Journal2001 v5 1

The Core Deficit in Autism and Disorders of Relating and Communicating The Journal Of Developmental and Learning Disorders

Interdisciplinary Council on

Special Edition

Simon Baron-Cohen, Ph.D., et. al.

Christopher Gillberg, M.D. Stanley I. Greenspan, M.D. Nancy Minshew, M.D. Peter Tanguay, M.D., et. al.

Andrew W. Zimmerman, M.D. and Barry Gordon, M.D., Ph.D.

Volume 5 Number 1 2001

Developmental and Learning Disorders

Journal of Developmental and Learning Disorders EDITORIAL POLICY The goal of The Journal of Developmental and Learning Disorders is to improve the identification, prevention and treatment of disorders that interfere with adaptive developmental and learning processes.

Many disciplines work with these disorders, including, for example, child development, psychology, psychiatry (child and adult), social work, education (including special and early childhood), neurology, pediatrics, speech language pathology, occupational and physical therapy, nursing and others. Those who work with developmental and learning disorders often have opportunities to communicate with colleagues within their own disciplines, but less often with those in other disciplines who share the same concerns and interests. Yet, each of the disciplines is discovering its overlap with other fields, as well as new ways to identify, prevent and treat developmental problems. There is also enormous growth in research on the development of the nervous system and the various physical, psychological, and cognitive factors that influence it. Many of these discoveries are informing the development of new diagnostic and intervention approaches.

The Journal will present research, clinical and case studies from various disciplines working with developmental and learning disorders. It will also report on new information, events, services, training, and networking activities taking place throughout the country and the world, providing periodic information updates and overviews. The Journal will cover a range of topics, including overviews of important and growing areas, new research, clinical observations, intervention studies, discussions of clinical practice, and educational interventions.

As of the fall 2001 the Journal has begun a new policy and will be published in hard copy once a year. Articles that have been peer reviewed and accepted for publication in our Journal will be posted on our website at WWW.ICDL.COM. Each fall we will publish the Journal in hard copy containing all of the articles for that year.

Call for Papers The Journal of Developmental and Learning Disorders, an official publication of the Interdisciplinary Council on Developmental and Learning Disorders, encourages original submissions. Papers will be peer reviewed. Please submit five copies, double spaced and a disk in Word format. Tables, charts and pictures should be submitted in camera ready format. The title page should include the author’s full name, street and e-mail address, telephone and fax numbers, affiliation, and a 150 word summary of contents (abstract). Reference format is American Psychological Association style.

Send submissions to: Ms. J. Raphael, MSW, 3213 Midfield Road, Baltimore, Maryland 21208. Phone or fax: (410) 486-1251. E-mail: JO@ICDL.COM. For subscription information: (301) 656-2667 or WWW.ICDL.COM.

JOURNAL OF DEVELOPMENTAL AND LEARNING DISORDERS Volume 5

2001

Number 1

CONTENTS

The Affect Diathesis Hypothesis: The Role of Emotions in the Core Deficit in Autism and in the Development of Intelligence and Social Skills— Stanley I. Greenspan, M.D. Studies of Theory of Mind: Are Intuitive Physics and Intuitive Psychology Independent?—Simon Baron-Cohen, Sally Wheelwright, Amanda Spong, Victoria Scahill and John Lawson Asperger Syndrome and High Functioning Autism: Shared Deficits or Different Disorders?—Christopher Gillberg, M.D., Ph.D. A System of Classification for Autism Spectrum Disorder—Peter E. Tanguay, M.D., Julia Robertson, M.D., Ann Derrick, A.R.N.P., M.S., C.S. The Core Deficit in Autism and Autistic Spectrum Disorders— Nancy J. Minshew, M.D. Neural Mechanisms in Autism—Andrew W. Zimmerman, MD and Barry Gordon, M.D., Ph.D.

ICDL Bethesda, Maryland

Copyright © 2001

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Journal of Developmental and Learning Disorders Editor Stanley I. Greenspan, M.D. George Washington University Associate Editor Serena Wieder, Ph.D. Assistant Editor Georgia DeGangi, Ph.D. Treatment and Learning Center Administrative Editor Jo Raphael, M.S.W. Editorial Board Margaret Bauman, M.D. Harvard University

Toby Long, Ph.D., P.T. Georgetown University

Harry Chugani, M.D. Wayne State University

Stephen W. Porges, Ph.D. University of Maryland

Leon Cytryn, M.D. George Washington University

Barry Prizant, Ph.D., C.C.C.-S.L.P. Brown University

Sima Gerber, Ph.D. Queens College

Ricki G. Robinson, M.D., Ph. D. University of Southern California

Arnold P. Gold, M.D. Columbia University

Rebecca Shahmoon Shanok, M.S.W., Ph.D. Child Development Center, New York

Myron Hofer, M.D. Columbia University

Milton Shore, Ph.D. Catholic University

Pnina Klein, Ph.D. Bar-Ilan University, Israel

Richard Solomon, M.D. University of Michigan

Pat Lindamood, M.S., C.C.C.-S.L.P. Lindamood-Bell Learning Processes

THE AFFECT DIATHESIS HYPOTHESIS: The Role of Emotions in the Core Deficit in Autism and in the Development of Intelligence and Social Skills

Stanley I. Greenspan, M.D.

Abstract. In this paper we will explore the role of affect in the core deficit in autism and in the development of intelligence and social skills. We discuss how children with autistic spectrum disorders may uniquely, for biological reasons, miss a critical developmental capacity, the ability to connect affect or intent to motor planning and sequencing capacities as well as symbol formation and, therefore, have a difficult time engaging in the long reciprocal chains of affective interaction so necessary for creative and abstract thinking and high-level social skills (Affect Diathesis Hypothesis). We will also discuss how these same affective interactions underlie intelligence and social development. Additionally, we explain that to improve assessments and interventions for children with a variety of challenges including autistic spectrum disorders, it is imperative to appreciate the role of affective interchanges in disordered and healthy development. Finally, we explain that to fully operationalize the role of affective interaction and the Affect Diathesis Hypothesis for the assessment and intervention process, we have formulated the Developmental, Individual-Difference, Relationship-Based model (DIR) (Greenspan, 1992, 1997b; Greenspan & Wieder, 1997, 1998, 1999).

The Affect Diathesis Hypothesis Introduction There is a growing appreciation of the role of emotional interactions in human development. It’s been long acknowledged that affective exchanges influence such basic capacities as the formation of relationships, self esteem, and impulse control.

Recent studies suggest that emotional interaction in infancy and early childhood also influences cognitive and language capacities. For example, higher quality care, including emotionally sensitive caregiving, is associated with stronger cognitive, language, and emotional and social development (NICHD, 1998, 1999, 2000; Vandell & Wolfe, 2000; Peisner-Feinberg, et al., 1999). Risk factors that undermine

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caregiver and family emotional functioning are associated with compromises to intellectual functioning (Sameroff, Seifer, Barocas, Zax, & Greenspan, 1986; Sameroff, Seifer, Baldwin, & Baldwin, 1993). A large empirical base, neurological research looking at brain lesions interfering with emotional regulation, explorations of the types of thinking that are part of skillful social interactions (i.e., emotional intelligence), and concepts of multiple intelligences have further increased interest in the role of emotions (Shonkoff & Phillips, 2000; Damasio, 1994; Goleman, 1995; Gardner, 1983).

In spite of greater interest in the role of emotions in human development, however, there has not been sufficient understanding of how emotions exert their influence. How do emotions and emotional interactions affect intelligence and its related cognitive and language capacities as well as many complex social and self-regulation capacities? What are the psychological mechanisms of action by which affects work on these different aspects of the mind?

In The Growth of the Mind (Greenspan, 1997), we presented a theory of the process through which emotional interactions influence intelligence. This theory suggested that affective interactions emerge earlier than the sensorimotor schemes postulated

by Piaget (1962) and that they are the most primary probes we use to understand, conceptualize, and “double code” our experiences with the world. It also suggested that most types of abstract thinking are based on reflections on these personal affective experiences.

In this article, we further develop this theory regarding how emotional processes influence various aspects of the mind. The Affect Diathesis Hypothesis examines the critical role of affective interactions in self-regulation, communication, language, creating meanings, and constructing a sense of reality. It also examines how various types of deficits in the expectable diathesis (i.e., spread) of affects during early development contributes to our understanding of autistic phenomena and other developmental and emotional problems.

Part 1: The Affect Diathesis Hypothesis and Autistic Spectrum Disorders Among the many symptoms of autism, language, cognitive, and social deficits are prominent. Recent studies suggest that these compromises can be conceptualized as a series of functional developmental deficits. The pattern of these deficits provide clues regarding a core psychological mechanism that may express the neurological differences characterizing autistic spectrum disorders. When children with autism are compared to children without autism, and level of intelligence, as measured with IQ tests, is controlled for, there are a number of autism-specific functional developmental problems. These include deficits in the ability for empathy and seeing the world from another person’s perspective in both physical and emotional contexts (theory of mind) (Baron-Cohen, 1994); higher-level abstract thinking, including making inferences (Minshew & Goldstein, 1998); and shared

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attention, including social referencing and problem-solving (Mundy, Sigman, & Kasari, 1990). In addition, deficits in the capacities for affective reciprocity (Baranek, 1999; Dawson & Galpert, 1990; Lewy & Dawson, 1992; Osterling & Dawson, 1994; Tanguay, 1999; Tanguay, Robertson, & Derrick, 1998) and functional (pragmatic) language (Wetherby & Prizant, 1993) also appear specific to autism.

Do these functional developmental deficits stem from a common pathway? In clinical work with infants and children with biological and environmental challenges and without challenges, we have found that the capacities for empathy, psychological mindedness, abstract thinking, social problem-solving, functional language, and affective reciprocity all stem from the infant’s ability to connect affect or intent to motor planning capacities and emerging symbols (Greenspan, 1979, 1989, 1997a).

Relative deficits in this core capacity leads to problems in higher-level emotional and intellectual processes. The core psychological deficit in autism may, therefore, involve an inability to connect affect (i.e., intent) to motor planning and sequencing capacities and symbol formation.

A child’s capacity to connect affect to motor planning and emerging symbols becomes relatively apparent between 9 and 18 months of age as the infant shifts from simple patterns of engagement and reciprocity to complex chains of affective reciprocity that involve problem-solving interactions. Consider a 14-month-old child who takes his father by the hand and pulls him to the toy area, points to the shelf, and motions for a toy. As Dad picks him up, and he reaches for and gets the toy, he nods, smiles, and bubbles with pleasure. For this complex, problem-solving social interaction to occur, the infant needs to have an emotional desire or wish (i.e., intent or affective interest) that indicates what he wants. The infant then needs to connect his desire or affective interest to an action plan (i.e., a plan to get his toy). The direction-giving affects and the action plan together enable the child to create a pattern of meaningful, social, problem-solving interactions. Without this connection between affect and action plans, complex interactive problem-solving patterns are not possible. Action plans without affective direction or meaning tend to become repetitive (perseverative), aimless, or self-stimulatory, which is what is observed when there is a deficit in this core capacity.

As the ability to form symbols emerges, the child needs to connect her inner affects (intent) to symbols to create meaningful ideas, such as those involved in functional language, imagination, and creative and logical thought. The meaningful use of symbols usually emerges from earlier and continuing meaningful (affect-mediated) problem-solving interactions that enable a toddler to understand the patterns in her world and eventually use symbols to convey these patterns in thought and dialogue.

Without affective connections, symbols like action plans are used in a repetitive (perseverative) manner (e.g., scripting, echolalia).

The capacity to connect affect to action plans and symbols is likely part of a larger transformation of affect. The infant goes from global and/or catastrophic affective patterns (in the early months of life) to reciprocal ones. The capacity for engaging in a continuous flow of reciprocal affective interactions enables the child to modulate

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mood and behavior, functional preverbal and verbal communication, and thinking.

It also enables more flexible scanning of the environment because the child gets feedback from what he sees and, based on that feedback, explores further. There is, therefore, more integrated visual-spatial and motor functioning because intense global affects push for discharge and vigilant or overly focused or highly distractible visualmotor patterns, whereas long chains of reciprocal interaction support back-and-forth exploration of the environment and, therefore, flexible, broad, integrated perceptual patterns.

In facilitating back-and-forth interaction with the environment, the capacity for reciprocal interaction also facilitates associative learning. Associative learning (building up a reservoir of related experiences, thoughts, feelings, and behaviors which give range and depth to one’s personality, inner life, and adaptive responses) is necessary for healthy mental growth. Its absence leads to rigid, mechanical feelings, thinking, and behavior patterns, as are often seen in autistic spectrum disorders.

Reciprocal, affective interactions and affectively-guided problem-solving interactions and symbols, as can be seen, are necessary for all the unique capacities that distinguish individuals with autism from individuals without autism, as outlined earlier. For example, long chains of social reciprocity depend on affect guiding interactive social behavior. Shared attention, which includes social referencing and shared problem-solving, also depends on affect guiding interactive social behavior.

Empathy and theory of mind capacities depend on the ability to understand both one’s own affects or feelings and another person’s affects or feelings and to project oneself into the other person’s mindset. This complex emotional and cognitive task begins with the ability to exchange affect signals with another person and, through these exchanges, emotionally sense one’s own intent and the other person’s intent through a sense of “self” in interaction with another. Similarly, higher-level abstract thinking skills, such as making inferences, depend on the ability to generate new ideas from one’s own affective experiences and then reflect on and categorize them (Greenspan, 1997a).

In observations of infants and toddlers heading into autistic patterns and in taking careful histories of older children with autism, we noted that children with autistic spectrum patterns did not fully make the transition from simple patterns of engagement and interaction into complex affect-mediated, social problem-solving interactions. They, by and large, did not progress to a continuous flow of back-and-forth, affective, problem-solving interchanges (i.e., a continuous flow of circles of communication). Even affectionate children who were repeating a few words or memorizing numbers and letters, and who went on to evidence autistic patterns, did not master, for the most part, this early capacity to engage in a continuous flow of affectmediated, gestural interactions. They were also unable to develop empathy and creative and abstract thinking unless they were involved in an intervention that focused on facilitating affect-mediated interactions.

In a review of the functional developmental profiles of 200 children with autistic spectrum disorders, we observed that most of the children shared this unique

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processing deficit. Approximately two-thirds of the children who developed autistic spectrum disorders had this unique type of biologically based processing deficit that involved the connection of affect or intent to motor planning and sequencing capacities as well as to emerging symbolic capacities (Greenspan & Wieder, 1997). At the same time, however, the children differed with regard to other processing deficits involving their auditory, motor planning, visual-spatial, and sensory modulation abilities. These differences accounted for the different types and degrees of language, motor, and cognitive impairments that accompany the fundamental deficit in engaging in fully purposeful and meaningful social and intellectual interactions.

The hypothesis that explores the connection between affect and different processing capacities (the core deficit) is called the affect diathesis hypothesis. In this hypothesis, as indicated previously, a child uses his affect to provide intent (i.e., direction) for his actions and meaning for his words. Typically, during the second year of life, a child begins to use his affect to guide intentional problem-solving behavior and, later on, meaningful use of symbols and language. Through many affective problem-solving interactions, the child develops complex social skills and higherlevel emotional and intellectual capacities.

Because this unique processing deficit occurs early in life, it can undermine the toddler’s capacity to engage in expectable learning interactions essential for many critical emotional and cognitive skills. For example, she may have more difficulty eliciting ordinary expectable interactions from her parents and the people in her immediate environment. She may perplex, confuse, frustrate, and undermine purposeful, interactive communication with even very competent parents. Without appropriate interaction, she may not be able to comprehend the rules of complex social interactions or to develop a sense of self. These may include implicit social functions and social “rules,” and developing friendships and a sense of humor, which are learned at an especially rapid rate between 12 and 24 months of age (Bell, 1970; Emde, Biringen, Clyman, & Oppenheim, 1991; Greenspan, 1979, 1997a; Kagan, 1981; Piaget 1981/1954; Werner & Kaplan, 1963; Winnicott, 1931). By the time a child with processing difficulties receives professional attention, her challenging interaction patterns with her caregivers have, therefore, excluded her from important learning interactions and may be intensifying her difficulties. The loss of engagement and intentional, interactive relatedness to key caregivers may cause her to withdraw more idiosyncratically into her own world and become even more aimless and/or repetitive. What later looks like a primary biological deficit may, therefore, be part of a dynamic process through which the child’s lack of affective reciprocal interactions has intensified specific, early, biologically-based processing problems and derailed the learning of critical social and intellectual skills.

The capacity for long chains of affective reciprocity may have early roots which can potentially lead to earlier opportunities for identifying risk patterns. A precursor of the capacity to connect affect to motor planning and symbol formation in the second year of life may be the capacity observed initially in the early months of life for connecting motor actions to interactive, affective rhythms conveyed through facial expressions, vocalizations, or other gestures. For example, babies will move

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rhythmically to the rhythm of their mother’s voice (Condon & Sander, 1974; Condon, 1975). We are currently conducting studies to see if children at risk for autistic spectrum disorders evidence a deficit in their earlier, rhythmic affective-motor patterns as well. The Affect Diathesis Hypothesis may, therefore, involve a number of developmental levels. This possibility has important implications for early identification and preventive strategies.

Biologically based processing (regulatory) difficulties often contribute to, but are not always decisive in, determining relationship and communication difficulties.

When problems are perceived early, appropriate professional help can, to varying degrees, teach children and caregivers how to work with the processing (regulatory) dysfunction, including helping the toddler connect affect to emerging action plans and associated relationship and communication patterns. Many children can become capable of forming warm relationships and, to varying degrees, climb the developmental ladder leading to language and thinking capacities.

There are many children who do not evidence autism but have developmental problems in which intentionality or purposeful action is difficult in its own right (e.g., severe motor problems). Such problems result in less practice in using intentional behavior and participating in intentional interactions. These children may, therefore, either have difficulty forming or may secondarily lose their ability to connect intent or affect to motor planning because they are unable to exercise this critical function (i.e., their impaired motor skills make purposeful action difficult). In these circumstances, creating purposeful interactions around any motor skill (e.g., head or tongue movements) may strengthen the affect-motor connection and reduce aimless, repetitive behavior, thereby facilitating problem-solving and thinking. Recent MRI studies suggest that practicing and improving motor skills may enhance the developmental plasticity of neuronal connections (Zimmerman & Gordon, 2000).

Also, as indicated, in our review of 200 cases of autistic spectrum disorders, although many children shared a primary deficit (i.e., connecting affect to processing capacities), their differences in the levels and strengths of developmental functioning in other processing capacities or “component parts” tended to determine symptoms and splinter skills, such as whether a child lined up toys (which requires some motor planning) or just banged them, or scripted TV shows (which requires some auditory memory) or was silent. It was also found that children with relatively stronger component parts tended to make rapid progress once they were helped to connect affect or intent to their other processing capacities. Children with weaker component parts tended to make more gradual progress and required specific therapies, such as speech and occupational therapy in an intensive manner, in order to improve the component part directly, as well as work with the affect-component part connection.

