 possible characteristics of autism. However, no examples are provided of how a lack of social or emotional reciprocity would be manifested in behavior.

One would think that the very well known Social Reciprocity Scale (Constantino, 2002), which has been used in several studies of autism (Constantino & Todd, 2000; Constantino & Todd, 2003; Constantino, Gruber, Davis, Hayes, Passanante, & Przybeck, 2004; Towbin, Pradella, Gorrindo, Pine, & Leibenleft, 2005), would provide examples. And indeed, a few of the 65 items on the Social Reciprocity Scale do approximate a rough vernacular of what might constitute socially or emotionally reciprocal cognitions, for example, “is unaware of what others are feeling or thinking,” and perhaps “doesn’t recognize when others are taking advantage of him/her,” and “would rather be alone.”1 However, even among the first several items on the Social Reciprocity Scale there are items that do not fit a true meaning of reciprocity (or its lack), for example, “expressions on his/her face don’t match what he/she is saying,” and “doesn’t seem self-confident when talking.” Other items seem completely unrelated to social reciprocity, for example, “is not well coordinated in physical activities,” or “doesn’t have good personal hygiene.”

Other items on the Social Reciprocity Scale illustrate the thesis of this article: Some professionals have forgotten the true meaning of reciprocity. Consider the item, “is regarded by other children as odd or weird.” This item appears to measure other 1. I have relabeled these as “cognitions” because I find it baffling that they would be considered “behaviors,” given that they are thoughts (e.g., awareness of what other people are thinking or feeling) or perhaps predilections (a preference to be alone). However, such items demonstrate a type of arrogance if the observer— the parent or teacher, who completed the questionnaire about the target child—truly believes that he is aware of what the other person (the target child) is thinking.

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children’s lack of social or emotional reciprocity. Regarding another child as odd or weird implicates the regarder—not the target child—as lacking in empathy or understanding. As a final example, consider the item on the Social Reciprocity Scale that asks whether the child “gets teased a lot.” How in the world the occurrence of a child being teased could be construed as a metric that he or she lacks social or emotional reciprocity is baffling. However, as the researchers who constructed this scale have demonstrated, this item is highly correlated with autism: Autistic children do get teased a lot, so much so that being teased and bullied has been elevated to a phenotypic criterion (Kunihira, Senju, Dairoku, Wakabayashi, & Hasegawa, 2006). Why do autistic children get teased so much? I submit this is because many non-autistic children, in addition to professionals and sometimes parents, forget that reciprocity is a two-way street.

Consider the following anecdote. On a lark one day a few years ago, I typed into the search bar of eBay the word “autism.” I was surprised to see over 500 items listed for auction that claimed to have some relation to autism. One item in particular caught my attention. The auction was titled, “Autism: See the World through My Eyes,” and the auction item was a button, such as one wears on a lapel. The button contained a picture of a young girl named Sarah, looking out a window, and the message: “I wish you could see the world through my eyes!” The auction description explained that Sarah’s father created this button because the message captured how Sarah responded to a homework assignment that asked what she would wish for if she had a magic wand. Sarah wished that others could see the world through her eyes.

On the exact day that I bumped into that eBay auction, an article appeared in the New York Times entitled, “Experiment Offers Look through Eyes of Autism” (O’Neil, 2002). The article stated that “using a high-tech eye-tracking device developed for the military, researchers at Yale ran experiments that came closer than anything yet to offering a look at the world as seen through the eyes of people with autism.” Could this be Sarah’s most fervent wish coming true? No, sadly not. As the New York Times article stated, “In the experiment, described in the current issue of The American Journal of Psychiatry, the researchers compared the eye movements of a highly intelligent autistic adult and a control subject of the same age, sex, and I.Q as they watched the relentless emotional conflicts of “Who’s Afraid of Virginia Woolf?”

From this eye-tracking experiment, the researchers concluded that “the two subjects were seeing the movie in starkly different ways. When Mr. Burton and Ms. Taylor, playing an alcoholic professor and his shrewish wife, confronted each other face to face, the gaze of the non-autistic adult swung intently between their eyes, while the autistic subject looked back and forth, as well—but focused on the actors’ mouths.”

If the researchers could really see through the eyes of the autistic participant, they might have seen that it was more comfortable for him to focus on the mouths rather than the eyes (Gernsbacher & Frymiare, 2005), or that the mouths were even more informative—particularly because the individual with autism had a history of language impairment (Campbell & Dodd, 1980; Kuhl & Meltzoff, 1982; McGurk & MacDonald, 1976). Indeed, we know that other individuals with a history of language impairment who are not autistic focus on mouths for further information processing during discourse. It is a very adaptive strategy. But this very adaptive strategy was billed in the New York Times as “a profound social disability.”