These observations are consistent with recent neuroscience studies suggesting that different processing capacities may compete for cortical access, depending on functional use (Zimmerman & Gordon, 2000). They are also consistent with neuropsychological studies of individuals with autism, but without mental retardation, that show that “within affected domains, impairments consistently involved the most complex tasks dependent on higher-order abilities” (i.e., concept formation, complex

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memory, complex language, and complex motor abilities) (Minshew & Goldstein, 1998). Higher-level capacities tend to depend more on “meanings” which, in turn, depend on affective interactions with the world. Furthermore, these observations are also consistent with work on the shifts to a more complex central nervous system organization, including hemispheric connections that occur at the end of the first year of life and early part of the second year, just as the ability to engage in affectmediated chains of social problem solving are on the ascendancy (Benson & Zaidel, 1985; Courchesne, et al., 1994; Dawson, Warrenburg, & Fuller, 1982; Sperry, 1985).

Interestingly, many children with autistic spectrum disorders use peripheral vision, rather than central vision, to scan their environment (i.e., they don’t look directly at caregivers but seem to look from the side). The neuroanatomy of the visual tracks is such that peripheral vision only requires one hemisphere, the left or right one, to function. Central vision, however, requires both hemispheres to function together (because some of the pathways cross over and others do not). It would be reasonable to explore the hypotheses that problems in integrating the two hemispheres, which facilitates long chains of reciprocal, affective interaction and integrated central vision, may contribute to autistic spectrum patterns. Work showing that the limbic system and hippocampus is developing, including forming cortical connections, at around 11/2 years of age, is also consistent with these clinical observations on the increasingly purposeful and meaningful use of actions and ideas in the second year of life (Bauman, 2000).

Part II: Transformation of Affects in the First Three Years of Life Historically, emotions or affects have been viewed in a number of ways: as outlets for extreme passion, as physiologic reactions, as subjective states of feeling, as interpersonal social cues (Young, 1943; Greenspan, 1997b). Beginning nearly six decades ago, the importance of emotions for aspects of learning was documented by psychoanalytic observers such as René Spitz and John Bowlby, who described the effects of emotional deprivation, and Heinz Hartmann and David Rappaport, who explored clinical and theoretical relationships (Spitz, 1945; Bowlby, 1952; Hartmann, 1939; Rappaport, 1960). Sibylle Escalona (1968) and Lois Murphy (1974) further explored affective development and described individual differences in infants and their relationship to psychopathology. Building on this work, Pediatrician T. Berry Brazelton systematized the observation of the infant’s social and emotional repertoire (Brazelton & Cramer, 1990). In Intelligence and Adaptation (1979) and other works (Greenspan, 1989, 1992; Greenspan & Greenspan, 1985; Greenspan & Lourie, 1981; Greenspan & Wieder, 1998, 1999), Greenspan presented developmental observations and a model to integrate cognitive and affective aspects of the developing mind. In The Growth of the Mind (1997b), Greenspan showed how emotions create, organize, and orchestrate many of the mind’s most important functions, including intelligence and emotional health. He further

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showed that intellect, academic abilities, sense of self, consciousness, and morality have common origins in our earliest and ongoing emotional experiences and that emotions are the architects of a vast array of cognitive operations throughout the life span.

During the formative years there is a sensitive interaction between genetic proclivities and environmental experience. Experience appears to adapt the infant’s biology to his or her environment (Hofer, 1988, 1995; Rakic, Bourgeois, & GoldmanRakic, 1994; Greenough & Black, 1992; Weiler, Hawrylak, and Greenough, 1995; Holloway, 1966; Turner & Greenough, 1983; Turner & Greenough, 1985; ThinusBlanc, 1981; Wiesel & Hubel, 1963; Singer, 1986; Hein & Diamond, 1983; Schanberg & Field, 1987). In this process, however, not all experiences are the same. As described in the prior section, children seem to require certain types of experiences involving a series of specific types of emotional interactions geared to their particular developmental needs.

The difficulty in connecting affect to motor planning and symbols discussed in the last section is only one part of a larger set of transformations of affect that depend on specific types of emotional interactions. To more fully understand the importance of affect in autism, and the development of intellectual and social skills, it may prove useful to explore a number of affective transformations during the first three years of life.

In the first year, affects become more complex. There is a transition from simple affective states like hunger and arousal to, by 8 months, complex affect states like surprise, fear and caution, joy and happiness, and enthusiasm and curiosity. As the child progresses, affects become more differentiated. Eventually, affects organize reciprocal interactions and problem-solving. Then they become symbolized. Eventually, it becomes possible to reflect on them. The transformations affects undergo can be described in terms of six core early organizations that give the organism its desire to act and underlie intelligence and emotional health (Greenspan, 1997b).

First, to attend to the outside world, and eventually to have joint attention or shared attention, requires affective interest in the world outside one’s own body—in sights, sounds, and movements. Obviously, parents who provide pleasurable sights and sounds to a new baby will entice the baby into focusing on the world. Babies who are visually hypersensitive or auditorially hypersensitive will need a different type of enticement—a more soothing type—to take an interest in that outside world.

Babies who are underreactive will require more animated interactions. Consider infants with low muscle tone who are underreactive and who grow up in institutional care. They often lose weight and some don’t survive.

An early and continuing component of shared attention involves attending to the world outside one’s own body with rhythmic, affectively-mediated perceptual motor patterns. For example, in the early months of life, babies can be observed to move their arms and legs in rhythm to their mother’s voices (Condon & Sander, 1974; Condon, 1975). Soon they begin integrating what they hear and see (Spelke, 1976).

By four to five months, one can readily observe synchronous movement in rhythm with mother’s affective communication via her voice, facial expressions, or

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body movements. As development proceeds, reciprocal gestural, vocal, and verbal communication generally occurs in an interactive rhythm. A consequence of this may be the observation that it’s harder to remember or understand verbal phrases presented in a monotone than in an affective rhythm.

The second functional developmental capacity is engagement. For an infant to engage with a caregiver requires joy and pleasure in that relationship. When that’s not present, children can withdraw and become self-absorbed. For children who have processing problems, it may be much harder to pull them into that joyful relationship. But in clinical work, we have not encountered many children evidencing autistic spectrum disorders who could not be pulled into greater degrees of relating through therapeutic work that works with their processing differences and relationships at the same time. Engagement and relating appears to be a very flexible capacity. While language and certain cognitive functions may improve slowly for some children, the capacity for warmth and relatedness seems to progress more readily.

The third functional developmental capacity is two-way purposeful communication. Two-way communication and affective reciprocity, which Peter Tanguay and Simon Baron-Cohen discuss (in this issue) obviously requires affect to provide the “intent.” When an infant reaches for Daddy to take the rattle off his head or hand it back to him, or gets into a back-and-forth smiling game, one clearly sees affect (intent) guiding the interaction (i.e., the infant wants that rattle). Piaget thought means-ends relationships occurred at nine months with motor behavior (i.e., an infant reaching and pulling a string to ring a bell). But Piaget missed the role of affect.

The baby’s affective probe occurs much earlier than the motor probe. Causal affective behavior occurs earlier than causal large muscle motor behavior. First we see a smile begetting a smile, a frown begetting a frown. Later on, we see the baby reach for and give back objects. At this stage as well, the affect diathesis is occurring, now transforming relating into two-way, affective communication (rather than just joyful interest in the caregiver).

The fourth level of transformation occurs between 10 months and 18 months. It involves the development of a range of new capacities, all related to the toddler’s ability to engage in longer sequences of affective reciprocal interactions with clear intent or problem-solving goals and the ability to perceive and interact in these larger patterns. This transformation enables the toddler to form a more integrated sense of self, integrate affective polarities, social problem-solve, and broaden visual-spatial and auditory processing abilities.

As indicated earlier, during this stage we often start seeing differences with some of the children who will be diagnosed with autistic spectrum disorders. Many of the children have relative degrees of mastery of the first three stages, but the fourth stage is more difficult. Now, the infant has to connect his affect to his motor planning and sequencing, as well as his emerging symbol formation. In order to be able to take a parent by the hand and walk him to the toy area and point to the toy that he wants, the infant has to have both a constant inner signal of intent or affect and a motor plan which is connected to it. If either one of those are problematic the infant may not be

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able to implement complex, problem-solving, social behavior. As a child begins to imitate words (“Mom,” “Dad,” “go,” “door”), those symbols or words have to be invested with affect to have meaning. The word “juice” only has meaning to the degree the child can invest the words with the many affective experiences that come to mean “juice,” including the pleasure and image of drinking the juice.

Even grammar, which Chomsky and other linguists have assumed is innate, depends on affect and affective interactions to become functional. Children with autistic spectrum disorders frequently verbalize nouns in a repetitious way (“Door, door.”). If the intervention can get them affectively interactive, however, they can often learn to use proper grammar. For example, a child is opening and closing a door. We get stuck behind the door. If they push us away, they are becoming purposeful. Purposeful, affectively-mediated behavior creates a foundation for the purposeful and meaningful use of words. Soon the same child is saying “go” while pushing us away. We may then say, “Where go? Where go?” We might further say, “Should we go away or stay? Away or stay?” The child may say, “Go away, go away.”

Now the child is using correct grammar. Noam Chomsky and his colleagues (Chomsky, 1966, 1980; Pinker, 1994) were mistaken when they thought that grammar was largely innate and that only experience in a very general sense was required to turn on the language switch. Grammar requires very specific types of affective experience. Affective reciprocity is needed to create purposeful action and then related purposeful symbols or words. The affect, by providing intent, enables the components of language to align (e.g., “open door” versus “door, door, door.”). Many investigators may have missed the importance of affective reciprocity because it occurs routinely with most infants and toddlers and their caregivers.

At the fourth level of transformation many complex social problem-solving interactions, in addition to involving vocalizations and words, involve visual-spatial patterns. Johnny can find his mother in the other room because between 12 months and 18 months, he has learned to construct a visual-spatial road map of the house. This road map allows him to do what Margaret Mahler described as “separation-individuation” (Mahler, Pine, & Bergman, 1975). He explores independently, but then comes back to his base of security for “refueling.” Mahler, however, did not realize, he could use his visual-spatial processing and auditory processing to refuel from afar.

He can have his security blanket from across the room, either by looking at Mom and communicating with looks or other gestures or by hearing her voice from another room and figuring out where she is based on her voice. If his visual-spatial or auditory processing is weak, or the affect system is not investing his visual-spatial or auditory processing, however, this emerging capacity will not properly form.

Simon Baron-Cohen (in this issue) describes the folking of cognition and divides children into the physicists (interested in the mechanics of things) and the novelist group (interested in people and emotional interactions) in terms of relative cognitive and social strengths and weaknesses. What happens, however, when a child has strong visual-spatial and mechanical skills and invests that system with a lot of pleasurable affective experience with primary caregivers? Do they become both a physicist and a poet (i.e., a physicist with a warm heart, big smile, and feel for people)?

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One possibility is yes. We have observed that children who are able to use strong visual-spatial systems in reciprocal affective interactions often use physical metaphors to deal with emotions. They’re not the kind of people who are afraid of affect or feeling. Quite to the contrary, they talk about their feelings, but often use physical images to communicate (“I feel as angry as a four megaton nuclear blast!”).

The affect diathesis hypothesis suggests that affect invests not simply the capacity for complex interactions to give meaning to sounds, words, and behaviors, but also invests processing capacities, such as motor planning and visual spatial processing. It gives meaning and functional range to these capacities. Individuals can then use different processing capacities in a variety of ways—not just to solve an equation, but also for social, personal problem-solving (e.g., figuring out how to work the crowd politically).

It may not appear obvious how to affectively interact through the visual-spatial system. But, playing chase games, hide-and-go-seek games, and treasure hunts are good vehicles for bringing visual-spatial capacities into an affective context, as are discussions involving how angry or loving we feel on a 1–10 scale. This is exactly what we do with some children who need more work “affecting” their visual-spatial and motor planning systems. The stage for these types of games are often set earlier in the third and early fourth stages, with peek-a-boo and other types of play that combine pleasurable affect, affective expectation, and visual-spatial processing.

In this fourth stage, the child is also beginning to integrate affective polarities.

Early on, infants tend to have extreme affect states—all happy or gleeful or all sad— but by 18 to 19 months we see children begin to shift affect states more readily and actually integrate affect states such as happiness and sadness, anger and closeness.

They can be angry and then seem to want forgiveness and make up. When playing with a 13-month-old child, it feels like if he were angry and had a gun, he very well might pull the trigger. With the 18-month-old, it feels like he integrates his caring and anger. He might look mad and feel connected and warm at the same time. One can often feel the quality of these affect states when playing with infants and toddlers at different ages.

Complex affective patterns emerging during this fourth transformation lead to patterns of affective expectations. A toddler purposefully behaves cooperatively, hams it up and acts funny, or becomes mischievous, all in relation to specific internal states. A child also anticipates what Daddy’s going to do next when he comes home. He looks at his face and if it’s angry, he hides behind the door. If he looks like he’s feeling warm and will be nice, the toddler will run up and flirt with him. The toddler can anticipate the “other” as well as the “self” in terms of affects and behaviors. This capacity sets the stage for many of the “theory of mind” tasks that Simon Baron-Cohen describes (this issue).

At the fifth level, transformations involve the affect system investing ideas. For example, in pretend play, affects or desires drive the theme (dolls hugging or kissing) as well as functional language (“I’m hungry,” “I’m angry,” “Give me that.” “Look! I want to show you something.”). Functional language, whether it’s on a need basis (Give me juice.”), or at a collaborative “show you this or that,” or sharing opinions

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“I didn’t like that” basis, is very different from simply labeling objects or pictures.

Here is also where IQ tests fall down. IQ tests don’t discriminate well enough between the different uses of ideas and language, such as between pragmatic language or creative and abstract thinking and simply using language to label objects or for rote, memory-based problems.

Many researchers use IQ tests to create comparable groups. For example, children with autism and without autism are matched on IQ tests and then given theory of mind tasks or other cognitive tasks. The goal is to see if the children with and without autism differ on theory of mind tasks when they have similar IQs. If they differ, it would suggest that theory of mind tasks distinguish autistic from non-autistic children. But, there is a problem with this approach. Even though the groups have similar IQs, they may not be the same in terms of their intelligence. Their intelligence patterns may be quite different. For example, they may have very different pragmatic language levels and very different abstract reasoning skills. In these studies, we must control for pragmatic language and abstract thinking (i.e., true intelligence), not IQ, if we want to get at the essence root of how certain cognitive capacities, such as those involved in theory of mind tasks, are related to autistic spectrum disorders. In other words, theory of mind capacities may relate more to the level of pragmatic language and abstract thinking than to whether a child does or does not have autism. Only proper control groups can tease out this distinction.

Research on theory of mind tasks and other cognitive or perceptual capacities, such as the ability to discriminate facial expressions to be cognitively rather than affectively oriented. For example, asking a child to figure out how another child is feeling in the middle of a power struggle, in heated debate, or in situations that might lead to disappointment or sadness, would get at his ability to understand someone else’s true emotions in an emotional context. Figuring out what someone else will see in a room, on the other hand, or identifying pictures of facial expressions are more cognitive and perceptual tasks. These areas of research have led to cognitively oriented interventions. These interventions do not work enough at the level of affective interchanges. The importance of engaging in long chains of reciprocal affect cueing in order to establish a sense of self and a sense of other (through these back-and-forth affect signals) is often overlooked in many of these interventions. The cognitive procedures utilized in such interventions are many steps removed from the affective interchanges that are necessary to establish the compromised capacities.

For example, there has been a great deal of interest in children with autistic spectrum disorder evidencing difficulty in discriminating facial expressions of different emotions. Based on this research, children who have trouble interpreting the emotional expressions of others are “taught” about emotional expressions by looking at pictures of people with different facial expressions or through identifying emotional expressions of others in structured exercises. This conscious cognitive appreciation of a picture is, however, not what’s missing. What’s missing is the intuitive, almost automatic sense of another person’s affect. This is the capacity one uses in appreciating a friend’s subtle, emotional state or in working the crowd at a cocktail party.

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In other words, the understanding of the other person’s emotions is experienced very rapidly through a personal, visceral, emotional reaction. In fact, we can often respond to the person’s affect before it even consciously registers. Thus, we flirt back, look puzzled or grimace in anger as part of our intuitive, affective response. Once we have experienced, at the intuitive level, the other person’s emotional signal, we can also reflect on it in a conscious and deliberate manner. We may say to ourselves, “they look sad” or happy or angry. In making these determinations, however, we are relying on our own affective response, not simply on the other person’s facial expression. Also, as indicated, in the ordinary course of events, such as working the crowd at a cocktail party or negotiating peer relationships on the playground, there are many affect signals being exchanged in a brief period of time. If a child or adult consciously tries to figure out each separate one, they will be doomed to failure and confusion. Therefore, the only way to help a child with problems reading affect signals is to provide him or her extra practice in experiencing and reading those signals (i.e., in social situations involving lots of reciprocal, affective interactions, initially with one-on-one caregiver, child, and peer play and gradually in more complex situations). The “practice” needs to involve the personal inner experiences of someone else’s affect, as well as one’s own, in a series of reciprocal interactions. Similarly, children who have theory of mind problems are often provided with cognitive exercises involving figuring out other people’s perspectives, rather than working at the primary level of affective signaling, which is often compromised and at the core of these children’s problems.

Some may believe that children with autism or Asperger’s Syndrome are not able to learn to feel their own and someone else’s affect and, therefore, can only learn to read facial expressions through pictures or perform theory of mind tasks in a conscious, deliberate manner. We have found this assumption not to be correct. With a program focusing on relating and affect cueing, the majority of children made progress in this capacity (Greenspan & Wieder, 1997).

In general, the missing piece in many intervention programs is a lack of understanding of the developmental steps involved in acquiring certain cognitive, social, and emotional skills. By understanding these steps, which often involve transformations of affect, intervention strategies can help the child master the critical foundations for cognitive and social skills.

At the sixth level of transformation, a child builds bridges between affectively meaningful ideas. Establishing reality-testing, a symbolic sense of self, and moving back and forth between fantasy to reality depends on reaching this next level. For example, critical to establishing reality-testing (which is the basis for later abstract thinking) is an affective “me” intending to do something with an affective “other.”

There has to be an interaction involving affect between the “me” and the “other” to establish a psychological boundary (i.e., an affective sense of what’s “me” and an affective sense of what’s “outside me”). That boundary doesn’t come out of reading books or out of doing puzzles. It comes from interactions involving the exchange of affective gestures and symbols. It comes out of interactions such as “I want this.” “No, you can’t have it,” or “Yes, you can.” In addition, these interactions must be part of

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a continuous flow of back-and-forth affective gestures. Islands of affective interactions followed by self absorption leads to an “in and out” affective probe or rhythm with the external world (reality). A stable sense of reality requires a continuous interactive relationship to the significant “others” in our lives. Abstract and inferential thinking grows from a solid reality boundary.