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In her book, How to Be a Para-Pro: A Comprehensive Teaching Manual for Paraprofessionals, non-autistic Twachtman-Cullen (2000) takes the perspective of an autistic child who requests the following of those around him or her: “Even though there are many things about me that are unique, in the ways that really matter, I am just like other children. I learn best from people I trust, and learn to trust when I sense that people like me. Please try to see the world through my eyes. Please know that even though it may not seem so, I really am trying to adapt to a world that my neurological challenges [sometimes] prevent me from understanding.”

Such neurological sensitivities were identified in a research article published in the Journal of Applied Behavioral Analysis (Tang, Kennedy, Koppekin, & Caruso, 2002).

In this article, titled “Functional Analysis of Stereotypical Ear Covering in a Child with Autism,” four researchers conducted 43 half-hour observations across four days and submitted those extensive and intricate observations to numerous detailed behavioral analyses to understand the origin of “stereotypical ear covering that was reported by the child’s teachers to serve no identifiable function” (p. 95). The researchers concluded that “the results of a descriptive analysis revealed a correlation between ear covering and another child’s screaming. An analogue functional analysis showed that ear covering was emitted only when the screaming was present” (p. 95). It is difficult to imagine that a magic wand, high-tech expensive military eye-tracking equipment, or a detailed applied behavioral analysis was needed to appreciate this child’s very adaptive response to an assault against his auditory sensitivities. What was needed was greater social and emotional reciprocity—social and emotional reciprocity by the teachers and the researchers toward the autistic child.

Toward a Behavior of Reciprocity How can parents, clinicians, teachers, and researchers move toward a greater behavior of reciprocity? In the words of the Count of Monte Cristo (Dumas, 1846/2000, p. 592): “A secret voice seems to whisper to me that there must be something more than chance in this unexpected reciprocity of friendship.” The behavior of social and emotional reciprocity needs to be acquired with something more than chance; reciprocity needs to be developed more purposefully by non-autistics and applied more generously toward autistics. Twenty years of applied behavioral analysis (ABA) support this plea, although this body of ABA research has never been interpreted from a truly reciprocal perspective.

For example, in 1985 researchers taught three typically developing kindergartners some basic pro-social behaviors such as “offering to share with peers and to help peers . . . [i]nviting peers to play and requesting permission to play with peers” (Kohler & Fowler, 1985, p. 191). Two of the three typically developing children maintained and increased these pro-social behaviors; a third child did not. What happened with the third child? Very simply, the “third child’s play invitations were not reciprocated by [her] peers; her invitations subsequently decreased in rate” (p. 187).

In 1986 researchers taught four typically developing preschoolers to either initiate interaction with three autistic preschoolers or to respond to the interaction that the three autistic preschoolers initiated, in other words, to be reciprocal (Odom & Strain,

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1986). Which intervention had the more lasting influence on the autistic preschoolers’ social interaction? When the typically developing preschoolers were taught to respond to the interaction that the autistic preschoolers initiated, the autistic preschoolers responded more frequently. In other words, when the typically developing preschoolers behaved reciprocally, the autistic preschoolers responded more positively.

In 1988 researchers taught three autistic kindergartners to initiate pro-social physical interaction—giving high fives, patting a friend on the back—by incorporating the actions into a song, such as “if you’re happy and you know it, give your neighbor a high five” (McEvoy, Nordquist, Twardosz, Heckaman, Wehby, & Denny, 1988). The three autistic kindergartners then interacted with six typically developing kindergartners, only half of whom had also gone through the pro-social physical interaction training themselves. The typically developing kindergartners were considerably more likely to reciprocate the autistic kindergartners’ interactions if they too had gone through the training.

In 1992 researchers taught three typically developing preschoolers, called peer tutors, to prompt for the verbal labels of preferred toys from three autistic children, whom the researchers called target children (McGee, Almeida, Sulzer-Azaroff, & Feldman, 1992). The peer tutors were told to “(a) wait for the target child to initiate a request for (i.e., reach for) a toy, (b) ask the target child for the label of the toy (e.g., “Say duck”), (c) give the toy to the target child when he labels it, and (d) praise the correct answer (‘That was great! You said duck’). None of the target autistic children maintained their initiation with the typically developing peer tutors after the training sessions were completed. Why not? I submit it was because the interactions were not reciprocal. Recall that reciprocity is defined by “a relation of mutual dependence or action or influence” and “a mode of exchange in which transactions take place between individuals who are symmetrically placed, that is, they are exchanging as equals, neither being in a dominant position.” Peer tutors prompting autistic target children for verbal labels is neither mutual nor symmetrical.

Given these ABA data, the following scenario related by a mother in the section called “From the Front Line” of the near-classic ABA-for-autism manual, Behavioral Intervention for Young Children with Autism: A Manual for Parents and Professionals (Maurice, Green, & Luce, 1996) makes infinite sense. The mother began by describing how she established a behavioral therapy program for her daughter.