A stable reality boundary also allows empathy to develop. A child can project a “me” into a “you” and figure out how “you’re” feeling to the degree that a child has established a separate sense of “me.”

In this context, abstract thinking, empathy and theory of mind tasks are extensions of the stage of building bridges between affective ideas. In addition to affective interactions, the child’s individual differences in processing capacities (i.e., visualspatial processing, motor planning, auditory processing) will contribute to these advanced mental capacities and they have to be taken into account in considering these capacities.

For example, consider the theory of mind task Simon Baron-Cohen (this issue) has described where the child is looking into the basket and the other child has to describe what he’s doing. In a task like that, if we show one child a diagram, he’ll get it and tell you exactly what the other child is doing. But if we describe it in words to that child (not visually, but auditorially). “Gee, a child is looking in, what is he seeing?” The child won’t get it. Another child, however (also with an autistic spectrum disorder), may be just the opposite—stronger with the verbal than the visual. The processing capacity is, therefore, a very important component of a child’s ability for, and pattern of, abstract thinking and empathy. Also, if a child has sequencing problems and there are five steps in the problem, the child may get lost simply because of the sequencing challenge, not because of an inability to project himself into someone else’s shoes. Therefore, higher levels of abstract thinking, including theory of mind tasks, may occur in certain processing modalities and not other modalities and with regard to certain affect realms and not others.

In summary, we’ve described the affect transformation that occurs in each of the six functional developmental capacities. Affect is responsible for helping the child go from simple interest in the world all the way up through social problem-solving (and procedural knowledge). It enables a child to progress through procedural knowledge up to symbolic knowledge. It gives meaning to what the child hears and how he processes visual-spatial information and sequences motor actions.1 1 The importance of genes is often cited to minimize the role of affective interactions and the environment, but the role of genes is more complex than is often acknowledged. Consider a very interesting study on schizophrenia. Investigators looked at identical twins that shared a placenta and identical twins that did not share a placenta. The concordance rates of the identical twins that shared a placenta was very high in keeping with the literature on the genetic basis of schizophrenia. The concordance rates of identical twins that did not share a placenta were very low close to the rates for dizygotic twins (Davis, Phelps, & Bracha, 1995). Therefore, unless we control for the sharing of a placenta, we won’t know how much the genes contribute and how much the intrauterine environment contributes. This article was published in Schizophrenia Bulletin, but has not been sufficiently used in behavioral genetics research.

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Distinguishing the Capacity to Engage from the Capacity for Exchanging Affective Signals In discussing the different stages of development, it’s important to emphasize the difference in the level of affective transformation involved in patterns of simple engagement and relating versus reciprocal affective signaling. Many children with autistic spectrum disorder are capable of deeply engaging and forming patterns of warmth, trust, and dependency with a great deal of pleasure and joy. Some of these children will have varying degrees of difficulty, however, in developing ongoing, reciprocal, affective interchanges. Even if they are warmly and deeply engaged, it’s especially difficult for some children to develop a continuous flow of reciprocal, affective interactions.

There are many reasons for this difficulty, including biologically based processing difficulties involving motor planning, visual-spatial processing, auditory processing, or sensory modulation. Motor planning problems, for example, make it hard for the child to sequence and, therefore, engage in a multi-step, affective interactions.

Visual-spatial processing difficulties make it hard for the child to construct larger spatial patterns and, therefore, picture and negotiate a multi-step, affective sequence leading to a goal. Sensory reactivity difficulties will also make it hard for children to participate in long chains of reciprocal, affective interactions. They become overwhelmed with catastrophic affects, with short bursts of intense reactions rather than modulated, long chains of interaction.

The distinction between the ability to engage and the ability to engage in long chains of affective, reciprocal interactions is especially important for children with autistic spectrum disorders. We hypothesized that children with autistic spectrum disorders have a biologically based deficit in the capacity to connect affect to motor planning and sequencing and, therefore, are unable to enter into long chains of reciprocal, affective interaction. They also often have motor planning, visual-spatial, language processing, and sensory reactivity problems further intensifying this basic difficulty.

Yet, many children with autistic spectrum disorders have, or are capable of relatively quickly forming, patterns of engagement that involve a few circles of back-andforth affective interchange. They are capable of engaging with pleasure, warmth, and joy. They’re, therefore, capable of the earlier levels of affect transformation, involving basic engagement, even though they have difficulty with forming reciprocal affective interchanges. The basic capacity to love, experience intimacy and deep dependency is relatively stronger than generally acknowledged. It is the capacity for reciprocal, affective gesturing (i.e., the ability to negotiate within a loving relationship) that’s more problematic.

Many of the children we’ve worked with start off with the capacity for deep pleasure. They enjoy cuddling, being held, and show joyful smiles when their caregivers engage them in a warm pattern of relating. Other children appear to be more avoidant, self-absorbed, or affectively constricted in terms of showing joy and pleasure. Often these children can be helped to enjoy fundamental relating in a deep and satisfying manner, once we figure out their sensory processing and motor profiles.

For example, some of the children are very sensory over reactive and, therefore,

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uncomfortable with closeness involving touch or high- or low-pitched sounds. When the sensory environment is tailored to their unique profiles, these children begin evidencing enormous pleasure in relating. Children who have difficulty with motor planning become more deeply engaged when their caregivers learn how to position themselves in a way that makes the motor planning challenge simpler. In other words, the child who only has to reach out and hug or is helped to be in pleasurable sensory contact so he can feel where his caregiver is, finds it much easier to reach his goal of closeness with mother and father than the child who has to sustain focus and interest through four or five independent actions in order to reach mother or father.

In our review of 200 cases (Greenspan & Wieder, 1997) of children who received a comprehensive, intensive program of intervention, we found that the first gain the vast majority of children made was in the capacity to engage with warmth and pleasure. The capacity for engaging with warmth and pleasure occurred before gains in language skills, cognitive skills, or motor skills. Engaging appeared to be the aspect of functioning that was the most quickly responsive to the intervention efforts.

The observations that the capacity to engage responds most quickly and that many children diagnosed with autistic spectrum disorders can show a lot of joy and pleasure even before an intervention program has begun suggests a possible misconception about autistic disorders. Often, the capacities for affective reciprocity and affective engagement are believed to be part of the same process and children with autism are, therefore, viewed as less capable of love and intimacy than others. But, affective interactions are fundamentally different from the capacity to form a basic relationship characterized by pleasure and joy and, ultimately, a sense of trust and intimacy.

Many of the children we’ve been following for over five years (some for over 10 years) evidence patterns of closeness and warmth that are both joyful and deeper, in many respects, than typical children their age are able to show. We have observed that many evidence a great deal of warmth and closeness for their age group. It’s not surprising that these children can evidence intimacy because their parents have been spending extraordinary amounts of time with them in a warm and nourishing way that is sensitive to their processing profiles. Children without challenges whose parents are very available also form deep, satisfying patterns of closeness, warmth, and intimacy.

As indicated, historically, however, it has often been thought that children with autistic spectrum disorders have a biologically-based deficit in their ability for warmth and closeness (i.e., the capacity for a deep sense of love). It’s been thought that this is part of their difficulty with forming patterns of social interaction. It’s been believed that they experience the type “autistic aloneness” that Kanner described in his classic descriptions (Kanner, 1943). Even though many studies have refined Kanner’s original observations and different degrees of social relating have been described and incorporated into diagnostic criteria for children with autistic spectrum disorders, nonetheless, the perception persists (and continues to a partial degree even in the most recent diagnostic criteria) that children with autistic spectrum disorders

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are less able to engage with depth and warmth and with a deep, abiding sense of love than other children who don’t have these developmental challenges.

Our clinical observations would suggest that this common belief is simply incorrect. If we distinguish a child’s capacity for deep, joyful relating from the capacity for affective, reciprocal interchanges, it is possible to observe that many children with autistic spectrum disorders are capable of the full range of warmth, love, and closeness. This intimacy is relatively easy to observe in families who focus a great deal on promoting relaxed intimacy by observing spontaneous relating for long periods of time (hours, not minutes) and attending to all the subtle ways the children have of showing their intimacy. In our review of 200 cases, over half the children evidenced a deep rich capacity for intimacy and over 90% showed a continuing growth in this pattern (Greenspan & Wieder, 1997).

One may expectedly raise the question: why do many children with autistic spectrum disorders appear to spend so much time avoiding relationships or with constricted affect or in states of self-absorption? Why don’t many show a great deal of obvious pleasure and joy in relating to others? The answer to these two important questions is that children with autistic spectrum disorders who are capable of enormous warmth, joy, and deep relating can withdraw from relationships if the relationships are experienced as aversive or painful or simply not pleasurable. This often happens, not because the children are incapable experiencing joy or because the parents are not extraordinarily loving,but because caregivers are not sufficiently helped to figure out the unique sensory processing profile of the child so that they offer patterns of relating in a way that is pleasurable and deeply satisfying.

Some of the children have sensory processing patterns that are not so challenging and their caregivers find it relatively easy to approach and entice them into warm, nurturing patterns of relating. Other children, however, have complicated sensory patterns where caregivers require assistance. If this assistance is not forthcoming, children can pull away from the very relationships they might otherwise enjoy and seek. In addition, if the children are not helped to progress into reciprocal affective interactions, it’s hard for them to negotiate intimacy and, as indicated, they are more likely to experience intense, catastrophic affects.

This distinction between the child’s capacity to engage and the child’s capacity for affective reciprocal interchanges is being emphasized because it clarifies the misperception about children with autistic spectrum disorders mentioned above, that is, that this group of children somehow loves less deeply or less profoundly than other children. This misperception, as is well known, can easily become the basis for a selffulfilling prophecy if caregivers are discouraged from trying to find ways to draw their children into deeper patterns of intimacy. Simply not encouraging caregivers to explore this capacity can be a way of it becoming a prophecy come true.

There are, in fact, two misperceptions that need to be avoided. One is that the children who have a more challenging time learning to relate because of their biological differences, (such as sensitivities to sound or touch or language problems), are unable to learn to relate warmly through the availability of special interactions geared to their unique developmental profiles. The other misperception, equally worrisome,

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is that caregivers who construct special patterns of care that woo their child into relationships are somehow contributing to the causes of their children’s problems. What we’re saying here is that many children, especially those with autistic spectrum disorders, have biological differences that express themselves in the way the child processes sensations and organizes and plans responses. These biologically based processing differences can make the expectable milestones of learning to relate and communicate very challenging and, in some cases, possibly even impossible given current knowledge. The caregiving environment, however, while therefore not the cause of the child’s biological challenges can be a vital part of the process that helps the child master, to varying degrees, aspects of his or her biological challenges. We have found that the caregiving environment can be especially vital in helping children with autistic spectrum disorders learn to engage with greater degrees of warmth and intimacy if their caregiving overtures are tailored to the child’s developmental profile. Therefore, while not being the cause of the problem, the caregiving environment can be an important component of a comprehensive approach to intervention.

Perhaps the best way to conceptualize the challenges to forming relationships for children with autistic spectrum disorders is as follows. Due to their unique sensory processing profiles, the negotiation of a deep sense of intimacy is a complex and subtle process. The capacity appears to be there, but needs to be met with caregiving overtures that are sensitive to the child’s unique processing patterns. It is very easy for children with challenging processing profiles to respond negatively to even simple environmental challenges. Children without these processing challenges might easily have a more flexible capacity to engage others even under difficult conditions. The children with complex processing profiles are, therefore, extremely sensitive to the subtleties in their environments and can easily regress or form patterns of avoidance and self-absorption. At the same time, however, they can be drawn into wonderfully, deep, and satisfying patterns of closeness and intimacy. Parents are in a unique position because of their long-term relationship to the child to foster this intimacy and engage in long sequences of pleasurable affective interactions. Children’s capacity for intimacy, coupled with their sensitivities, in fact, suggest a need for nurturing, intimate care that is especially deep, flexible, and persistent.

Part III: The Role of Emotions in the Development of Intelligence and Social Skills If each of the transformations just described occurs, affects give rise to higher and higher levels of intelligence and emotional health. The emotional interactions described in the prior section, therefore, are not simply responsible for early social, cognitive, and language capacities, but for higher level intellectual and social capacities as well. A continuous flow of emotional interactions between children and caregivers is especially important for the development of the highest levels of human thinking involving self-reflection, making inferences, creating new problem-solving strategies, having empathy and insight, and regulating mood and

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behavior. This section explores the connection between affect and the capacity to regulate behaviors and construct the highest levels of intelligence and social interactions. In doing so, it shows why interference in the development of affective interactions, as seen in autism, is associated with a large range of cognitive, behavioral, and social deficits.

Our awareness of the importance of affect for higher level cognitive and social skills was heightened when we observed and talked with children with strong selfawareness and reflective thinking skills, and realized that most of them also showed positive self-esteem, demonstrated a capacity for moral judgment, were analytical in their reasoning, and did well in school and with their peers. We sought to understand what helped them become this way, and, therefore, spoke with them and with other children who had opposite personal characteristics. We learned that what we commonly label as intelligence, social skills and morality was based on the child’s ability to use his affects to think, which, in turn, is supported by the six types of emotional interactions, described in the prior section, that are negotiated during the early years of life.

For example, when we asked a group of eight-year-olds abstract questions, such as what they thought about justice or fairness, their comments were very revealing.

Some of the children responded with a rote listing of people who behaved “fairly,” such as a particular parent or teacher or television character. However, others gave far more reflective answers, along the lines of “Well, when I hit my brother after he hit me it was unfair for me to be punished, but when I hit him first it was fair for me to get a punishment. If I bump into him by accident, it’s not fair to be punished, but if I do it on purpose it is fair.”

Not surprisingly, when we looked at the two groups of children more closely, those who gave us the rote list tended to be the ones who were experiencing more problems in their relationships and in their schoolwork. The children who gave us more creative and reflective responses tended to do better in these social and intellectual areas.

We then took a second look at the more reflective responses and discovered that they had two components. This was true whether our test question focused on fairness or any other abstract quality, such as honesty, friendship or freedom. The first component was that the children’s responses always started off with a personal anecdote, an account of lived emotional experience. The second component was that the children put these experiences with abstract concepts into some sort of analytic framework and context.

When we later asked this same question of adolescents, they were able to list more categories (five different types of fairness, for example) and supplied an even more worldly-wise analytical framework. But in every instance, and at every age, two components were evident in the more sophisticated replies: lived emotional experiences and a framework, or context. The children who didn’t have a lot of lived emotional experiences—due to either nurturing or biological challenges that interfered with interaction, such as difficulties with language, for example—tended to be the ones who responded with concrete lists, rather than anecdotes. Interestingly, we

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found that the most effective way to teach such children analytic reasoning or thinking was by creating opportunities to have more “lived emotional experiences” and to reason about them. We observed that even children with severe developmental problems, including autistic patterns, could become more creative and reflective when they were exposed to more one-on-one interactions with their caregivers.

It thus became increasingly clear that certain types of emotional experiences seemed to be necessary for generating abstract ideas or thinking. This concept had been overlooked, because for many hundreds of years it has been a given in Western culture that emotions are separate from intelligence. We have commonly assumed that emotions are experienced as bodily reactions or passions that lead us to do irrational things; and more recently we have also viewed them as the cues that enable us to function socially. But in these conceptions of emotions, they are viewed as fundamentally different from intelligence, which has been considered to be the logical part of our minds that helps us be rational and make sense of the world.

Our new observations suggest that emotional interactions play a far more critical role in intellectual functioning. They can help us go beyond Howard Gardner’s important idea of separate, multiple intelligences (1983), or Antonio Damasio’s research on the brain which suggests that emotions are important for judgment but somehow separate from academic capacities or overall intelligence (1994). Even Jean Piaget, the pioneering cognitive psychologist, overlooked this vital connection.

Piaget observed that when an eight-month-old is accustomed to pulling a string that is attached to a bell and to hearing the bell ring in response, he will eventually stop pulling the string if it is detached from the bell. To Piaget, this sort of behavior revealed that the child is a causal thinker, because he pulls the string only if it leads to his hearing the sound of the ringing bell. Although Piaget’s observations were accurate, he did not realize that this was not the child’s first opportunity to learn about causality. A baby’s first lesson in causality occurs many months earlier, when he pulls on his mother’s or father’s heartstrings with a smile that brings a responsive smile of delight or some other joyful expression to his parent’s face. The child then applies that emotional lesson to the physical world of pulling strings, banging objects and the like.

At each succeeding stage of development, we have found that emotional interactions like a little baby’s smile leading to a hug enable the child to understand how the world works, and eventually to think, solve problems and master academic challenges. Emotions are actually the internal architects, conductors, or organizers of our minds. They tell us how and what to think, what to say and when to say it and what to do. We “know” things through our emotional interactions and then apply that knowledge to the cognitive world.

Consider how a young child first learns how to say “Hi!” as he greets other people.

A toddler doesn’t memorize lists of appropriate people to say hello to. He merely connects the greeting with a warm friendly feeling in his gut that leads him to reach out to other people’s welcoming faces with a verbalized “Hi!” If he looks at them and has a different emotional feeling inside, one of wariness, he’s more likely to turn his head or hide behind your legs.

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It is his feeling, or affect, that triggers the child’s decision over whether or not to greet a stranger. We encourage this kind of “discrimination” because we don’t want our children to say “Hi!” to a menacing stranger in a back alley. We want them to say hello to nice people like Grandma. If the child won’t say “Hi” to his grandmother, it’s because he’s not experiencing a warm feeling inside. If we can teach Grandma how to evoke that warm, fuzzy feeling inside her grandchild, she’ll eventually get a friendly “Hi!” back in response. Similarly, if a child learns to greet those people who make him feel warm inside, he will quickly say “Hi!” to a friendly teacher or to a new playmate. He carries his emotions inside him, helping him to generalize from known situations to new ones, as well as to discriminate, or decide when and what to say.

Not only thinking grows out of early emotional interactions; so does a moral sense of right and wrong. The ability to understand another person’s feelings and care about how he or she feels can only arise out of a series of nurturing interactions. We can only feel empathy if someone has been empathetic and caring with us or else we would not know what the feeling of empathy felt like. Even something as purely academic and cognitive as math and concepts of quantity is based on early emotional experiences. “A lot” to a three-year-old is more than he wants; “a little” is less than he expects. Later on, numbers can systematize this feel for quantity. Children with math blocks can be helped to become solid students by going back to the early emotional roots of learning about quantity. Similarly, concepts of time and space are learned by the emotional experiences of waiting for Mom, or of looking for her and finding her in another room.

Words also derive their meaning from emotional interactions, as our example of fairness illustrates. A word like “justice” acquires content and meaning with each new emotional experience of fairness and unfairness. Comprehension of a word like “apple” is based on numerous emotional experiences involved in eating one, throwing one and giving one to your teacher, in addition to its obvious physical characteristics of redness and roundness. As we showed earlier, even our use of grammar, which the noted linguist Noam Chomsky and others believe is largely innate and only needs some very general types of social stimulation to get going, is based in part on very specific early emotional interactions.

To provide the optimal quality and quantity of the types of emotional interactions requires, however, not simply caring loving adults, but caring loving adults who are consistent in the child’s life and who have time to spend with the child each day.

Ongoing empathetic caring is especially important for qualities of the human mind that can only be learned through ongoing experience—compassion through compassion, and intimacy by experiencing intimacy. These capacities are different from motor, language or cognitive skills. They require consistent care giving of one or a few stable caregivers who are there for years in the child’s life. For example, children can learn altruistic behaviors in an impersonal way by copying or learning rules (i.e., to do “the right thing”), but truly caring for another human being only comes through experiencing that feeling of being cared for oneself. It is a self-evident truth that to feel an emotion we have to experience that emotion in an ongoing relationship.

We can’t experience emotions that we have never had, and we can’t experience the

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consistency and intimacy of ongoing love unless we’ve have had that experience with someone in our lives. For some it may be a grandmother or an aunt, or it may even be a neighbor, but it must be there. There are no shortcuts to life’s most important experiences.

Therefore, family patterns that foster healthy relationships are essential for healthy emotional and intellectual growth. In one study we found that families with four or more risk factors interfering with relationships were 20 times more likely to have marginal IQ scores and behavior problems at age four. This pattern continued and was again documented when the children were 13 years old (Sameroff, Seifer, Barocas, Zax, & Greenspan, 1986; Sameroff, Seifer, Baldwin, & Baldwin, 1993).

Emotional Interactions and the Regulation of Behavior, Feelings, Moods, Problem-Solving, and Thinking The basic feature of caring, caregiver-infant relationships, back-and-forth affective interactions within which we read and respond to the baby’s signals and the baby reads and responds to our affective overtures, is responsible for a surprisingly large number of vital mental capacities.

For example, the child eyes the red rattle and parent holds it up and the child reaches for it, takes it, the parent holds his hand out and the child puts it back in the parents hand, there is a big smile, the parent smiles back, the child makes some sounds, the parent makes some sounds back. We have an interactive dialogue involving sounds and gestures and emotional expressions, such as big smiles, all happening in a rapid back-and-forth set of exchanges. As described earlier, this rapid back-and-forth set of exchanges (i.e., “opening and closing circles of communication” or “reciprocal affective interactions”) is the beginning of learning to think purposefully or causally, “I can make something happen.” It also teaches babies how to take initiative (you do something and it makes something happen, your smile gets a smile from mommy or daddy). The infant is beginning to have a sense of purpose and will and, very importantly, a sense of “self” (it’s “me” making something happen, “me” getting that smile or getting that little red rattle with reaching out “my” hand). The sense of self, will, purpose, assertiveness and the beginning of causal logical thinking all occur through long chains of reciprocal affective interactions.

But something else also occurs as a product of these back-and-forth interactions that has not been sufficiently described before. Through these reciprocal affective interactions the child learns to control or modulate his behavior and his feelings. We all want children who are well regulated or modulated, that is, who can be active and explorative some of the time, concentrate and be thoughtful and cautious other times, joyful yet other times. We all want children who can regulate their emotions in a way that is appropriate to the situation and also regulate their behavior in a way that is appropriate to the situation. We all admire adults who are able to do this. But how do we learn to control or regulate our behavior and moods?

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What is the difference between a child who can regulate their mood, emotions and behaviors and a child who can’t and where the slightest frustration feels catastrophic, as though the world were going to end, or where anger is enormous and explosive, or sadness seems like it will go on for ever and ever? What is the difference between these extreme and almost catastrophic emotional reactions and the ones that are finely regulated and responsive to the situation at hand? (Sometimes there is sadness, sometimes joy, sometimes even anger.)

The difference is in the degree to which the child learns and masters this important capacity for rapid back-and-forth exchanges of emotions and gestures through these reciprocal interactions.

When a child is capable of rapid back-and-forth interactions with his caregiver, he is able to negotiate, in a sense, how he feels. If he is annoyed, he can make a look of annoyance or a sound or hand gesture. Mother may come back with a gesture indicating “I understand” or “OK, I’ll get the food more quickly,” or indicating “Can’t you wait just one more minute?” Whatever the response is, if it is responsive to his signal he is getting some immediate feedback that can modulate his response. The anger may be modulated by the notion that mother is going to do something, even if she can’t do it immediately. Just the sound of her voice signals to him that she is getting that milk bottle ready and it’s coming real soon. Or his pushing the bottle away with an angry glance at her and her putting her hand out to take it from him is another way he knows that his anger is being responded to. Similarly, when his big smile gets a smile back he knows his joy is being responded to. He gets a sense that he can regulate his emotions through regulating the responses he gets from environments. He gets the quick sense that he and his caregivers are in this pattern where they are regulating one another, where the back and forth is a finelytuned nuance system involving lots of feedback.

We now have a fine-tuned system rather than a global or extreme one. The child doesn’t have to have an extreme tantrum to register his annoyance, he can do it with just a little glance and a little annoyed look. Even if mother doesn’t agree with him or can’t bring that food right away, nonetheless she is signaling something back which gives him something to chew on while he is deciding whether to escalate up to an even more annoyed response if she doesn’t move fast enough. This is a system of steps. Even if he does escalate up to a real tantrum, he is not going from 0 to 60 in one second. More often than not, however, his mood and behavior will be regulated as a part of this back-and-forth interaction. All the different feelings, from joy and happiness to sadness to anger to assertiveness become a part of fine-tuned regulated interactions where a subtle reciprocal pattern comes into play rather than an all-or-nothing one.

Why would we have an all or nothing pattern if we didn’t have this chain of backand-forth interactions? What happens when a child doesn’t have access to sufficient reciprocal interactions? Perhaps he can’t gesture or signal well or has an unresponsive parent who is not signaling back or has a parent who is too intrusive and anxious and can’t respond to his signals or is too self-absorbed or depressed to respond.

For any one of these reasons, we may see a compromise in this fine-tuned interactive

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system involving the regulation of mood, feelings and behaviors and instead see extreme or catastrophic type reactions.

When the child who is not learning how to engage in finely-tuned back-andforth interactions where there is lots of feedback has an emotion, he doesn’t implicitly expect it to lead to an immediate response from his environment. The emotion consequently exists somewhat in isolation. Without the modulating influence of a reciprocal response, the feeling may simply get more intense. The child is left to using more global responses of anger or rage, fear or avoidance, or withdrawal or self-absorption. Very young infants are more prone to these extreme reactions in the early months of life. When they cry, they cry very hard and loud because they are very frustrated until we help settle them down. When they cry with anger we can feel their rage in their vocal tone until we soothe them. These extreme emotional reactions have certain similarities with what has been described as flight/fight reactions, global reactions of the human nervous system in comparison to finely-nuanced back-and-forth interactions with finely regulated emotions and behaviors. Children are not limited to flight/fight reactions. They can have a variety of global reactions including avoidance, withdrawal, self-absorption, and fear, rage, or impulsivity.

The child graduates from global responses in the early months of life to nuanced fine-tuned reciprocal interaction patterns (from about 3 months to 9 or 10 months).

By 9 or 10 months these finely-tuned reciprocal patterns become well established and then become more complex, goal-directed, and problem-solving between 10 and 24 months. By the time the child is talking up a storm at age 2 and 21/2, he already has the capacity to be involved in long chains of back and forth interactions (back-and-forth reciprocal interactions) involving different emotions and behaviors.

If all has gone well, they are already part of a nuanced, finely-tuned system where mother’s serious glance signals limits to the child; where her joyful expression signals permission for the child to be more expansive and try new things; where the child’s annoyance signals the parent to have a quizzical look of “what can I do to help you out?” and so forth. These series of actions and interactions involving emotions, mood and behavior help the child to develop a finely-tuned, subtly-nuanced regulatory capacity, rather than to retain and exaggerate early global catastrophic reactions.

What we have been describing is especially important when we see children who are operating in a catastrophic or extreme manner, that is, extreme meltdowns or tantrums, or getting carried away with excitement, anger, sadness, or even depression. Often, these extreme reactions will mean that not only are things happening at the moment to cause anger or despair, but that the reactions are out of proportion to the events of the moment, suggesting that some parts of the child’s feelings, mood and behavior didn’t have a chance to become regulated through long chains of backand-forth reciprocal interactions.

For most families it’s easier to get involved in back-and-forth negotiations around certain behaviors and feelings than others. Some children and caregivers develop long chains of regulated reciprocal interactions around assertiveness and anger quite

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well, but don’t do it as well around sadness or sense of loss. Other are just the reverse and are better around sadness and loss and issues of intimacy and warmth, but are very anxious and therefore don’t interact very much or don’t interact in a finelytuned nuanced way around assertiveness or anger. In this context, it is not surprising that as children become older they have different modulation capacities for different feelings. As adults many of us are better with one set of feelings than another set of feelings in the way we regulate our moods, have a sense of being able to negotiate feelings with others and understand them in ourselves.

As children learn to regulate their behavior and feelings as part of long chains of back-and-forth interactions they can use this skill to get to the next level where they can problem-solve with the feelings and try to change what’s happening in their environment. If it is unpleasant, they can do things to change the situation and the feeling. If it is a pleasant feeling, they can change their environment to bring on more of those events. By 18 to 20 months, toddlers can already try to lessen those conditions that make them feel sad or angry and increase those conditions that make them feel happy. It could be the way they arrange the toys, the way they flirt with and seek out a caregiver. Toddlers are already becoming active social problemsolvers using finely regulated emotional interactions, now in a larger problemsolving context.

Children progress further up to age 2 or 21/2, and, as indicated earlier, can form images in their mind (symbols or ideas) and label the feelings that have come under fine regulation. They understand these regulated feelings more fully than unregulated ones. When a feeling is part of a regulated interaction with someone else, one understands its context and gains perspective on it. We see this in the pretend play of well-regulated children. They have many long chains of back-andforth interactions with many details in their dramas as they create scenes where there are subtle interactions around anger, happiness or sadness. Children who are more extreme in their reactions in contrast tend to evidence more global pretend play patterns. The characters get excited and bang the floor, simply crash cars, or just go to sleep. Their pretend play often reflects the degree to which they can regulate and modulate their feelings. For children capable of regulated reciprocal interactions at the level of using ideas, they are able to label feelings and begin to ponder them.

At the next level (building connections between ideas), as discussed earlier, children can begin reasoning about their feelings, figuring out why they are happy or sad or joyful. This occurs between ages 3 and 4. As they become older, they can further reflect on these feelings and understand them in a larger context of their peer relationships. They can understand more subtlety in the gray area of feelings, in other words, how angry, happy, or sad they feel. As a child becomes older this capacity for reflective thinking with feelings becomes stronger and stronger.

These steps of labeling and reflecting on feelings depends on that important earlier step of experiencing these feelings and behaviors as part of a back-and-forth signaling system. Without that step, the feelings stay in a catastrophic global mode (the all-or-nothing mode where I am extremely angry or excited). The continuation

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of a global, unmodulated quality interferes with the progression to reflective thinking because it’s hard to symbolize unmodulated extreme feelings. There is too much pressure to put the feelings into action rather than into ideas and words. The feelings are so strong in the unmodulated form that they create a reality about them, a sense of urgency and immediacy that is stronger than the idea that could represent or symbolize them. In other words, when the feelings are extreme, the tendency is to discharge the feeling, put it into action or just shut down and avoid it entirely rather than label and think about it. The child who is in the middle of a rage may be able to say, “I’m angry,” but he is still biting, yelling, screaming and hitting. Even if he can label a little bit, the labeling isn’t serving the purpose of using the idea or reflecting on it.

In contrast, the child who says, “I’m angry. I need my milk now, please” is using the idea to convey the feeling. He is not being dominated by the feeling but is trying to communicate something that will alter the feeling.

Perhaps most importantly, the capacity for a continuous flow of back-and-forth, affective signaling is essential for establishing a sense of reality, reality testing (the ability to distinguish fantasy from reality), the capacity for organized thought (rather than fragmented thinking), and an organized sense of “self.” Children who do not engage in a continuous flow of affective gesturing live in a world of islands of back-and-forth episodic reality contacts with the world. Their sense of reality, as defined by the continuous reciprocal exchange of information with another (to balance and define one’s inner life) is piecemeal. As a result, their thinking, sense of reality, reality testing, and sense of self is fragmented. Not surprisingly, many children with special needs who make outstanding language and cognitive gains have difficulty with these higher-level capacities involving a stable sense of “self” and “reality,” because their programs don’t sufficiently emphasize a continuous flow of affective gesturing as a foundation for higher level capacities. In contrast, the continuous flow of affective gesturing, when coupled with emerging symbolic interaction, creates the nexus for organized, reality-based thinking, a stable sense of self, and the capacity to learn still higher level capacities for judgement, self reflection, and insight.

It should also be pointed out that extreme anxiety tends to disrupt the child’s capacity for long reciprocal chains of subtle and differentiated affect cueing.

Individuals, when they’re anxious, typically stiffen their facial muscles and become more global (i.e., less differentiated) in their affect expressiveness, even though their anxiety or fear may be quite observable in their facial features. The result of this anxiety-based interruption in affect cueing is a tendency toward fragmented (rather than integrated) thinking. Fragmented thinking, in turn, lends itself to distortions, exaggerations and polarizations, and further intensifies fear and anxiety. This pattern leads to a cycle of increasing dysfunction.

Children with sensory processing difficulties, including visual-spatial processing, auditory processing, or motor planning, or sensory modulation challenges are especially prone to extreme anxiety because it’s more difficult for them to regulate, comprehend, and operate on their social and physical worlds. It is, therefore, particularly easy for children with special needs to become involved in these cycles of

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anxiety and fragmented thinking. As indicated, the fragmented thinking then leads to more polarized perceptions and often catastrophic emotional states (which operate at an all-or-nothing level, rather than a finely regulated, modulated one) and the intensification of the cycle of dysfunction.

Recognizing this pattern has important implications for intervention. The most helpful intervention strategy is to calm the intense anxiety and fear through reestablishing affective or emotional contact with the child in a highly soothing manner.

Then it is vital to begin the process of reciprocal, affective exchanges with an especially soothing manner and tone. One is simultaneously calming the child and bringing the child back into reciprocal affective interchanges, which will enable him to organize his thinking, become more reality based, and exercise more finely tuned judgment (rather than operate under the agencies of catastrophic affects in highly polarized, distorted thinking patterns). The long term goal is to facilitate the child’s ability to better and better re-engage on his own so that he can become a better agent at initiating long chains of soothing, affective interchanges.

A child who is operating under fine-tuned regulated affective interactions will be in solid position to use logical reality-based and integrated thinking to gradually increase his intellectual and social capacities. On the other hand, a child operating under states of intense anxiety with polarized and catastrophic patterns will be compromised in his or her intellectual and social progress.

In addition to dealing with anxiety, the pattern of reciprocal affective interaction can be a helpful therapeutic tool for working with problems with unstable or labile mood, attention and activity problems, and impulsivity. The individual with labile moods has difficulty sustaining a mutually soothing, calm, reciprocal affective pattern. If the reciprocal partner (e.g., therapist, caregiver) can down-regulate (i.e., a soothing tone of voice while maintaining a continuous flow of affective interchanges), as the patient or child is revving up, over time a new capacity for more continuous, soothing reciprocal interactions may be learned (often for the first time). As the patient is helped to gradually experience emotions or thoughts associated with mood shifts, these reciprocal patterns are especially helpful. Not infrequently, the original parental response to what may have been a biologically based tendency was to reciprocate the child’s revving up with counter agitation or withdrawal, neither of which would provide what the child needed.

For the inattentive, active child, the reciprocal pattern may need to emphasize longer and longer chains of reciprocal interaction (to maintain attention), coupled with modulation patterns where the therapist or caregiver changes the rhythm of interaction (from fast to slow, slow to fast) and changes the intensity of response (such as loud to soft sounds and vice versa). In a sense, one catches the other person into longer and longer sequences with greater and greater modulation.

For the impulsive individual, the goal would be a combination of the intervention described for the moody and inattentive, active individuals, with increased soothing, longer sequences, and more modulation. This pattern would be implanted as the individual was helped to gradually experience the emotion that precipitated the impulsive behavior.

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Affective Reciprocity, Evolution, and Intelligence The capacity for a continuous flow of increasingly differentiated affective expressions may be a universal process in the development of intelligent behavior in different members of the animal kingdom. This hypothesis would suggest that the greater the capacity of the animal (or group of animals), including humans, to evidence differentiated, affective expressions and use them in gestural interactions to communicate and problem solve, the greater the animal’s intelligence. In addition, the greater the capacity for a continuous flow of differentiated affective interaction, the greater the animal’s ability to form complex social networks. Furthermore, the greater the social networks, the greater the ability to deal with basic needs and, therefore, the greater the ability to employ mental resources for the development of higher levels of intelligent behavior.

The capacity for affective reciprocity may, therefore, have been an important step in evolution as well as in human development. In human development, it is a critical step that enables exploration of the world and the regulation of behavior, mood, and eventually, thought. In evolution, the capacity for affective reciprocal interactions may have played an important role in the development of complex social organizations and culture. Reciprocal affective interactions are necessary for social groups (i.e., a method for quick and efficient communication of intents without resorting to extreme behaviors). Aggression, dependency, sexuality, and the like could be negotiated through affective cues. For example, an aggressive gesture could lead the “other” to gesture submission without a violent confrontation, as is often seen among mammals. Many such interchanges equal complex negotiations, for example, the capacity to communicate and negotiate favors. Social organizations which, in turn, allow for more efficient self-and group protection, food, housing, and weaponry production. Freedom from meeting survival needs during all of the waking time, in turn, would permit time for other endeavors, including more complex social interactions, pattern recognition under non-catastrophic survival emotions, and exploration of the next step beyond complex patterns, i.e., symbol formation.

Affective Reciprocity and Symbol Formation: Perception Without Action This section will suggest a hypothesis about how symbol formation arose from the capacity for affective reciprocity. The ability for affective reciprocity may be both a critical step in the evolution and the human development of thought and symbol formation. As with many human capacities, evolution may repeat itself in the adaptive development of each infant and child. As indicated earlier, affective reciprocity is associated with regulating emotions and behavior and, thereby, mastering catastrophic behavioral discharge, feelings, and interactions. The regulation of behavior through affective signaling enables the individual to have perceptions

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without taking action. What is perception without action? Perception without action is imagery. When the capacity for imagery is combined with the intentions (and their related affects) that are involved in reciprocal affective interactions, symbolic meaning develops.

Furthermore, while catastrophic survival emotions would keep one pretty well tied to concrete behaviors, modulated reciprocal affective states, in contrast, would promote higher-level mental (less concrete) capacities. It would promote associative learning and allow time for associative mental processes because affects would be motivating feedback-oriented interactions and learning from the environment and others, rather than immediate survival-oriented action. Symbolic art characterizing real events may have been an early form of symbolic expression. In other words, the capacity for affective reciprocity would favor social organizations, pattern recognition, symbol formation, and other higher-level mental abilities—all of which, in turn, would have evolutionary advantage.