The first order of business was to establish attending behaviors. This was accomplished by the therapist holding a food reinforcer at her eye level while stating “Rebecca.” Rebecca wanted that reinforcer (a raisin or a Cheerio) so she would look momentarily at the therapist who would immediately give her the Cheerio and praise her verbally (Good looking, Rebecca!). Once Rebecca began to attend, she was taught to follow simple gross motor imitations and simple commands (stand up, clap hands, wave bye-bye). (p. 366) By the time we hit the one year anniversary of our program 3 months ago, Rebecca had developed a great deal of skills and language. . . . A sampling of her current skills includes her ability to expressively identify all the letters of the alphabet presented in random sequence. She knows her shapes and colors, she can count up to 12 items, and she has an extensive vocabulary (several hun-

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dred words). Additionally, she has become proficient in categorizing items among nine different groupings. I was recently quizzing her in the car and asked “What’s a zebra?” “It’s a animal.” “What’s a triangle?” “It’s a shape.”

“What’s a couch?” “It’s furniture.” “Who’s William?” “It’s a person.” “What is a w?” “It’s a letter.” “What’s a helicopter?” “It’s something you ride in.”

“What’s a bathing suit?” “It’s clothes.” “What’s cake?” “It’s food.” (p. 369) As the mother wrote, “I present these examples to illustrate that many of the things that Rebecca knows are quite advanced for a child her age. I am convinced that Rebecca is a highly intelligent child. Her teachers tell me this constantly. In a way, that makes her deficits all the more maddening” (p. 369). What are these deficits that are so maddening to her mother? As the mother laments, If, for example, I enter the kitchen after my morning walk and [my two daughters] are sitting at the kitchen table eating breakfast, Rebecca might glance up at me for a second and then look away. I have to walk up to her, get in her face, and force the interaction (“Hi Rebecca.” “Hi Mama.” “How are you?” “Okay.”

“I love you.” “I love you, too.”). I have always found the contrast between my two children to be the most obvious and the most painful at mealtimes. Holly is such a talkative and observant child, and Rebecca will be sitting there like a sphinx, unable to participate in the give and take.

We find ourselves continually trying to draw her into our conversations.

“Rebecca, what are you doing?” “I’m eating.” “What are you eating?” “Pasta.”

“Good. What’s pasta?” “It’s a food.” “Good! Is it delicious?” “Yes.” “Say, ‘It’s delicious.’ ” “It’s delicious.” (p. 368) Furthermore, as the mother describes, “One big problem that we have recently been tackling concerns Rebecca’s compliance during her [behavioral therapy] sessions. At times Rebecca becomes very silly … We had decided to completely ignore Rebecca’s behavior during these incidents and to revert to a simple command presented over and over until Rebecca would get bored and comply. Unfortunately, this tactic did not succeed in extinguishing the noncompliance (it was going on for more than a month), so we are now resorting to putting Rebecca in time out, which we have determined is an aversive for her” (pp. 369–370). Such an approach might be helpful for teaching a child to see the world through your eyes, which is the promise of Bridges for Children with Autism (bridgesABAtapes.com), an internet company that sells ABA therapy training tapes, but recall that Sarah, the girl on the eBay button— and perhaps Rebecca, also—wished that others could see the world through her eyes.

How can we do that?

Follow the Child’s Lead According to one very prominent intervention style: “Follow your child’s lead and play at whatever captures her interest” (Greenspan & Weider, 1998, p. 123–124). A wealth of empirical evidence supports the benefit of following this crucial mantra in

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both typical and atypical development. For example, Herman (2002) wrote the following in her essay titled, “What Parents Do to Encourage Communication and Language” regarding typical development: The process of getting to know their new child involves parents noticing what interests them and how they react. Parents watch to see what their baby looks at and will often talk about whatever it is that appears to interest their child. In this way, the parent follows the baby’s lead. For example, if the baby gazes towards the light, the parent may comment “are you looking at the light?” In this way, the parent imposes meaning on the baby’s actions, even though the baby’s actions at this early stage are without any specific purpose. Eventually, this teaches the baby that actions lead to responses. In addition, the fact that communication is closely tied into whatever activity the baby is engaged in helps the baby begin to make sense of the stream of words they hear.

Herman wrote that toward the end of the first year of life, An important behaviour to emerge at this time is the development of joint attention. This is a natural development from the parent following the baby’s lead and talking about the child’s focus of attention, as described above. Babies begin to be more aware of when they and their parents are focusing on the same object or activity. By the age of 9–12 months, they are able to follow their parent’s line of vision and make use of pointing gestures. This helps them to begin to match the language they hear with the focus of attention. Indeed, where parents follow the infant’s focus of attention when providing language, infants’ vocabulary acquisition has been shown to proceed at a faster pace.

But what about the child who is delayed in developing the ability to follow his parent’s line of vision? What about the child who is delayed in developing the ability to make use of pointing gestures, that is, to follow a parent’s manual point or to make his own pointing gesture? Or even to make his own reaching gesture? Experience suggests that this is when parents—and professionals—need to enact even more reciprocity, need to share even more of the child’s world, need to follow even more of the child’s lead, and need to become something of a detective to discern the ways that the child is expressing joint attention and social and emotional reciprocity.

Consider the detective work effectively accomplished by Robert Hughes, a Chicago writer, who chronicled his life with his autistic son Walker in a critically acclaimed book, Running with Walker. In an essay titled “Autism and Empathy,” published in Chicago Parent magazine, Hughes (2004) wrote the following about 17 yearold Walker: He can’t converse, play a game, sit still, tie his shoes. He does every mainline autistic behavior in the book: waves his hands and stares at reflected light, shouts certain words and phrases over and over, rewinds his audiotapes until they break. . . . But there is one quality he has in such abundance that it seems almost to define him: empathy. Bouncing on his therapy ball, his throne in our dining room, he knows his family’s hidden feelings no matter how well we mask them.

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Unfortunately, when he was much younger, his mother and I did not always catch on to this depth of feeling in him. Since he never nodded “yes” and “no,” much less enunciated those words in any consistent way, even some of his essential character traits tended to stay under our radar. They were only revealed in dramatic blips that slowly enabled us to see him in a new way.

One such moment came when he was four years old. I had just come home from three days in the hospital undergoing tests for chest pain. The tests showed that I had experienced one of those Middle-aged Dad Hypochondria Alerts: My heart was fine; I was nuts. When I walked in our front door (as far as Walker knew, back from the dead) he took my hand and pulled me over to the couch. He got out a copy of Pinocchio, one of those Disney books a child reads along with an audiotape, and turned the pages until he got to the place where he wanted me to read to him.

It was the passage about Pinocchio saving his father from the whale. I stopped in the middle of a sentence and stared at him, amazed. It was my odd, silent four-year-old’s articulate way of telling his father of his love and concern. Since then, [my wife] and I have read his strange behavior in the light of the boy revealed that day: The one who feels far more deeply than he lets on, who signals his thoughts and feelings in unconventional, but still very telling ways.

It is those “unconventional, but still very telling ways” that parents, researchers, clinicians, and members of society must seek to identify. As autistic advocate, Jim Sinclair, has written in an essay titled “Don’t Mourn for Us” (Sinclair, 1993): The ways we relate are different. Push for the things your expectations tell you are normal, and you’ll find frustration, disappointment, resentment, maybe even rage and hatred. Approach respectfully, without preconceptions, and with openness to learning new things, and you’ll find a world you could never have imagined. Yes, that takes more work than relating to a non-autistic person. But it can be done—unless non-autistic people are far more limited than we [autistic people] are in their capacity to relate. We spend our entire lives doing it.

The Power of Imitation In what ways can non-autistics show the behavior of reciprocity? We have known for centuries that imitation is the sincerest form of flattery, and we have known for decades that imitation improves social responsiveness in all children, including autistic children (Dawson & Adams, 1984). I am not referring to autistics imitating nonautistics, but rather non-autistics imitating autistics. When a stranger—such as an experimenter in a psychology laboratory—imitates an autistic child’s object-oriented behavior, that is, the experimenter manipulates a duplicate object in the same way that the child does, the child makes dramatically longer and more frequent eye contact with the experimenter (Tiegerman & Primavera, 1984). When mothers imitate their autistic children’s manipulation of toys, autistic children gaze longer and more frequently

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at their mothers, the children engage in more exploratory and creative behavior with the toys, and the children show considerably more positive affect (Dawson & Galpert, 1990). These effects are independent of the child’s developmental level.

In another laboratory experiment (Field, Field, Sanders, & Nadel, 2001), autistic children displayed more socially reciprocal behaviors after repeated sessions in which the experimenter imitated their behavior, in contrast to a control group of autistic children with whom the experimenter played responsively but not imitatively. During a second session in this experiment, autistic children who were imitated by the experimenter increased in looking, vocalizing, smiling and playing with the experimenter; during a third session, autistic children who were imitated by the experimenter increased in being close to the experimenter, sitting next to the experimenter, and touching the experimenter.

Can these reciprocal behaviors be packaged into a treatment program—a program that trains parents and others to behave more reciprocally with their autistic children?

The answer is yes, and empirical evidence demonstrates the effectiveness of such programs. One study (Mahoney & Perales, 2003) used relationship focused intervention to enhance the social emotional functioning of autistic children by implementing responsive teaching with the children’s parents. Some of the behaviors that the parents were taught included the following: join the child’s perseverative play; read the child’s behavior as an indicator of interest; follow the child’s lead; respond to the child’s behavioral state; match the child’s interactive pace; and expect the child to react according to his or her temperament or behavioral style.