In addition, the long interactive patterns that result from reciprocal interchanges create the capacity for expectations (i.e., pattern recognition). It is only a small step, then, to being able to abstract these “expected” patterns into a symbolic form. Both the taming of the extreme catastrophic emotions and the formation of complex patterns of expectations are important contributors to symbol formation.

Therefore, in both each child’s development and in the evolutionary patterns that have preceded us, it is likely that the capacity for affective reciprocity enables the regulation of behavior and mood (i.e., the mastery of catastrophic behavior discharge emotions), and promotes social signaling, more efficient social organizations (which frees individuals from survival necessities and promotes economic and cultural growth), and the capacity for imagery and symbolic functioning. Much of this occurs because affective reciprocity frees perception from action.

Variation in Affective Reciprocity and Symbol Formation These high-level mental capacities are far from universal, even among human beings. Affective reciprocity and the resultant capacity for symbolic functioning, as well as derivative social, emotional, and intellectual capacities, vary in relationship to experience. These capacities are not completely relative, however,(as one might expect from the perspective of cultural relativism). In spite of variation, there are two sources of similarity among peoples. One relates to the human perceptual apparatus.

There are certain commonalties among most people in terms of, for example, frequencies of sound that will register and patterns of color or light that can be perceived. Less obvious, there are also certain functional developmental capacities (in terms of their basic structure) that are also shared by most people. These include, in addition to the capacity for affective reciprocity discussed earlier, the capacities for shared attention, relating to others, engaging in purposeful or willful interactions, negotiating complex reciprocal affective problem-solving interactions, creating ideas, building bridges between ideas, and progressing to some degree of higher-level

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abstract and reflective thinking. It is interesting to look at how different cultures provide their own form of opportunities for babies to engage in experiences leading to these basic functional developmental structures and to see if some cultures do not provide such opportunities. In fact, the field of cultural anthropology may wish to consider these structural capacities together with ones already being studied.

The common perceptual features (e.g., sound registration) are based largely on a relatively similar biology. The common functional developmental capacities for relating, communicating, and thinking are based on common child-rearing and family practices and include experiences such as nurturing human caregiving to promote relating and sensitive affective signal reading and opportunities for interaction to promote purposeful, willful interactions and affective reciprocity. To the degree most infants have access to nurturing interactive caregivers, these structural personality characteristics will be at least somewhat similar among people.

At the same time, however, there will be variations on these capacities based on both biology and experience Some babies, for example, have a narrower range of functional sound recognition and are quite sensitive or reactive to high frequency sounds. Many children will not have access to nurturing caregivers and, therefore, will not learn to engage with others and participate in a continuous flow of affective interactions and, therefore, will not master the capacity for affective reciprocity. Consequently, their capacities for symbolic functioning will also be quite constricted.

At present, however, only small numbers of children evidence these more extreme biological or psychological patterns. What will happen if most children do not have opportunities to learn how to engage with caregivers and master the capacity for affective reciprocity due to changing child rearing, such as poor quality day care? What will happen if, due to toxic substances such as lead or dioxins, most children evidence extreme difficulties in the way their central nervous systems function? In such circumstances, the common ground that supports shared human capacities will decrease. This decrease will not lead simply to more human diversity, however. It will erode a shared sense of what constitutes reality, rational thought, or moral behavior. The glue that holds many societies together would be in jeopardy.

In addition to these relatively stable features of human functioning (for the moment at least), there are other features of human functioning that clearly vary from person to person. Within each of the functional developmental capacities, such as relating, affective reciprocity, and using symbols, each individual, based on their unique experiences, will cast their own signature. One individual will interact more around assertiveness, another around dependency, another around sexuality.

Unique cultural and family experiences will contribute to these personal signatures.

While sharing the capacity for thoughts and feelings, each individual’s specific thoughts and feeling will, therefore, be uniquely personal and related to their personal history.

Importantly, however, the capacity to organize uniquely personal experience at a gestural, affective reciprocal or symbolic level (i.e., form a symbolic sense of self)

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depends on the basic functional developmental capacities described above. As indicated earlier, perhaps the most critical of these functional developmental capacities for human development and for evolution is the capacity for long chains of affective reciprocity. It should not be surprising, therefore, that working with affective reciprocity should be at the center of clinical work with children with autistic spectrum disorders.

From Affective Reciprocity to the Development of Ego Signal Functions Another important dimension of reciprocal, affective interactions is that they lead to the capacity for an individual to use affect as a signal, which fosters anticipation and consideration of alternatives rather than direct discharge, shut-down, or withdrawal. The regulation made possible by back-and-forth affective exchanges, as indicated, leads to symbolization and the symbolization of affect makes possible the use of affect as a signal.

Consider the case of a latency-aged child who tended to be either agitated or depressed. The goals of his psychotherapy were to help him progress to higher levels in his functional emotional capacities (i.e., ego development). Specifically, one of the goals was to enable him to engage in longer chains of regulated, reciprocal affective exchanges. During longer and longer exchanges, the therapist would help Andy better regulate his affective and behavioral expressions through critical preverbal, as well as verbal responses. For example, when Andy would begin to evidence more agitation in his voice and body movements, the therapist would deliberately move towards a more soothing, comforting tone to attempt to downregulate the intensity of affect. When Andy would become more apathetic and selfabsorbed, the therapist would deliberately move towards a more energized rhythm of preverbal and verbal exchange (e.g., more animated facial expressions and faster tempo) to up-regulate. At the same time that the therapist was working at the preverbal level, he would also, periodically, explore how Andy felt during these shifts of affective rhythm and intensity. During these times, he was attempting to help Andy symbolize and reflect on the subtle feeling states Andy was experiencing when either agitated or apathetic.

Over a period of six months, Andy was able to make progress towards both of these goals. He gradually responded to the therapist’s soothing, comforting tone of voice and interactive rhythm by becoming more regulated (less agitated) when talking, for example, about his father being unfair or kids at school picking on him. He was also able to begin verbalizing more abstracted feeling states, shifting from somatic descriptions and descriptions of actions he was going to carry out to true descriptions and reflections on inner feelings. For example, instead of talking about his exploding insides or how he was going to punch so-and-so, he began describing “Feeling like my insides were shouting...like I was so mad.”

Interestingly, as Andy was able to symbolize affect, he began being able to use affect as a signal (i.e., to both unconsciously and consciously anticipate next steps).

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For example, he began to become aware of feeling angry and then could consider alternate actions, when his brother came into his room uninvited. It’s important to note that his capacity to use affect as a signal was based on his first learning to regulate reciprocal affective exchanges and then describe his affective states symbolically. Both steps appear to be important. Without the regulation, affective states tend to be intense and, therefore, are often experienced in an overwhelming or catastrophic manner, and there is a tendency toward discharge or somatization or interpersonal withdrawal. The regulation of the affective interchanges enables shifts towards symbolization (i.e., greater awareness and description of subtle affective states) and, in turn, the symbolization enables the affects to also serve as intrapsychic signals.

Implications for Attention and Processing Capacities The importance of reciprocal emotional interactions also becomes central when we are trying to help children who are having challenges, such as fears, anxieties, or impulse control problems. These and other challenges often involve some degree of unregulated feelings. Therefore, in addition to other therapeutic strategies determined by the child’s and family’s unique developmental profile, creating opportunities for long empathetic nurturing interactions around the child’s different feelings can often go a long way to helping a child learn to regulate feelings and behavior (e.g., parents get down on the floor, follow their child’s lead and tune into the child at the level of gestures and, if the child is 2 or older, through pretend play as well).

Interestingly, back-and-forth, regulated, affective interactions also help the child develop many of their most important information processing abilities, such as their capacity for attention, planning and sequencing actions, understanding space (visualspatial thinking), and using words and language meaningfully.

Consider language. Words have to have meanings and meanings are conveyed through the emotional context within which a word is used. A word that is used as part of a back-and-forth pattern of negotiation will be a word with many emotional subtleties to it. The child who learns the word “fair” or “unfair,” for example, can learn this in an all-or-nothing way, this is simply “fair” or “unfair,” or can have subtle gradations of what’s a little fair, very fair, extremely fair, or not fair, somewhat not fair, etc. These subtle gradations will only be learned as part of interactive relationships that involve a lot negotiation.

More illusive, though, is how these reciprocal interactions help a child learn to pay attention and plan and sequence actions (e.g., executive functions). Many have wondered why we are seeing more children with attention and motor planning problems. One contribution might be fewer opportunities for long chains of reciprocal problem-solving interaction in child/caregiver relationships. Consider how this process may work. In order for a child to carry out a two-step and then a three-step and then a five-step plan, it is very helpful to have all the elements of that plan invested with lots of emotion.

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The ability to carry out a number of steps in a row, that is, to plan and sequence actions, begins with simple reciprocal interactions. The emotional recognition that one’s actions can have an impact on someone else is the foundation for sequencing (i.e., the ability to carry out many steps in a row where each one is related to the prior one). This is exactly what reciprocal interactions are. Smiles lead to smiles, frowns to frowns, sounds to sounds, movement to movement. The harder it is for the child to continue a long chain of interaction, the more important it is to practice long, regulated sequences of interactions.

In order to practice affectively, however, one needs to put more and more emotion into the interactions. The more vibrant and interesting and emotionally meaningful the interaction is to the child, the longer the sequence the child will mobilize.

This doesn’t mean loud or extreme emotions, it means subtlety and expression (soft or gentle, exciting or captivating, depending on the moment and the child). In essence, some degree of emotion or intent is what carries the child’s ability to sequence. Therefore, the emotional interest that the adult must bring to the situation will have to be greater when the task is harder.

As a child graduates from simple reciprocal interactions to more problem-solving interactions, the ability to plan and sequence also improves because the child is now sequencing longer chains of reciprocal interactions. At the next level where ideas regulate behavior, a child can map out sequences with visual images and verbal ideas. And as logical thinking begins to dominate, the child can plan strategies for executing actions and consider a number of alternatives. The entire system of planning and executing problem-solving strategies, though, depends on the child being able to link many pieces of behavior together into a long reciprocal pattern.

The degree to which these patterns can be elaborated in many different domains of life increases the degree to which the child can plan and execute actions in these different domains. For example, some children are very good at social negotiations, but not very good at fixing a toy, figuring out how to find a hidden object, or self care in the bathroom.

The domains that are more difficult for the child require more involvement with long chains of reciprocal emotional interactions. In essence, one needs to build up the basic patterns in areas that are hard for the child. For example, a child who is very engaged, warm, and is very good at social sequencing, negotiation, and problemsolving has a hard time with visual-spatial sequencing (he has never been able to conceptualize how space is laid out). For this child, emotional interactions using space, such as hide-and-go-seek games, treasure hunts, other search games and like, would strengthen this basic capacity. This same principle applies to children who have trouble understanding the spatial dimensions of their own bodies, integrating their left and right sides, for example. Here, too, reciprocal interactions involving the human body, games such as “touch my nose and I’ll touch your nose” would facilitate body-oriented visual-spatial problem-solving.

Many clinicians who work with exercises such as left hand to right shoulder or different kinds of games involving different types of crawling and walking often believe that all that is going on is exercising the body and processing capacities. The

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gifted clinician working with the child, however, is often working in a highly reciprocal manner developing reciprocal sequences in the context of visual-spatial thinking, or other processing abilities. It is the chains of regulated reciprocal interaction in that particular domain that creates the foundation for improved cognitive abilities in that domain.

It would be useful to study caregiving patterns associated with different capacities for attention and sequencing. The hypothesis would be that less reciprocal caregivers are associated with greater attentional and sequencing problems in their children.

Furthermore, the optimal attention and sequencing capacity would be associated with caregivers capable of long reciprocal chains in many functional areas (e.g., motor, language, visual-spatial, social) with a tendency to support the child’s gradually increasing assertiveness. The caregiver would begin with a continuous response pattern, but gradually shift to a more intermittent pattern as the child became more self sufficient. For example, the caregiver would reciprocate each gesture initially, but as the child became able to sustain his or her initiative, reciprocate relatively intermittently but sufficiently to help sustain the pattern. If the child were talking, one would gradually shift to letting the child say more and more before commenting or asking a question.

Affective Reciprocity, Motor Planning, Rhythmicity, and the Development of Language Long chains of reciprocal interaction support the toddler’s capacity for engaging in planning and sequencing actions (i.e., long problem-solving sequences involving social interaction and mastery of his physical environment). These sequences of long problem-solving interactions, in turn, support many critical aspects of language development. As discussed earlier, preverbal gestural (i.e., problem-solving actions), social, and problem-solving interactions create the context for meaning of verbal symbols. Without this basic level of knowing through doing, words, when they became possible, would have no experiences to draw on to create meanings. In other words, the child knows what love is through his hugs, cuddles, and flirtatious glances. The word summarizes the concept or meaning he has been gradually forming. Similarly, words for “open,” “up,” or “door,” all have their experiential contexts.

Reciprocal affective interactions also influence the basic grammar and semantic aspects of language. We have found, for example, that children not capable of reciprocal affective interactions (e.g., children with autistic spectrum disorders), tend to use words ungrammatically, repeating nouns or verbs perseveratively, for example.

Interestingly, if we try to simply correct their grammar, it doesn’t work very well.

They make progress, however, when we first help them engage in reciprocal affective gesturing and use their affect and gesturing purposefully (e.g., we get stuck behind the door they are opening and closing and they eventually learn to push us

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away). At that point, they begin to align their verbs and nouns in a grammatically correct manner—“Daddy, go!” or “Leave me alone.” We observe the same patterns in children from deprived backgrounds, such as orphanages. Whether the insults are environmental or biological, it appears that a prerequisite for correct use of grammar is the purposeful use of affects in interactive relationships. This fact may have been missed by linguists who suggested grammar was largely innate and simply turned on or off by global features of the environment because it’s easy to take reciprocal affect cueing and other preverbal aspects of communication for granted. They occur so regularly. It’s only when we find circumstances where they don’t occur that we can see their true impact.

Similar to grammar, the meaning of words, both the semantic and pragmatic aspects are also imbedded in the earlier reality of gestural interactions, which are used to explore and know the world. The literal meaning of a word or concept, for example, the concept of a door or a table or a mommy or a daddy is first known through gestural interactions with it. The capacity to form the word is then linked to what is already partially known. The known entity takes on additional meaning through context and further emotional experience with it. Therefore, both the literal and the relative meaning of words and concepts emerge from reciprocal affective interactions which provide the foundations and context for meanings.

The capacity for long chains of reciprocity and the basic capacity to plan and sequence actions may also support the ability to sequence words or ideas and eventually concepts in a speech, essay, or debate, or simply a long conversation. Sequencing ideas relates both to this basic ability to abstract meaning from earlier preverbal experiences and then sequence them meaningfully.

Also, as discussed earlier, the very capacity for forming symbols derives from the toddler’s ability to negotiate through reciprocal interactions involving long problemsolving sequences. An image not tied to the need for direct discharge can become a thought (i.e., a symbol). In addition, long chains of reciprocal communication become pleasurable in their own right because they foster greater co-regulation of relationships and provide safe and secure ways to express and negotiate feelings and needs and therefore become an end in their own (rather than a means to some other gratification).

There are, however, other subtle contributions of affective reciprocity and motor planning and sequencing to language development. Affective reciprocity and planning and sequencing capacities occur in rhythmic patterns. Vocal and motor interactions between caregiver and toddler exist in various rhythms, rapid exchanges of vocalizations, slow exchanges, simple rhythms of monotones, novel rhythms of animated dialogues, and so forth. We all get bored and tune out with a slow, even, rhythmic monotone and perk up and listen better with a more rapid, novel, changing rhythm, particularly when these are in tune with the meanings of the words being expressed (e.g., speeding up or slowing down to emphasize an emotional point). Some people, however, are better at listening, even if it’s a slow monotone. Similarly, as infants and toddlers are identifying and using vocal patterns, there is an intimate relationship between what can be perceived (i.e., processed

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auditorially) and what can be articulated (a child hears sound patterns and tries to imitate them). A toddler or child who has a hard time planning and sequencing actions and therefore with reciprocal affect cueing, may have a relatively more difficult time engaging in and recognizing the rhythmic patterns underlying aspects of auditory perception and expressive language.

In many respects, the capacity of rhythmic interactive patterns, which is a component of motor planning and affective reciprocity, is a vital dimension of language. There has been recent research on the temporal aspects of auditory processing and language, including intervention strategies developed based on temporal dimensions, for example, slowing down the presentation of sound sequences (Tallal, et al., 1996). Another vital component of the temporal system, however, is the rhythmicity of sound sequences. There is likely very different thresholds of sound sequencing for perceiving patterns. Too slow a presentation, for example, may make pattern recognition more difficult. Research in progress on the Interactive Metronome (Shaffer, Jacokes, Cassily, & Greenspan, 2001) is revealing an optimal rhythmic range below which sound patterns are very difficult to perceive. This research is also identifying differences in the degree to which individuals with different processing challenges and diagnoses can perceive these patterns.

Reciprocal gesturing and motor planning and sequencing, particularly its rhythmic dimensions, may also be especially important for oral-motor sequencing capacities and overcoming oral-motor dysphoria, as well as stuttering and lack of expressive intonation. Improving reciprocal affective gesturing and the related capacities for motor planning and sequencing may, therefore, contribute in a number of ways to the processes that support language development. These may range from the basics of auditory perception and imitative production of sounds and words to symbol formation and meaning.

In summary, a baby uses simple exploration of relationships outside herself to enter into reciprocal interactions. She then uses reciprocal interactions to explore her world. Longer and longer and increasingly more complex chains of reciprocal interactions, using the different senses and the motor system, then give birth to a variety of the seemingly discrete cognitive, language, social, and visual-spatial and motor planning skills. Gradually, the child progresses through the six stages described earlier to higher levels of creative and reflective thinking.

Implications for Children with Special Needs An important consequence of understanding how important reciprocal affective interactions are for regulating emotions, mood, and behavior relates to therapeutic and educational interventions for children with special needs.

Many children with developmental or emotional problems have difficulties at the fundamental level of back-and-forth signaling globally or in a certain area, as indicated above. Their difficulty may be an inability to engage in or sustain long chains

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of affective reciprocal interactions or to mobilize them in specific processing or emotional areas (e.g., around motor planning, visual-spatial thinking, or feelings of anger or loss).

An appropriate therapeutic approach must work at the level of facilitating reciprocal affective interactions generally and/or specific areas such as language, motor planning, visual-spatial thinking, or expressing anger. The Developmental, Individual-Difference, Relationship-Based model (DIR, i.e., floor time) conceptualizes a comprehensive approach with reciprocal exchanges of affect cues at its foundation (Greenspan, 1992; Greenspan & Wieder, 1998). Many therapies, however, try to help children without establishing reciprocal chains of affective interaction generally or in the area where they are missing. For example, many very structured approaches to therapy, such as behavioral approaches for children with autistic spectrum disorders, fail to realize that one of the primary goals for many of the children is to establish the ability for interacting in a continuous reciprocal flow, that is, for entering into these long chains of reciprocal back and forth communicating. In fact, the lack of reciprocal interaction is one of the key deficits in autistic disorders. The goals of all interventions for autistic spectrum problems needs to involve reciprocal affective interaction, abstract and creative thinking, true empathy, flexible peer relationships, and emotional flexibility and spontaneity.