The participants were the mothers of 20 young children diagnosed as being on the autism spectrum. The mothers received weekly one-hour intervention sessions for 8 to 14 months. Before and after the treatment, both the parents and the children were assessed with a set of measures, but it is important to note that the treatment—the responsive teaching—was delivered only to the parents. Post-treatment, the mothers were observed to have increased in their responsiveness and their affect, which was the predicted outcome, and to have decreased in their achievement orientation and their directiveness, which was also the predicted outcome (although the decreases in achievement orientation and directiveness were not statistically significant). Posttreatment, the children’s interactive behavior was observed to have increased an average of 50% in affect, persistence, interest, cooperation, initiation, and joint attention.

All improvements were statistically significant, and the largest gain was in joint attention, which improved 84%.

Post-treatment, the children’s socioemotional behavior was rated by their mothers as being significantly less detached, more socially reactive, and better regulated, according to the Temperament and Atypical Behavior Scale (Bagnato, Neisworth, Salvia, & Hunt, 1999). In addition, as observed by the researchers using the Infant Toddler Socioemotional Assessment, the children increased in their self-regulation and social competence (Briggs-Gowan, Carter, Irwin, Wachtel, & Cicchetti, 2004; Carter, Briggs-Gowan, Jones, & Little, 2003).

The gold standard in treatment outcome research is the randomized clinical trial (i.e., an experiment in which there is both a treatment group and a control group, with each participant being randomly assigned to one of the two groups). After decades of

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claims such as “thirty years of research demonstrating the efficacy of applied behavioral methods in reducing inappropriate behavior and in increasing communication, learning, and appropriate social behavior” in autism (U.S. Surgeon General’s Office), there exists only one randomized clinical trial assessing the efficacy of ABA intervention for autism (Smith, Groen, & Wynn, 2000; see Gernsbacher, 2003, for a review).

Unfortunately, the one randomized clinical trial of ABA intervention for autism produced no significant improvements in social interaction or communication.2 Consider in contrast a randomized clinical trial evaluating the effectiveness of a social communication intervention. Like the intervention delivered in Mahoney and Perales (2003); however, this randomized clinical trial (Aldred, Green, & Adams, 2004) delivered intervention to only the parents of autistic children. The treatment involved “educating parents and training them in adapted communication tailored to their child’s individual competencies . . . promoting highly sensitive adult responses, where actions made by the child are interpreted by the adult as having meaning and being related to the child’s assumed intentions and desires, and replacing [the parents’] controlling and intrusive responses with responses aimed at facilitating the child’s active communication exchanges” (p. 1421–1422). Fourteen parents of autistic children were randomly assigned to the treatment group, and the same number was randomly assigned to the control group. The results of this randomized trial were quite impressive.

Analysis of a 30-minute parent-child free play session by coders who were naïve as to whether parents had been in the treatment or the control group identified several statistically significant changes. First, parents in the treatment group increased 7.3% in their synchronous communication, which comprises comments, statements, or acknowledgements that maintain the child’s interaction; in contrast, parents in the control group decreased 7.6% in their synchronous communication. Second, parents in the treatment group decreased 7.1% in their asynchronous communication, which comprised statements aimed at redirecting, controlling, or making demands on the child to respond; in contrast, parents in the control group increased 7.6% in their asynchronous communication. Third, parents in the treatment group increased 6.8% in their reciprocal communicative acts, which comprised verbal and non-verbal behaviors that share communicative intent, while parents in the control group decreased 2.5%.

What effect did these parental changes have on their children? As measured by the Autism Diagnostic Observation Schedule (Lord et al., 1989), children whose parents received treatment were shown to increase significantly in their reciprocal social interaction, their social engagement, their social rapport, their social responses, and their spontaneous initiation of social interaction. The children also demonstrated dramatic improvements in their language development, on the parentally reported MacArthur Communication Development Inventory (Fenson et al., 1993). As shown in Figure 1, children whose parents received treatment improved dramatically in their expressive vocabulary, whereas children whose parents were in the control group did not. As

2. Although the original article reports significant effects on language development, there was an error in data analysis, and an erratum was subsequently published (Smith, Groen, & Wynn, 2001).

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Expressive Vocabulary Vocabulary Size (on MCDI)

250 200 150

Treatment Group

100 Control Group

50 0 Pre-Treatment

Post-Treatment

FIGURE 1. Data from Aldred et al. (2004)

Receptive Vocabulary Vocabulary Size (on MCDI)

250 200 Treatment Group 150 Control Group

100 50 0 Pre-Treatment

Post-Treatment

FIGURE 2. Data from Aldred et al. (2004)

shown in Figure 2, children whose parents were in the treatment group as well as the control group improved in their receptive vocabulary.

Toward an Attitude of Reciprocity Thus, parents can increase their reciprocity behavior. It is my hope that we can also increase society’s reciprocal behavior and that greater reciprocity will permeate more and more of our community’s attitude. Rather than reading a Newsweek “My Turn” column (Lee, 2003), in which a mother bemoans a dreadful ride with her autistic son on a hot, overcrowded, noisy trolley—an activity she had enjoyed when she was a child but clearly her child did not, I’d like to see more media coverage like the Associated Press story of Annie Lewis who camped out for 13 nights with her 12 year-old

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autistic son Gregg so that Gregg, who is fascinated by Krispy Kreme donuts, could be the first person to turn on the Krispy Kreme Hot light sign at the store’s grand opening (Lucy, 2003). “It was a terrific experience, every minute,” Annie Lewis reported.

“I can now do a stand-up comedy act about this whole experience because it was tremendously fun. I would do it again in a split second.”

Rather than reading on a state autism society list serve a mother’s description of her child’s fourth birthday party that went like this: Anna’s birthday started off fine, I had everything done and ready before the first guest arrived at noon. The whole family was here by 1 so we ate, then Anna fell asleep for her afternoon nap. Around 3ish I woke her up to open gifts. She got all worked up, crying and yelling no, carrying on. It was mostly because I woke her up, and she was feeling under the weather thanks to a wonderfully timed cold. Anyhow, my husband Mark sat in her bedroom with her opening gifts while the rest of my family sat there in the living room and dining room. She finally warmed up and enjoyed a couple of the gifts. She then worked her way to the dining room to play with a few new toys. I went and got the cake, put the candles in, we sang, and Anna cried. That was an autistic moment; she NEVER likes it when people sing the Birthday Song like that, even if it’s someone else’s birthday. So I blew out the candles, we ate and soon after everyone went home.

After the cake issue I wondered why I even bother.

I’d like to read about more birthday parties such as the one Paul Collins (2004) related in his recently published book, Not Even Wrong: Adventures in Autism: There’s one couple in Los Angeles with a son obsessed by all things relating to trash and recycling. He has memorized the garbage collection routes, the makes and types of disposal vehicles, and he talks of little else. So they arranged with the local garbage men to have a seventh birthday party for him out at the local landfill. The Los Angeles Times sent a reporter to cover it, blissfully unaware that perhaps this boy was—well, even more different than he seemed. “We don’t know where this interest in trash came from,” they quoted the boy’s mother. “He’s been this way since he was 2.” But both parents say they are fine with him spending his life working with trash, if that’s what makes him happy.

Rather than reading the following opinion from a mother on www. epinions.com (Wendywitch, 2004): I hate that I have to drive her to therapy twice a week and go to IEP meetings.

I wanted tea parties, I got speech therapy. My dreams have become to make her an independent adult, when they started out as having a daughter winning a Nobel Prize or a Pulitzer. I envy parents who can take their children to Disney World or to the movies.

I’d like to hear about more parents like Nancy Alar, who shared on the video, Straight Talk about Autism with Parents and Kids: Childhood Issues (1998), some features of her reciprocal relationship with her teenage son, Matthew Ward:

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Last year he got interested in the gods of Egypt; who knows why. And we don’t know where this came from, this absolute intense interest in hairless dogs. We don’t know why hairless dogs. But, my husband and I are cat people. We now have a hairless dog.

In each of these alternate scenarios, the parents’ behaviors embodied an attitude of reciprocity. As Greenspan and Weider (1998) have warned, “This can be hard. It’s natural to want to take over . . . You need to remind yourself to fight this tendency. Your child will take the most pleasure in activities he chooses himself” (p. 140). Without embodying an attitude of reciprocity and working toward a behavior of reciprocity, it is unlikely that enjoyment will be defined by reciprocity, that is, “experienced or felt by both sides” (American Heritage Dictionary of the English Language, 2000).

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Book Review

Barbara J. King

Primates, Parenting, and Plasticity Parenting for Primates

by Harriet J. Smith, Harvard University Press, 2005 One hot summer day, infant Rosie was trying to get herself from an outdoor area, where she was baking in the full sunshine, to an indoor room with air-conditioning. To do this, she needed to lift up a flap covering a small door, but the flap was too heavy for her to manage. Rosie began to make sounds of distress. Hearing these, Rosie’s Dad, Joe, roused himself from the shade of a peach tree, walked over, and lifted the flap for his daughter. As Rosie went indoors, Joe headed back to his patch of shade.

Why open a review of a book on parenting by highlighting an event of such a routine nature? Joe and Rosie are not humans; they are cotton-top tamarins, small monkeys that come from South America. And when Rosie was born, in captivity four months before the door-flap incident, things hadn’t gone smoothly at all. Rosie’s mother, Chartier, and dad Joe, rejected her and her sibling Ira (tamarins give birth to twins).