Behavioral treatment tends to be a stop-start approach, rewarding the child for matching a shape, for example, or for repeating a certain sound. Gifted therapists, in spite of the curriculum sometimes enter into continuous flow with the child, which is usually associated with better progress. Ivar Lovaas, at a meeting where he and I presented and compared the ABA Discrete Trial approach and the Floor Time approach (and had a chance to discuss the relative strengths of both approaches), showed a videotape of himself working with a child in his early years. In the tape, he was entering into a continuous flow of back-and-forth reciprocal communication, which is very different from many of those who carry out his procedures. He was charming and warm and exchanged lots of affect while purporting to offer rewards and punishments. I gently pointed this out to him and he intuitively acknowledged the importance of getting into a relationship with a child where the child feels warm, appreciated, and nurtured. This didn’t lead to a fundamental altering of his theoretical position about what he felt was important, however.

The stop-start approach advocated by formal behavioral theory and procedures often interferes with caregivers or therapists establishing a continuous reciprocal flow and affective rhythm. We’ve seen many children in consultation who have been involved in intensive, 30 + hours/week behavioral (discrete trial) programs. We’ve also observed children as part of a research program who were involved in intensive 30 + hours of behavioral-discrete trial programs. The children we observed in the research program were described by their therapists and parents as having had very good outcomes. The patterns we observed are informative and suggest some of the strengths but also some of the weaknesses of behavioral approaches which did not focus sufficiently on a continuous flow of spontaneous back and forth affective

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gesturing and (and use of language). While there were exceptions the general trend we observed are as follow: the children in these programs generally have learned to use some words and even read and do math, but often cannot engage in a pattern of continuous relating and back-and-forth gesturing; they have difficulty with spontaneous conversation; their behavior is often unregulated and unreciprocal in the sense that they can only conform to specific rules under specific circumstances; new situations are difficult; creative and abstract thinking, including the capacity for making inferences is severely restricted.

In fact, as indicated earlier, a deficit in reciprocal interactions and creative and abstract thinking is a defining characteristic of autistic spectrum disorders (Minshew & Goldstein, 1998; Dawson & Galpert, 1990; Tanguay, et al., 1998).

After years of exlusively very structured behavioral intervention (stop/start), rather than a continuous flow of spontaneous reciprocal interactions, in our observation, many children still present as self-absorbed, idiosyncratic and repetitive, even though with the proper cues they can do very concrete and memory-based academic tasks.

When we then work with these children on their ability to interact with affective gestures, starting with simple fun games, and work up to back and forth negotiations (to open the door or to get the juice), we find that many children can move towards a continuous flow of affective interaction. As we engage children in this way, their repetitive, idiosyncratic and unreciprocal behavior begins to change. They begin using their behavior and existing language and thinking skills in a more purposeful creative and abstract manner. For children who begin this work at age 8 or 9, there is lots of catch-up, however. It can take a number of years to help them develop the basic skills for reciprocal affective gesturing that were skipped over. Many children appear to develop these skills more quickly and fully when intervention is begun at younger ages (Greenspan, 1992; Greenspan & Wieder, 1998). Many children benefit from a balanced program where there is a focus on both spontaneous reciprocal affective interchanges and semi structured problem solving activities. In our experience the key is that when working on specific goals in a semi structured way, the semi structured activities be set up as a challenge which illicits enthusiastic affect and a continuous flow of back and forth interaction while meeting the challenge. For example, teaching a child to “open� in the context of his trying to open the door to get his favorite toy which has been deliberately placed behind the door.

Implication for Child Care The notion that emotional relationships are essential for regulating thoughts, behavior, moods, and feelings is one that needs greater emphasis as we think about child care settings and children’s activities. First, consider that the chains of long back-and-forth affective interactions that are necessary for regulating our behavior, moods and feelings can only occur with a loving caregiver who has lots of time to devote to her child.

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A busy day care provider with four babies or six or eight toddlers usually won’t have the time for these long sequences of back-and-forth emotional interaction.

Similarly, a very depressed mom or dad or an overwhelmed caregiver with five children may not have the needed time, energy, or know-how. Full-time working parents, exhausted at the end of the day, may not be able to engage in these long patterns of back-and-forth interaction. In addition, parents who are being told that structured exercises with picture cards or computer games can improve their children’s intelligence (rather than person-to-person interaction) may mistakenly take time away from important spontaneous, reciprocal interactions in order to do “exercises.” They often do not realize that what they are giving up is more important.

Implications for Children with Emotional and Behavioral Problems The importance of a continuous flow of affective communication is also especially relevant for many traditional types of psychotherapies that work with a range of children, adolescents or adults with circumscribed challenges. The following comments are, therefore, important for children or adults with special needs who have progressed to being quite verbal and related but who have circumscribed emotional challenges and for children and adults who do not have a history of special needs, but evidence selective emotional difficulties.

Traditional psychotherapies tend to focus on listening, reflecting back and summarizing what is being told to the therapist. For the child, this may involve reflecting on patterns revealed in his play; for an adult, it may involve carefully listening and summarizing back empathetically the feelings that are being shared with attempts at insight and pattern recognition. Many therapies involve a fair amount of empathy, warmth and support and sometimes selective guidance and advice.

What’s missing, however, as a point of emphasis in many child and adult insightoriented therapies is the importance of establishing a back-and-forth affective reciprocal flow. In other words, there will often be long times where the therapist is relatively passive, taking in, perhaps empathizing, summarizing, and clarifying periodically, but not working at establishing a dynamic back-and-forth affective interaction. Some child therapists do this as part of the give-and-take in play and are very helpful to their children, but others do not. Some adult therapists who are generally interactive people will do some of this intuitively, particularly for patients who are a little more self-absorbed, withdrawn or depressed. By and large, however, reciprocal affective interaction has not been an explicit focus of therapy, and there is a deliberate stop-start quality to many therapeutic interactions (i.e., long passive pauses rather than dynamic, gestural, back-and-forth, affective cueing and interactions).

Some patients come to treatment with well-developed reciprocal affective regulatory capacities and require help with circumscribed feelings, thoughts, or behaviors. The traditional stop-start approach may not be a problem for such patients and the patterns, clarifications, or insights discussed may prove helpful. For the

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patients whose affects, behaviors or moods are not part of well-established regulatory interactions, i.e., have not been part of this dynamic continuous flow of regulated behavior since infancy and early childhood, however, the focus on reciprocity is paramount for the success of the therapeutic endeavor. As a first step, simply entering into a reciprocal flow around particular emotional themes may be extraordinarily helpful to the patient. One could postulate that the regulation and differentiation occurs through reciprocal interactions around particular emotional areas, such as assertiveness or aggression or sadness or loss or humiliation or shame, etc.

Establishing reciprocity in specific emotional areas is an early step in the therapeutic hierarchy. Just as this step is necessary for normal development, it is necessary for many patients who lack this ability in specific emotional areas or generally. The unregulated patient is at the mercy of global or extreme feeling states. These must be regulated before they can be fully understood symbolically.

Over time, regulated reciprocal interactions in emotionally and thematically important areas lead to problem-solving around that particular emotional theme and then to labeling with ideas and eventually to reasoning. This can lead to high levels of reflection and insight. The process starts, however, with the ability to enter into affective reciprocity around the emotional theme in question. The importance of reciprocal affective interactions may explain why gifted intuitive therapists, even without a lot of experience, may at times do better than experienced, but emotionally less intuitive, therapists. We all know aides or helpers who don’t have an educational background who can often be quite therapeutic. Perhaps it is this ability to establish affective communications in a particular thematic area and engage in a reciprocal continuous flow in these areas that enables such people to be “therapeutic.” Some individuals have a naturally bigger range of different emotional areas They can empathetically respond in a continuous affective flow in the areas of warmth, intimacy, aggression, assertiveness, loss, humiliation, shame, etc. Others are more limited. The individual’s “range” may also be part of what makes some individuals gifted in terms of their therapeutic capacity regardless of their background and training. Interestingly, the explicit training of the therapist may become more important at the symbolic levels where we try to help the patient label the feelings, engage in symbolic elaboration and pattern recognition, and develop reflective capacities as well as insights. Many training programs help professionals develop these traditional skills which are also important for successful therapy. These skills can’t be successfully implemented, however, unless the patient comes in already skillful at the earlier levels of affective reciprocity or is helped to work on these earlier levels.

Some therapists who are less inclined to work on insight and reflection and more on changing behavior will use cognitive behavioral approaches. Imagery is worked on in specifically designed ways. Here, too, however, the ability to work successfully may depend on the mastery of the earlier level of entering into long chains of affective reciprocity. With greater awareness of the importance of affective reciprocity, perhaps it will be possible to train therapists more fully. What’s intuitive for some perhaps can be learned by others.

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The importance of affective reciprocity is relevant to other therapists as well, especially those who use structured techniques (e.g., speech pathologists, occupational therapists, physical therapists, special educators, and early childhood educators).

Working in areas such as auditory processing, motor skills, or visual-spatial thinking requires a highly interactive affective reciprocal manner. As one does this, that system (the motor, visual-spatial processing or auditory processing) undergoes regulation and differentiation. This enables the child to move up the ladder to symbolic elaboration and reflection. Structured methods in these different therapies may be more useful once the child has mastered a reasonable level of affective reciprocity.

Rather than think of this as two steps in a process, where the child goes from reciprocity to symbol formation, the process can be thought of as operating at multiple levels at the same time. The emphasis is on reciprocity when it is not present and hasn’t been mastered. As one moves into the symbolic level, one continues working on reciprocity but adds on symbolic elaboration and the capacity for reflection.

Structured techniques can also help further differentiate language, motor, sensory, or visual-spatial thinking skills. They are most helpful, however, when operating in the context of ongoing affective reciprocal interactions.

Conclusion We have explored the role of affect in the core deficit in autism and in the development of intelligence and social skills. In a sense, we have come full circle. We have discussed how children with autistic spectrum disorders may uniquely, for biological reasons, miss a critical developmental capacity, the ability to connect affect or intent to motor planning and sequencing capacities and, therefore, have a difficult time engaging in the long reciprocal chains of affective interaction so necessary for creative and abstract thinking and high-level social skills. We have also discussed how these same affective interactions underlie intelligence and social development. To improve assessments and interventions for children with a variety of challenges including autistic spectrum disorders, it is imperative to appreciate the role of affective interchanges in disordered and healthy development. The Developmental, Individual-Difference, Relationship-Based model (DIR) enables us to appreciate the role of affect in development by systematizing its dimensions (i.e., its functional developmental level, individual difference, and interactive relationship patterns) (Greenspan, 1992, 1997b; Greenspan & Wieder, 1997, 1998, 1999).

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Mailing Address: Stanley I. Greenspan, M.D. 7901 Glenbrook Road Bethesda, Maryland 20814-4292

STUDIES OF THEORY OF MIND: Are Intuitive Physics and Intuitive Psychology Independent?

Simon Baron-Cohen, Ph.D., Sally Wheelwright, M.A., Amanda Spong, M.A., Victoria Scahill, M.A., and John Lawson, M.A.

Abstract. According to the framework of evolutionary psychology, the human mind should be considered in terms of its evolved adaptedness to the environment (KarmiloffSmith, Grant, Bellugi & Baron-Cohen, 1995). Two postulated neurocognitive adaptations are intuitive (or folk) psychology, for inferring social causality; and intuitive (or folk) physics, for inferring physical causality. In this paper we test these two aspects of our causal cognition in children with Asperger Syndrome (AS). To do this, we employ new tests of intuitive physics and intuitive psychology. Results show that children with AS are impaired in folk psychology whilst being superior in folk physics. Future work needs to test if intuitive psychology and physics are truly independent of one another (implying separate underlying mechanisms) or are inversely related to one another (implying a single underlying mechanism for both).

The Evolutionary Framework The model guiding this study holds that there are specialized neurocognitive mechanisms that have evolved to enable rapid discrimination of two classes of entity: agents vs. non-agents (Baron-Cohen, 1994; Leslie, 1995; Premack, 1990).

This follows from the classical view that in this universe there are only two Acknowledgments: SBC and SW were supported by the MRC and the McDonnell-Pew Foundation during the period of this work. VS was supported by the Anglia and Oxford NHS. JL was supported by the Isaac Newton Trust. Steve Cooter, Rachel Treadaway, Becky Hannon, and Nic Alexander carried out invaluable pilot studies for this study, as part of their final year undergraduate project, for which we are grateful. We are also indebted to Southlands School, Hampshire, and Wolverhampton Grammar School for their co-operation. Special thanks to Maggi Rigg, Ann Wakeling, and Tony Bennett for opening their schools to us.

47

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kinds of entity: those that have intentionality, and those that do not (Brentano, 1874/1970)1. The animate-inanimate distinction doesn’t quite cover the intentional/non-intentional distinction in that plants are of course alive, so the distinction is better covered by the concept of agency (Premack, 1990). Agents have intentionality, whereas non-agents do not. This also means that when agents and non-agents move, their motion has different causes (Csibra, Gergely, Biro, Koos & Brockbanck, 1999; Gelman & Hirschfield, 1994). Agents can move by self-propulsion, which we naturally interpret as driven by their goals and desires, whilst nonagents can reliably be expected not to move unless acted upon by another object (e.g., following a collision).

We assume that the task for hominids as information-processors, over millions of years, has been to compute the causes of these two distinct classes of motion rapidly, since to fail to do so would be self-evidently maladaptive. Dennett’s claim is that humans from infancy onwards use folk (or intuitive) psychology to deduce the cause of an agent’s actions, and use folk (or intuitive) physics 2 to deduce the cause of a non-agent’s movement (Dennett, 1987). Thus, if we see a rock rolling down the hill, and an agent is present then the event could be interpreted as having been caused by an intention (e.g. to throw it, roll it, kick it, etc.,). If no agent is present, the event could be interpreted in terms of a physical causal force (e.g. it was hit by another object, gravity, etc.,). Sperber, et. al., suggest that humans alone have the reflective capacity to be concerned about causality, and that “causal cognition” broadly falls into at least these two types (Sperber, Premack & Premack, 1995).

It may be that aptitudes in folk psychology and folk physics are independent of one another, or are inversely related to one another. The experiments reported below are relevant to these possibilities, since they investigate if some individuals are impaired in their folk psychology but not in their folk physics, and if others show the opposite pattern.

Folk psychology and folk physics may also be under some degree of genetic control. That is, they may comprise modules in a minimally innate sense (Baron-Cohen, 1999). One way one can test if such mechanisms are under some degree of genetic control is by testing for dissociations in individuals who are known to have a genetic disability. In the studies to be reported, we take this approach by investigating folk psychology and folk physics in children with Asperger Syndrome (AS). Before turning to AS, it is necessary to define folk psychology and folk physics, and to consider the evidence from normal development which points to these being “core domains of cognition” (Wellman & Inagaki, 1997).

1 Intentionality is defined as the capacity of something to refer or point to things other than itself. A rock cannot point to anything. It just is. In contrast, a mouse can “look” at a piece of cheese, and can “want” the piece of cheese.

2 We use the terms “folk psychology” “intuitive psychology”, and “theory of mind” interchangeably.

We also intend the terms “folk physics” and “intuitive physics” to be interchangeable.

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Defining Folk Psychology and Folk Physics We define folk psychology as comprising both low-level social perception, and higher-level social intelligence. Low-level here broadly refers to skills present in human infancy ( Johnson, 2000). These include being able to judge (a) if something is an agent or not (Premack, 1990); (b) if another agent is looking at you or not (Baron-Cohen, 1994); (c) if an agent is expressing a basic emotion (Ekman, 1992), and if so, what type. It also includes (d) engaging in shared attention, for example by following gaze or pointing gestures (Mundy & Crowson, 1997; Scaife & Bruner, 1975; Tomasello, 1988); (e) showing concern or basic empathy at another’s distress, or responding appropriately to another’s basic emotional state (Yirmiya, Sigman, Kasari & Mundy, 1992); (f) being able to judge an agent’s goal or basic intention (Premack, 1990). Higher-level here refers to skills present from early childhood and which continue to develop throughout the lifespan. These include the following: (i) Attribution of the range of mental states to oneself and others, including pretence, deception, belief (Leslie, 1987). (ii) Being able to recognize and respond appropriately to complex emotions, not just basic ones (Harris, Johnson, Hutton, Andrews & Cooke, 1989). (iii) Being able to link such mind-reading to action, including language, and therefore to understand and produce pragmatically appropriate language (Tager-Flusberg, 1993). (iv) Using mind-reading not only to make sense of others’ behaviour, but also to predict it, and even manipulate it (Whiten, 1991). (v) Our sense of what is appropriate in different social contexts, based on what others will think of our own behaviour. (v) Empathic understanding of another mind. In short, it includes the skills that are involved in normal reciprocal social relationships (including intimate ones) and in communication. We recognise that we have defined folk psychology broadly, such that it is unlikely to hinge on a single cognitive process. However, we argue that the domain is quite focused and narrowly defined, namely, understanding social causality.

We define folk physics as comprising both low-level perception of physical causality, and higher-level understanding of physical-causality. Low-level here refers broadly to skills present in human infancy, such as the perception of physical causality (Leslie & Keeble, 1987) and expectations concerning the motion and properties of physical objects. Higher-level here refers to skills present from early childhood and which continue to develop throughout the lifespan. These include concepts relating to mechanics (Karmiloff-Smith, 1992). Like folk psychology, folk physics is unlikely to hinge on a single cognitive process. However, like folk psychology, we argue that the domain is quite focused and narrowly defined, namely, understanding how things work.

Both folk physics and folk psychology have been proposed as “core domains of human cognition” because they share seven features (Carey, 1985; Gelman & Hirschfield, 1994; Sperber et al., 1995; Wellman & Inagaki, 1997). Both domains (1) are aspects of our causal cognition, (2) demonstrate precocity in human infancy, (3) are acquired or develop universally, (4) show little if any cultural variability, (5) have a specific but universal ontogenesis, (6) are adaptive, and (7) may be open to

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neurological dissociation. The first of these features (causal cognition) is definitional: folk psychology involves searching for the mental or intentional causes behind agentive events, whilst folk physics involves searching for the physical causes of non-agentive event. Evidence for features 2–5 applying to folk physics and folk psychology comes from studies in developmental psychology, reviewed in the next section.

The sixth feature (adaptiveness) may not be directly testable but has inherent plausibility and we imagine is non-contentious. The final feature (neurological dissociability) is tested with respect to these two domains in the experiment reported later in this paper.