When he helped Rosie escape the summer heat, then, Joe acted like a good Dad not because he’s a tamarin and that’s what all tamarins do, or because his genes had programmed him for paternal care. He did so because he had gained experience at good parenting, through Harriet Smith’s self-devised, in-home monkey parenting program. Joe had been hand-reared by Smith in the early 1970s, and thus had grown up without benefit of knowing how tamarins are supposed to raise their young. When he matured enough to mate and father offspring, Joe, together with his mate Chartier, forcefully rejected several sets of twins, monkeys that then had to be handraised also

by Smith.

Parenting for Primates is Smith’s account of how tamarin-raising led her to understand that nonhuman primates learn to be good parents from experience, and can overcome even a rocky start as Joe did. Her account of how she broke the cycle of poor parenting makes absorbing reading. Because Smith is not only a monkey-observer but also a clinical psychologist, her main point is to show that what is true for Joe, Chartier, Rosie, and Ira, can be true for a human family as well.

In addition to thinking across species about parenting, Smith thinks cross-culturally: “Training for parenthood is by apprenticeship for both boys and girls in most preindustrial societies. . . . This process of experience first, parenting second, is reversed in contemporary Western culture: we marry and establish our households first, and

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then get our childcare training on the job. Both mothers and fathers may be in the same boat, if neither have babysat younger siblings or other young children, and both may question their abilities as parents when parenting doesn’t come ‘naturally.’”

Fathers may be particularly disadvantaged by this lack of experience: “Fathers, whose role with infants has long been considered optional, may have little desire at first to become involved. They step aside while their wives become competent mothers by trial and error, with a little advice from family or experts thrown in.” Yet research shows clearly that “[w]hen fathers start taking care of their babies, the babies’ responsiveness increases” (pp. 104–105).

Smith conveys many valuable lessons about the healthy emotional development of human children in a family setting. The crux of her message is this: “Adequate parenting increases our chances of ensuring our own ‘immortality’: when our offspring grow up and reproduce, they pass on our genes to future generations. And yet, the fascinating and complex ways in which primate parenting behavior varies with characteristics of the environment, the social context, and individual experience shows us that parenting behavior is not totally determined by our genes. The flexibility and malleability of primate parenting behavior reveal that we have the ability not only to change our behavior but to make conscious choices about the kinds of parents we wish to be” (p. 11).

This last sentence is one I could have borrowed for my editorial in this inaugural issue of the Journal of Developmental Processes. Smith’s perspective on parenting emerged from an unusual career trajectory. First earning a PhD in comparative primatology, Smith carried out research on cottontop tamarins in the laboratory. For the next 30 years, she kept a colony of these monkeys at her home. (Smith makes a point of saying that “monkeys, like other wild creatures, should not be kept as pets,” so the book is a bit steeped in a do what I say, not what I do framework.) From that base, Smith went on to earn a post-graduate degree in clinical psychology, establishing a practice with, of course, human clients.

This blended background is both a strength and weakness of the book. Many primate-related books focus on chimpanzees, bonobos, or gorillas—the African great apes. This makes good sense given that these apes are humans’ closest living relatives, yet it is refreshing to find a popular counterpart to the work done by researchers such as Jeffrey French, Charles Snowdon, and John Terborgh in the world of tamarin and marmoset academic research. Twin-birthing, family-living mini-monkeys are the perfect exemplars for Smith’s point about primate plasticity.

It’s a strength as well that Smith continues on from a discussion of primate infancy to encompass juvenility and adolescence. It’s not all about the cute phase. Smith freely offers opinions on contentious matters. One example: “That human adolescents are fascinated with sex is a normal, healthy reflection of their primate heritage,” followed by advice for how parents may enable their teenagers to resist temptation (p. 204). Another: “A family with more than one capable adult sharing the responsibility for children, regardless of gender, has a better chance of positive outcome” (p. 298); of course, she means the parents’ gender—not the children’s—in a welcome advocacy for loving families of all kinds.

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Indeed, Smith zeroes in on societal patterns that affect parenting. Citing statistics about dual-career couples and working mothers, she notes that in some cases daycare is not a preference but a necessity, and laments the resources available: “Almost half a million childcare workers (mostly women) are paid less than workers in 99 percent of occupations in the United States today. The low pay offered to young females who work in daycare centers in the United States sends the message that there is almost no job less important than childcare” (p. 131). This matters, of course, because stable and long-term relationships between babies and caregivers matter: “A baby’s best chance for receiving quality care is having a babysitter that knows him, likes him, and wants to please him. . . Quality daycare given by nonkin babysitters does not have to be a contradiction in terms” (p. 132).

Yet I can’t give the book a pure rave. Comparative primatology is a good thing, but can be pushed too far, as when Smith jumps effortlessly from human to New World monkey behavioral patterns: “At the extremes of human fatherhood are titi-like fathers (albeit very few) who are their children’s primary caretakers, and squirrel monkey-like fathers, who play no role in their children’s development after conception” (p. 87). A flat conflation of fathering in a species that is well-adapted and clever with fathering in a species that creates linguistic-cultural norms made me quite uneasy.