Developmental Evidence Folk psychology appears to be present from at least 12 months of age (BaronCohen, 1994; Premack, 1990). Thus, infants show dishabituation to actions of “agents” who appear to violate goal-directedness (Gergely, Nadasdy, Gergely & Biro, 1995; Rochat, Morgan & Carpenter, 1997). They also expect agents to “emote” (express emotion), and expect this to be consistent across modalities (between face and voice) (Walker, 1982). They are also highly sensitive to where another person is looking, and by 14 months will strive to establish joint attention (Butterworth, 1991; Hood, Willen & Driver, 1997; Scaife & Bruner, 1975). By 14 months they also start to produce and understand pretence (Bates, Benigni, Bretherton, Camaioni & Volterra, 1979; Leslie, 1987). By 18 months they begin to show concern at the distress of others (Yirmiya et al., 1992). By 2 years old they begin to use mental state words in their speech (Wellman & Bartsch, 1988). By 3 years old they can understand relationships between mental states such as seeing leads to knowing (Pratt & Bryant, 1990). By 4 years old they can understand that people can hold false beliefs (Wimmer & Perner, 1983). By 5–6 years old they can understand that people can hold beliefs about beliefs (Perner & Wimmer, 1985). By 7 years old they begin to understand what not to say in order to avoid offending others (Baron-Cohen, O’Riordan, Stone, Jones & Plaisted, 1999a). With age, mental state attribution becomes increasingly more complex (Baron-Cohen, Jolliffe, Mortimore & Robertson, 1997a; Happe, 1993).

Folk physics is also present very early in human ontogeny as manifested in the infant’s sensitivity to apparent violations of the laws of physics. Thus, infants show dishabituation to the unexpected events of larger objects going into smaller ones, objects being unsupported, two objects occupying the same space, one object passing through another, or one inanimate object moving without being touched by another (Baillargeon, Kotovsky & Needham, 1995; Leslie & Keeble, 1987; Spelke, Phillips & Woodward, 1995). That is, even in infancy, humans appear to be sensitive to physical causality. With age, children’s understanding of mechanics grows (Karmiloff-Smith, 1992), but again the precocity of folk physics argues strongly for its status as a core domain. The little cross-cultural evidence that exists suggests a similar picture in very different cultures (Avis & Harris, 1991).

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These data have been interpreted in terms of two innate, independent modules being part of the infant cognitive architecture: a theory of mind mechanism (ToMM) and a theory of bodies mechanism (ToBy) (Leslie, 1995). A theory of mind takes several years to develop, but a more restricted Intentionality Detector (or ID) (BaronCohen, 1994; Premack, 1990) may be part of the starting state of our causal cognition in infancy. The studies reported in this paper are not concerned with whether folk psychology and folk physics are modular systems; rather, they are concerned with these two core domains of cognition in children with Asperger Syndrome. Asperger Syndrome is conceptualised as a variant on the autistic spectrum. This group of children are chosen for two reasons: previous work suggests that a dissociation between these core domains might characterise them; and that this might occur for genetic and neurodevelopmental reasons. We elaborate on these points next.

Asperger Syndrome Asperger Syndrome (AS) was first described by Asperger (Asperger, 1944), and the descriptions of the children he documented overlapped considerably with the accounts of childhood autism (Kanner, 1943). Little was published on AS in English until relatively recently (Frith, 1991; Wing, 1981). Current diagnostic practice recognises AS as meeting the same criteria for autism but with no history of language or communication delay, and with no cognitive delay (APA, 1994; ICD-10, 1994). Although some studies have claimed a distinction between AS and high-functioning autism (HFA) (Klin, Volkmar, Sparrow, Cicchetti & Rourke, 1995), the majority of studies have not demonstrated any significant differences between these. For this reason we use the term AS (for present purposes) as overlapping with HFA. In the experiment reported below, we test folk psychology and folk physics in these children. But first, why should one suspect a dissociation between these two domains will be found in such individuals?

Since the first test of folk psychology in children with autism (Baron-Cohen, Leslie & Frith, 1985), there have been more than 30 experimental tests, the vast majority revealing profound impairments in the development of their folk psychological understanding. These are reviewed elsewhere (Baron-Cohen, 1995; Baron-Cohen, TagerFlusberg & Cohen, 1993) but include deficits in: joint attention (Baron-Cohen, 1989d; Sigman, Mundy, Ungerer & Sherman, 1986); use of mental state terms in language (Tager-Flusberg, 1993); production and comprehension of pretence (Baron-Cohen, 1987; Wing & Gould, 1979); understanding that “seeing-leads-to-knowing� (BaronCohen & Goodhart, 1994; Leslie & Frith, 1988); distinguishing mental from physical entities (Baron-Cohen, 1989a; Ozonoff, Pennington & Rogers, 1990); making the appearance-reality distinction (Baron-Cohen, 1989a); understanding false belief (Baron-Cohen et al., 1985); understanding beliefs about beliefs (Baron-Cohen, 1989b); and understanding complex emotions (Baron-Cohen, 1991). Some adults with AS only show their deficits on age-appropriate adult tests of folk psychology (BaronCohen et al., 1997a; Baron-Cohen, Wheelwright & Jolliffe, 1997b). This deficit in their folk psychology is thought to underlie the difficulties such children have in social and

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communicative development (Baron-Cohen, 1988; Tager-Flusberg, 1993), and the development of imagination (Baron-Cohen, 1987; Leslie, 1987).

The above evidence points to an impairment in folk psychology, but it says nothing about how circumscribed this is. Does it leave their folk physics intact? Or might their folk physics even be super-developed? We predicted the latter, for reasons explained next.

Autism and Folk Physics If children with autism had an impairment in their folk physics, this might suggest that the cause of their problems in the intentional domain was a problem in “theory-building” per se (Carey, 1985). However, there are reasons to suspect that not only is their folk physics intact but may even be superior, relative to normally developing children.

First, there is no shortage of clinical descriptions of children with autism being fascinated by machines (the paragon of non-intentional systems). One of the earliest clinical accounts was by Bettelheim (Bettelheim, 1968) who describes the case of “Joey, the mechanical boy”. This child with autism was obsessed with drawing pictures of machines (both real and fictitious), and with explaining his own behaviour and that of others in purely mechanical terms. On the face of it, this would suggest he had a well-developed folk-physics. The clinical literature reveals hundreds of cases of children obsessed by machines. Parents’ accounts (Hart, 1989; Lovell, 1978; Park, 1967) are a rich source of such descriptions. Indeed, it is hard to find a clinical account of autism that does not involve the child being obsessed by some machine or another. Typical examples include extreme fascinations with electricity pylons, burglar alarms, vacuum cleaners, washing machines, video players, trains, planes, and clocks. Sometimes the machine that is the object of the child’s obsession is quite simple (e.g., the workings of drainpipes, or the design of windows, etc.,).

Of course, a fascination with machines need not necessarily imply that the child understands the machine, but in fact most of these anecdotes also reveal that children with autism have a precocious understanding too. The child (with enough language, such as is seen in children with AS) may be described as holding forth, like a “little professor”, on their favourite subject or area of expertise, often failing to detect that their listener may have long since become bored of hearing more on the subject. The apparently precocious mechanical understanding, whilst being relatively oblivious to their listener’s level of interest, suggests that their folk physics might be outstripping their folk psychology in development. The anecdotal evidence includes not just an obsession with machines, but with other kinds of physical systems. Examples include obsessions with the weather (meteorology), the formation of mountains (geography), motion of the planets (astronomy), and the classification of lizards (taxonomy).

Clinical/anecdotal evidence must however be left to one side, as this may not prove anything. More convincing is that experimental studies converge on the same conclusion: children with autism not only have an intact folk physics, they have

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accelerated or superior development in this domain (relative to their folk psychology and relative to their mental age, both verbal and nonverbal). First, using a picture sequencing paradigm, children with autism performed significantly better than mental-age matched controls in sequencing physical-causal stories (Baron-Cohen, Leslie & Frith, 1986). The children with autism also produced more physical-causal justifications in their verbal accounts of the picture sequences they made, compared to intentional accounts3.

Second, two studies found children with autism showed good understanding of a camera (Leekam & Perner, 1991; Leslie & Thaiss, 1992). In these studies, the child is shown a scene where an object is located in one position (A). The child is encouraged to take a photo of this scene, using a Polaroid camera. Whilst the experimenter and the child are waiting for the photo to develop, the scene is changed: the object is now moved to a new position (B). The experimenter then turns to the child and asks where in the photo the object will be. These studies found that children with autism could accurately infer what would be depicted in a photograph, even though the photograph was at odds with the current visual scene. Again, this contrasted with their poor performance on False Belief tests.

These “false photo” tasks (Zaitchik, 1990) closely parallel the structure of the false belief task. The key difference is that in the (folk psychological) false belief test, a person sees the scene, and then the object is moved from A to B whilst that person is absent. Hence the person holds a belief that is at odds with the current visual scene.

In the false photo task a camera records the scene, and then the object is moved from A to B whilst the camera is not in use. Hence the camera contains a picture that is at odds with the current visual scene. The pattern of results by the children with autism on these two tests was interpreted as showing that whilst their understanding of mental representations was impaired, their understanding of physical representations was not. This pattern has been found in other domains (Charman & Baron-Cohen, 1992; Charman & Baron-Cohen, 1995). But the False Photo Test is also evidence of their folk physics outstripping their folk psychology and being superior to mental age (MA) matched controls.

Family studies add to this picture. Parents of children with Asperger Syndrome (AS) also show mild but significant deficits on an adult folk psychology task (the adult version of the “Reading the Mind in the Eyes” task). This mirrors the deficit in folk psychology seen in patients with autism or AS (Baron-Cohen & Hammer, 1997). This familial resemblance at the cognitive level is assumed to reflect genetic factors, since autism and AS appear to have a strong heritable component (Bailey et al., 1995; Bolton et al., 1994; Folstein & Rutter, 1977; Le Couteur et al., 1996). One should also expect that parents of children with autism or AS to be over-represented in occupations in which possession of superior folk physics is an advantage, whilst a deficit in folk psychology would not necessarily be a disadvantage. The paradigm occupation for such a cognitive profile is engineering.

3 This study however did not involve a chronological age (CA) matched control group, so the apparent superiority in folk physics in autism may simply have reflected their higher CA.

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A recent study of 1000 families found that fathers and grandfathers (patri- and matrilineal) of children with autism or AS were more than twice as likely to work in the field of engineering, compared to fathers and grandfathers of children with other disabilities (Baron-Cohen, Wheelwright, Stott, Bolton & Goodyer, 1997c). Indeed, 28.4% of children with autism or AS had at least one relative (father and/or grandfather) who was an engineer. Related evidence comes from a survey of students at Cambridge University, studying either sciences (physics, engineering, or maths) or humanities (English or French literature). When asked about family history of a range of psychiatric conditions (schizophrenia, anorexia, autism, Down’s Syndrome, or manic depression), the students in the science group showed a six-fold increase in the rate of autism in their families, and this was specific to autism (Baron-Cohen et al., 1998).

This raises the possibility that the cognitive phenotype of autism spectrum conditions may involve superiority in folk physics alongside a relative deficit in folk psychology, relative of course to MA. In this paper we report an experimental test of the prediction that children with AS will have superior folk physics in the presence of impaired folk psychology.

The Experiment Subjects We tested 2 groups of subjects.

Group 1 comprised 15 children (all male) with a clear diagnosis of Asperger Syndrome (AS), defined according to internationally recognised, established criteria (APA, 1994; ICD-10, 1994). They were all attending a special school for Asperger Syndrome (the only one in the UK). This is a residential provision, reflecting the severity of their symptoms and the disruptive impact these had had on their previous schooling and on their family life. They were aged between 8 and 14 years of age, and were all of at least average intelligence. They had all received an IQ test within the previous 2 years, with a standard instrument (WISC-R). Their ages and IQ data are shown in Table 1. They had a range of obsessional interests, consistent with their diagnosis, and these included military tanks, explosives, the periodic table, historical dates, football, electricity, relativity, vehicles, and machines. They had all received a special educational needs statement specifying that they needed special provision as a result of their AS. Group 2 were pupils attending state primary and secondary schools in Cambridge and Wolverhampton, selected at random. They comprised n⫽63 male and n⫽40 female pupils, age range 12–13 (see Table 1), and n⫽53 children, age 6–10 yrs (see Table 2). The children in the 12–13 yr age group (in Table 1) were given the Folk Physics Test, whilst the children in the 6-10 yr age group (in Table 2) were given the Folk Psychology Test (see below). None had been statemented for having special educational needs. They were not given any IQ test because of time

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TABLE 1 Subjects Participating in the Folk Physics Test.

IQ GROUP

x

AS (n⫽15 males) Normal Males (n⫽63) Females (n⫽40)

AGE (sd)

x

VIQ (sd)

13.35

(1.18)

102.4

12.4 12.8

(0.3) (0.3)

– –

(10.1)

x

PIQ (sd)

93.6

(8.8)

FULLSCALE x (sd) 96.9

(9.9)

VIQ⫽Verbal IQ PIQ⫽Performance IQ

TABLE 2 Subjects Participating in the Folk Psychology Test.

IQ GROUP AS (n⫽15 males) Normals (n⫽53) 6-8 yr. olds Males (n⫽9) Females (n⫽11) 8-10 yr. olds Males (n⫽8) Females (n⫽6) 10-12 yr. olds Males (n⫽9) Females (n⫽10)

x

AGE (sd)

13.35

(1.18)

7.3 6.8

(0.7) (0.6)

8.9 9.0

(0.6) (0.3)

11.0 10.7

(0.5) (0.6)

x

VIQ (sd)

102.4

(10.1)

x

PIQ (sd)

93.6

(8.8)

FULLSCALE x (sd) 96.9

(9.9)

constraints but were assumed to have normal intelligence by virtue of their educational placement.

Method The children with AS were all given two tests: 1. The Folk Physics Test (see full test in Appendix A): This comprises 20 questions drawn from a variety of sources, with multiple choice format. This was piloted with a range of age groups of normal subjects, revealing meaningful results only above age 10 years. We consider it as a test of folk physics for two reasons. (a) All the problems could be solved from everyday real world experience of the physical-causal world. (b) The teachers of physics in the schools where our subjects were studying confirmed that these problems had not been taught as part of any school curriculum.

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Since the folk physics task was visual, as a control test for perceptual processing the children with AS were also give the Raven’s Coloured Matrices (Raven, 1956).

2. The Folk Psychology Test: this comprised the children’s version of the Reading the Mind in the Eyes Test, adapted from the adult version (Baron-Cohen et al., 1997a, 2001). Examples are shown in Appendix B. This comprises 28 photographs of the eye region of the face. The subject is asked to pick which of 4 words best describes what the person in the photo is thinking or feeling. The test is the result of piloting with normal children. 3 of the 4 words are foil mental state terms, and the other word is deemed “correct”. (See below for how “correct” was established). Position of the 4 words are randomised for each item. This is not simply a complex test of emotion recognition (although it is this in part) because the mental state words included both affective and non-affective (cognitive) mental state terms.

The Eyes task included a control for non-mentalistic social intelligence: the children were asked to judge the person in the photo’s gender, from their eyes alone. Mental state words were not displayed on this control task, and instead the words “male” and “female” appeared as a forced choice. This latter control test was given in full to the children with AS, but because of limited testing time with the normal children, just a random selection of 8 items were given to the normal subjects, all of whom performed at ceiling on this control test. While we do not claim that the Gender Recognition task is matched for complexity with the mentalizing condition, it nevertheless involves a (nonmentalistic) social judgement from the eyes, and attention to the relevant stimuli.

Regarding children in Group 2 (normal controls), only children over 12 were given the folk physics test, as piloting showed that prior to this age normal performance is poor. Thus, only children in the age groups 6-10 were given the Eyes test, in order to obtain normative developmental data on this test from this age range.

Results Folk Physics Test A one-way ANOVA was used to compare the AS group with the control males and females. There was a significant difference between the groups, F(2, 117)⫽30.4, p⬍0.0001. Post hoc Student Newman-Keuls tests, with significance set at p⬍0.05, indicated that the AS group performed significantly better than both the control males and the control females, who did not differ from each other. See Table 3 for

TABLE 3 Results of the Folk Physics Test: Means and Standard Deviations GROUP

x

(sd)

AS (n⫽15 males) Normal Males (n⫽63) Females (n⫽40)

16.3

(3.1)

10.6 9.9

(2.8) (2.8)

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TABLE 4 Folk Physics Test: Item Analysis (Normal group only)

ITEM

PERCENT OF CHILDREN PASSING ITEM

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20

60.4 76.4 73.6 16.0 73.6 89.6 46.2 18.9 69.8 50.0 83.0 67.9 25.5 61.3 13.2 44.3 42.5 19.8 39.6 65.1

results. An item analysis was carried out. This did not reveal any specific item was failed significantly more often than any other item, in the AS group. In the normal group, there was more variability. (Table 4 shows the item analysis for the normal group.) On the Raven’s Coloured Matrices, the AS group performed in line with (but not significantly above) their mental age (scores, x⫽30, sd⫽4).

Folk Psychology Test The test was first developed to parallel the (revised) Adult Version4 with 36 items, but using child-level vocabulary. It was piloted on a small group of normal children (n⫽6) age 8-12, to identify candidate target and foil words. In the larger sample tested here (n⫽53), all 36 items were screened in two ways. (a) By checking that in all cases the majority of normal subjects (more than 50%) in the 10-12 yr. age group (n⫽19) identified the target word as correct (more than 10 children out of 19 identifying this word). (b) By checking that the second word most commonly identified was chosen by no more than a third of normal subjects in this age group (i.e. no more than 5 children). This was true for all items analysed below (i.e., for 28 items). The remaining 8

4 The published version of this test (Baron-Cohen et al., 1997a) has 25 items. The revised version of this test improves on this by having 36 items. “(Baron-Cohen et al, 2001).”

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items failed to meet these criteria and were therefore dropped from any further analysis. Table 5 shows the item analysis for these remaining 28 items.

In a test of 28 items, with 4 response options, scoring 9 or more out of 28 is above chance (Binomial Test, p⬍0.05). 4 normal children in the 6-8 yr. age group (all girls) failed to score above chance. In the AS group, 2/15 boys failed to score above chance. A one-way ANOVA comparing performance of the AS group and the 3 groups of normal children on the Eyes Test was significant, F(3, 64)⫽16.0, p⬍0.0001.

Post hoc Student Newman-Keuls tests, with significance set at p⬍0.05, indicated that the two oldest groups of normal children scored significantly higher than both the AS group and the youngest group of normal children. This was the only significant difference found in the post hoc analysis. The AS group scored close to ceiling on the Gender Judgement Control Test (x⫽25.3, sd⫽0.3).

TABLE 5 Item Analysis from the Normal Group on the Folk Psychology Test (Data from 10–12 Year Olds Only).