Further, readers may sense that the book is dated. Smith reports quite a number of older studies, still valuable, but there’s a somewhat stale flavor to some of the analysis. Primatologists have described far too much variation in social organization within species for terms like “harem” (for gorillas) or “solitary” (orangutans) to be relevant any longer. It is simply incorrect to assert that no nonhuman primate females undergo menopause. And to say that “twenty years ago, most of the thinking about primate behavior was based on studies of rhesus monkeys and other macaques” (p. 95) is strange, given that ape fever had gripped primatology by the mid-1980s and much was flowing to us from long-term studies of chimpanzees, gorillas, and orangutans, not to mention baboons and other non-macaque monkeys. Suffice to know that although Smith thanks various primatologists for reading chunks of the manuscript, an overall keen, and scientific, editing eye was still needed.

More significantly, Smith does not always give the book’s topics the depth of coverage they deserve. Some of most exciting work in parenting is not just about top-down socialization, but about fully contingent and co-created behavior understood through a dynamic-systems perspective. The notion of the family as a system, with a change in one part affecting all, so that mutual transformation is possible, informs works ranging from Murray Bowen’s seminal Family Therapy in Clinical Practice to FivazDepeursinge and Corboz-Warnery’s The Primary Triangle to Stanley Greenspan and Stuart Shanker’s The First Idea—and indeed articles in this first issue of JDP. As the examples I have chosen indicate, Smith veers toward a systems understanding, in which each partner affects the other within a family, and in which the larger society affects the family. I appreciated, for instance, her discussion of the concept of micro-environment (p. 352), the idea that each child’s developmental trajectory is affected by a constellation of factors in his or her environment (including the genetic environment). What I missed was an appreciation that this isn’t just one partner or one

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level of society affecting another in a certain environment, but two partners negotiating and co-creating behavior and meaning, and family and society mutually constructing each other.

Still, Smith’s message is very much needed in a gene-besotted society. KNOW YOUR DNA, blares a headline on Scientific American’s front cover (January 2006).

The subtitle is: Inexpensive gene readers will soon unlock the secrets in your personal double helix. Harriet Smith’s thesis is that the most fascinating secrets of primate parenting lie not in DNA but the complex world of social plasticity and nurturing. When Joe, the tamarin Dad, got up from the shade on a hot day, his exemplified this point to his daughter Rosie; through Smith, we all benefit from his message.

Journal of Developmental Processes Submission Guidelines Description The goal of the Journal of Developmental Processes is to provide a vehicle for research and clinical studies that advance knowledge of the complexity inherent in all developmental processes. The JDP encourages exchange of ideas across fields including, but not limited to, animal behavior, anthropology, biology, education, linguistics, neuroscience, occupational and speech and language therapy, primatology, psychiatry, psychology, public policy, sociology, and social work.

The Journal is interested in both experimental and descriptive studies, including basic research, detailed case reports, ethnographic analysis, and theoretical explorations.

Particularly welcome are innovative conceptual frameworks and methods that capture the complexity of developmental processes as well as assessment procedures and interventions that enable children and families to overcome mental health, developmental, social, and learning challenges.

Submissions Send queries and submissions on clinical aspects and applications to Associate Editor Ira Glovinsky at ira1834@sbcglobal.net; all other queries and submissions, and books for potential review, should go to Editor Barbara J. King at bjking@wm.edu or Department of Anthropology, College of William and Mary, Williamsburg, VA, USA, 23187-8795.

Please submit manuscripts electronically, preferably in Microsoft Word® format.

Length is negotiable with the editor, but generally should not exceed 50 manuscript pages, including references. Submit your contact information, including phone, fax, and postal mailing address. Also enclose a cover letter indicating that the article has not been published, and is not under consideration elsewhere.

Tables, figures, and photographs should be used sparingly. Please include a high gloss black-and-white copy of the image as well as an electronic file in TIFF, EPS, or JPG format. Clearly indicate where the image should appear, as well as a title and explanatory note. Line art should have a resolution of 1200 dots per inch for good print quality.

References References should be listed in alphabetical order. Each listed reference should be cited in the text, and each text citation should be listed in the References. We follow the APA style, e.g., Greenspan, S. I., & Shanker, S. G. (2004). The first idea: How symbols, language, and intelligence evolved from our primate ancestors to modern humans. Cambridge, MA: Da Capo.

Greenspan, S. I., & Shanker, S. G. (2005). Developmental Research. In E. S. Person, A. M. Cooper, & G. O. Gabbard, American psychiatric publishing textbook of psychoanalysis (pp. 335–360). Washington, DC: American Psychiatric Publishing.

Greenspan, S. I., & Wieder, S. (1997). Developmental patterns and outcomes in infant and children with disorders in relating and communicating: A chart review of 200 cases of children with autistic spectrum diagnosis. Journal of Developmental and Learning Disorders, 1, 87–141.

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