Group 3 Correct Answers Shown in Bold n⫽19 ANSWER A 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28

26.3 0.0 63.2 0.0 36.8 5.3 10.5 78.9 5.3 21.1 0.0 10.5 84.2 5.3 52.6 57.9 5.3 89.5 5.3 5.3 52.6 0.0 21.1 68.4 15.8 10.5 31.6 5.3

ANSWER B 0.0 5.3 5.3 100.0 63.2 0.0 15.8 0.0 0.0 21.1 84.2 0.0 15.8 94.7 5.3 0.0 0.0 5.3 31.6 0.0 0.0 0.0 68.4 15.8 15.8 5.3 0.0 0.0

ANSWER C 57.9 5.3 0.0 0.0 0.0 63.2 68.4 0.0 0.0 57.9 0.0 0.0 0.0 0.0 21.1 15.8 5.3 5.3 5.3 94.7 26.3 5.3 0.0 15.8 10.5 63.2 52.6 73.7

ANSWER D 15.8 89.5 31.6 0.0 0.0 31.6 5.3 21.1 94.7 0.0 15.8 89.5 0.0 0.0 21.1 26.3 89.5 0.0 57.9 0.0 21.1 94.7 10.5 0.0 57.9 21.1 15.8 21.1

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TABLE 6 Results of Folk Psychology Test: means and standard deviations.

EYES TEST GROUP

x

(sd)

x

AS (n⫽15 males) Normals (n⫽53) 6–8 yr. olds Males (n⫽9) Females (n⫽11) 8–10 yr. olds Males (n⫽8) Females (n⫽6) 10–12 yr. olds Males (n⫽9) Females (n⫽10)

12.6

(3.3)

26.5

14.6 12.5

(5.1) (5.6)

18.1 17.7

(4.7) (3.5)

20.2 21.0

(2.4) (2.4)

GENDER CONTROL TEST (sd) (2.3)

Results are shown in Table 6. An Age by Gender ANOVA in the normal group alone, on the Eyes Scores, found a significant main effect of Age (F(2,52)⫽13.9, p⬍0.0001), with the youngest age group scoring significantly lower on the Eyes Test compared to the older two age groups, who did not differ from each other (Student Newman-Keuls Test, p⬍0.05). There was no effect of Gender (F(1, 52)⫽0.3, p⫽0.62), and no Age by Gender interaction (F(2,52)⫽0.6, p⫽0.60).

Correlation Between Folk Physics and Folk Psychology in AS A test of correlation between folk psychology and folk physics in the normal group was not possible since different groups of children were given each of these tests. In the group with AS, the two tasks were strongly inversely correlated (r⫽-0.63, p⫽0.001).

Discussion The experiments in this paper derive from the model that the human brain has evolved at least two independent modes of causal cognition: folk psychology and folk physics. In the extreme case, severe autism may be characterised by almost no folk psychology (and thus “mindblindness”). Autism spectrum conditions come by degrees, so different points on the autistic spectrum may involve degrees of deficit in folk psychology (Baron-Cohen, 1995). We predicted that in those individuals who have no accompanying mental handicap (i.e., whose intelligence is in the normal range), the child’s folk physics would develop not only normally, but even at a superior level. This was tested in a group of children with Asperger Syndrome (AS). This prediction was confirmed: children with AS were functioning significantly above their mental age (MA) in terms of folk physics, but significantly below their MA in terms of folk psychology.

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The control tasks in this experiment enable us to conclude that children with AS are not superior in all visuo-spatial tasks (since they were normal but not above average on the Raven’s Matrices). On the Eyes Task they were clearly attending to the eyes well enough to judge gender. This pattern of results suggests their understanding in folk physics may represent an islet of ability; and that their difficulties on the Eyes Task may be specifically linked to mind-reading.

We take seriously the notion that this profile in AS (impaired folk psychology, together with superior folk physics) might be partly the result of a genetic liability.

This is because AS appears to be heritable (Gillberg, 1991), and because there is every reason to expect that individuals with such a cognitive profile could have been selected for in hominid evolution. Good folk physics would have conferred important advantages to an individual’s inclusive fitness (e.g., tool use, hunting skills, construction skills, etc.,), even if that individual’s folk psychology skills were less proficient.

Note that a genetic factor could operate in at least two different ways: (a) An individual might have a genetically-based impairment in folk psychology; or (b) a genetically-based talent for folk physics. This second alternative derives from the idea of an independent module for folk physics (Leslie, 1995). It is possible that in autism spectrum conditions we see the twin genetic anomalies of impaired folk psychology co-occurring with superior folk physics. But whether the present results reflect (a) or (b) above, or both, such genotypes would lead the individual to spend less time interacting with the social environment, and more time interacting with the physical environment, since he or she would understand the latter better. A gene-environment interaction could then explain why such a brain, developing along an abnormally one-sided trajectory, would lead to a superiority in folk physics.

What is the extra explanatory scope of documenting superior folk physics in autism spectrum conditions, over and above the (now standard) demonstration of a theory of mind deficit in autism? The theory of mind account has been virtually silent on why such children should show “repetitive behaviour”, a strong desire for routines, and a “need for sameness”. To date, the only cognitive account to attempt to explain this aspect of the syndrome is the executive dysfunction theory (Ozonoff, Rogers, Farnham & Pennington, 1994; Pennington et al., 1997; Russell, 1997). This paints an essentially negative view of this behaviour, assuming that it is a form of “frontal lobe” perseveration or inability to shift attention.

Whilst some forms of repetitive behaviour in autism, such as “stereotypies” (e.g., twiddling the fingers rapidly in peripheral vision) may be due to executive deficits, the executive account has traditionally ignored the content of “repetitive behaviour”.

The current account draws attention to the fact that much repetitive behaviour involves the child’s “obsessional”5 or strong interests with mechanical systems (such as light switches or water faucets) or other systems that can be understood in physi5 Elsewhere (Baron-Cohen, 1989c) we review the argument for why the term “obsession” can only be used in the context of autism with some qualifications. This centers on the traditional definition of an obsession being “egodystonic” (or unwanted). In autism, there is no evidence that the child’s strong interests are unwanted. Rather, those individuals with autism or AS who can report on why they engage in these activities report that they often derive some pleasure from them. They are therefore probably egosyntonic.

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cal-causal terms. Rather than these behaviours being a sign of executive dysfunction, these may reflect the child’s intact or even superior development of their folk physics.

The child’s obsession with machines and systems, and what is often described as their “need for sameness” in attempting to hold the environment constant, might be signs of the child as a superior folk-physicist: conducting mini-experiments in his or her surroundings, in an attempt to identify physical-causal principles underlying events.

Certainly, our recent study of obsessions suggests that these are not random with respect to content (which would be predicted by the content-free executive dysfunction theory), but that these test to cluster in the domain of folk physics (Baron-Cohen & Wheelwright, 1999).

In this paper we have not presented a task analysis of folk physics, and it could be argued that the good folk physics skills seen here are simply an expression of an anomaly previously documented, namely “weak” central coherence (Frith, 1989; Happe, 1996). Weak central coherence refers to the individual’s preference for local detail over global processing. This has been demonstrated in terms of an autistic superiority on the Embedded Figures Task (EFT) and the Block Design Subtest ( Jolliffe & Baron-Cohen, 1997; Shah & Frith, 1983; Shah & Frith, 1993). Both of these are interpreted as evidence of good segmentation skills, and superior attention to detail. The latter has also been demonstrated on visual search tasks (Plaisted, O’Riordan & Baron-Cohen, 1998a; Plaisted, O’Riordan & Baron-Cohen, 1998b).

The question is whether superior folk physics, like weak central coherence, might simply reflect this superior attention to detail. This is a strong possibility, and merits direct testing in the future. If confirmed, this would not invalidate the usefulness of studying folk physics in autism spectrum conditions. Rather, it may show strong folk physics as an upstream benefit of weak central coherence.

Developing a New Model If folk psychology and folk physics are independent dimensions it is possible to plot on orthogonal axes possible scores from possible tests assessing these two abilities. Figure 1 provides a visual representation of this model of the relationship between folk psychology and folk physics. It suggests appropriate labels for different possible patterns of scores. The axes show number of standard deviations from the mean. The scale of the diagram is less important than the principle underlying it.

We have used the terms Balanced Brain, Social Brain, Technical Brain, Extreme Social Brain and Extreme Technical Brain as short-hand to describe these different possible patterns of scores. The terms describe the discrepancy between the folk psychology score and the folk physics score. In the Balanced Brain, there is no difference between scores. In the Social Brain, folk psychology is one or two standard deviations higher than folk physics. In the Extreme Social Brain, this discrepancy is greater than two standard deviations. The same pattern is used for the Technical Brain and the Extreme Technical Brain. In the Technical Brain, folk physics is one or two standard deviations higher than folk psychology whilst for the Extreme Technical Brain, this discrepancy is greater than two standard deviations.

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F IGURE 1. Folk psychology—folk physics dimensions.

It is worth underlining the fact that the key point is the discrepancy between the scores rather than the absolute scores themselves. For example, someone could score two standard deviations above the mean on folk psychology (a very high score) but if they scored three standard deviations above the mean on folk physics, they would be described as having the Technical Brain. Thus, the key issue is possible asymmetries of ability.

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Our ongoing work is testing this model. If folk physics and folk psychology are truly independent, then it should be possible to find individuals in every square within the diagram (no correlation). If there is some trade-off between abilities in folk physics and folk psychology, then the majority of individuals should have results which fit into the top left quadrant or bottom right quadrant of the diagram (negative correlation). If folk physics and folk psychology abilities are subserved by the same underlying system, then the majority of individuals should have results which fit into the top right quadrant or bottom left quadrant (positive correlation). It is important to clarify that we conceptualise folk physics and folk psychology will both vary with mental age (MA). Therefore, standardised norms will need to be obtained for each level of MA. Evidence from sex difference research (Kimura, 1992) suggests that the Technical Brain type is more commonly found in males whilst the Social Brain type is more frequent in females. For this reason we can also use the terminology Female Brain and Male Brain types as synonyms for the Social and Technical Brains, respectively. This claim is also being tested as part of ongoing work, using a wider variety of tests and assessments.

Autism has been described as the extreme form of the male brain (Baron-Cohen & Hammer, 1997). Figure 2 illustrates where we predict the vast majority of people with autism will be located in this (MA-matched) framework. Although this area overlaps with the Extreme Technical brain they are not exactly the same. This is because we predict that people with autism will always score more than one standard deviation below the mean on folk psychology and also that they will always score more than one standard deviation above the mean folk physics. We tested this prediction using the AS group data and control data from above. The scores for the AS group on the Eyes test were transformed to z-scores using the mean and standard deviation from the eldest group of control children (so the children were as closely matched on MA as possible). All the scores from the control children who did the folk physics test were used to produce the mean and standard deviation to standardise the AS group on the folk physics test. Figure 3 shows the relationship between the standardised folk physics and folks psychology scores in the AS group. Note that all but one of the children appear in the bottom right quadrant. Obviously, the number of subjects in this test is limited and in future studies, a battery of tests is likely to be used to make up the folk physics and folk psychology scores. However, this first test of the model is encouraging.

It is important to stress that this approach is in no way diagnostic. We do not intend to imply that someone who scores in the Extreme Technical Brain area should be diagnosed with autism. Rather, we are simply predicting that people with autism are more likely to score in the Extreme Technical Brain area than in any other area.

Figure 2 also illustrates where the contrast case to autism is located. This area is the exact opposite of the predicted autism area, overlapping with the Extreme Social Brain, but not matching it exactly. Some people have speculated as to whether people with Williams syndrome might have the Extreme Social Brain, (Karmiloff-Smith et al., 1995), though this is debated (Tager-Flusberg, Boshart & Baron-Cohen, 1998).

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F IGURE 2. The predicted location for autism spectrum conditions and the contrast case.

Note that in the same way that autism can be considered either from the perspective of difficulties (folk psychology ) or strengths (folk physics), so can the contrast case.

In the latter case, the difficulties are predicted to be in folk physics (we could think of this as technical-blindness) whilst the strengths are remarkable empathy. Such a case is predicted by this model but has not yet been documented. Our ongoing work will go out to test for such cases.

F IGURE 3. Distribution of standardised scores on the physics and eyes tests in the AS group.

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Note that the two dimensions of folk psychology and folk physics are conceptualised as independent of IQ. We certainly know of cases in individuals with Asperger syndrome whose IQ is in the superior range but who perform in the low range on empathy (folk psychology) tests (Baron-Cohen et al., 1999c). We speculate that whilst IQ may influence folk physics ability to a greater extent, there may be individuals whose folk physics is out of keeping with their IQ. The children with Asperger syndrome in the above study are an example of this, since they were normal on the Raven’s matrices.

This article has focused on folk physics and folk psychology, because they are two forms of causal cognition. As has been discussed by others (Hatano & Inagaki, 1994; Sperber et al., 1995; Wellman, 1990), other universal cognitive domains may also exist. The principal other candidates are folk mathematics (counting) and folk biology (classification of the animate world into species, predators, prey, etc.). We remain to be persuaded that these are independent domains, since it is plausible that folk mathematics is simply part of folk physics, for example. However, in the same way that a deficit in folk psychology should leave folk physics either unaffected or superior in autism, the same arguments should lead to unaffected or superior development of folk mathematics and folk biology in such individuals.

This model of the independence of folk physics and folk psychology (or social and non-social intelligence) also predicts the existence of very high functioning individuals with AS, who may be extreme high achievers in domains such as mathematics and physics—equivalent to Nobel Prize winners even - but who have deficits in folk psychology. Our recent case studies are beginning to identify such very highfunctioning individuals (Baron-Cohen et al., 1999c).

In conclusion, the present data suggest folk psychology is impaired in individuals with AS, whilst their folk physics is superior. This is consistent with recent neurological reports of the effects of specific lesions to the amygdala causing specific impairments in social perception (Damasio, Tranel & Damasio, 1990). It is of some interest that using functional magnetic resonance imaging (fMRI) the normal brain shows activation of the amygdala when performing the Eyes Task, whilst individuals with AS show significantly reduced amygdala activity (Baron-Cohen et al., 1999b).

Whilst the brain basis of folk psychology is gradually being unravelled, the brain basis of folk physics is as yet unknown.

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Appendix A: The Folk Physics Test

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Appendix B: Folk Physics Test Answers 1.

2.

3.

4.

5.

6.

7.

8.

9.

10.

11.

12.

13.

14.

15.

16.

17.

18.

19.

20.

c c b b c a a d b a b a a a c a c a d c

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Appendix C: Examples from the Children’s Version of the Reading the Mind in the Eyes (Folk Psychology) Test (Revised).

1. Female Correct answer⍽sure about something surprised

joking

sure about something

happy

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Appendix C: Examples from the Children’s Version of the Reading the Mind in the Eyes (Folk Psychology) Test (Revised).

2. Male Correct answer⫽Friendly friendly

surprised

sad

worried

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Shah, A., & Frith, U. (1983). An islet of ability in autism: a research note. Journal of Child Psychology and Psychiatry, 24, 613–620.

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Mailing Address: Simon Baron-Cohen, Ph.D. Autism Research Centre Departments of Experimental Psychology and Psychiatry, University of Cambridge, Downing St, Cambridge, CB2 3EB, UK

ASPERGER SYNDROME AND HIGH FUNCTIONING AUTISM: Shared Deficits or Different Disorders?

Christopher Gillberg, M.D., Ph.D.

Abstract. This paper provides a selective review and personal point of view about the relationship between Asperger syndrome and high-functioning autism. The terms are more likely synonyms than labels for different disorders. Most cases of Asperger syndrome and high-functioning autism are unlikely to be caused by one set of identical factors. We may be looking for genetic factors or brain damage factors, or other factors, not yet studied, but it is unlikely, particularly with the range of comorbidity demonstrated that we are dealing with one set of identical factors.

Overlapping and shared brain circuitries are likely to be involved in autism and some of its overlapping and comorbid conditions. For instance, the link with ADHD, DCD and Tourette syndrome suggests a common dopamine abnormality, and the link with affective disorders and the obsessive compulsive symptoms suggests serotonin dysfunction. Specific disorders, such as tuberous sclerosis and certain chromosomal disorders may provide very important links when it comes to the location of the brain lesion and also to the fine mapping of genetic factors.

Introduction Hans Asperger’s original paper from 1944 (Asperger, 1944) is interesting in that, long before anybody thought of including very high-functioning individuals with autistic features in the broader group with “autism” he described the characteristics of “highfunctioning autism”. True, he referred to “autistic psychopathy”, and most of us working in the field now use Lorna Wing’s term “Asperger’s syndrome”, but it has becoming increasingly clear that the constellation of symptoms he described reflects “autism” in individuals who are not moderately or severely mentally retarded (Gillberg & Ehlers, 1998).

Having said this, I should perhaps add that it was not Asperger who first described the syndrome that now bears his name. A Russian neurologist, Eva Ssucharewa, published a paper in the mid 1920s in which she described “schizoid personality disorder” in children. Reading Sula Wolff’s translation of that paper it becomes clear that Ssucharewa described the core deficits and major hallmarks of autism long before Asperger or Kanner (Ssucharewa 1926, Wolff 1995).

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The Diagnosis of Asperger Syndrome and High-Functioning Autism Asperger Syndrome Asperger never outlined diagnostic criteria for “autistic psychopathy”. The first operationalized criteria for diagnosing Asperger syndrome were outlined by our group at the first international conference on Asperger’s syndrome which was held in London in 1988. These criteria, which are based specifically on Asperger’s own case reports, appeared in print in 1989 and were elaborated in more detail in 1991 (Gillberg & Gillberg, 1989, Gillberg, 1991). The Gillberg criteria for Asperger syndrome have been systematically tested against other criteria for the disorder and against criteria for autism (typical or atypical). They delineate a group of highly verbal, ritualistic, socially severely malfunctioning individuals with special narrow interests and odd ways of communicating with other people (Table 1). About half of all high-functioning individuals in the autism spectrum meet these criteria (Leekam, et al., 2000). Many of these also meet criteria for autistic disorder or atypical autism (roughly equivalent to pervasive developmental disorder not otherwise specified). The Gillberg criteria are problematic in that they require a very severe and very specific type of symptomatology and that they do not rule out the diagnosis of autistic disorder. We have recently thought of changing the algorithm so that meeting criteria for five out of the six (rather than all six) symptom areas would suffice for caseness if the social criterion is met and reserve the diagnosis for individuals whose symptomatology does not better fit the criteria/clinical picture of autistic disorder.

Peter Szatmari published his criteria for Asperger’s syndrome in 1989 (Szatmari, et al., 1989). They are similar to those of our own group but can be used only for individuals who do not meet criteria for autistic disorder (Table 2). The ICD-10 (WHO 1992) and DSM-IV (APA 1994) criteria for the syndrome are virtually identical to each other (Table 3). They are problematic in that they specifically exclude cases with signs of early language, developmental or social delays.

Virtually nobody with an autism spectrum disorder fits these criteria (Leekam, et al., 2000). Asperger’s own cases do not meet criteria for DSM-IV Asperger’s disorder (Ozonoff and Miller, 1997).

In clinical practice, the DSM-IV criteria for Asperger’s disorder are not helpful.

There is a problem stemming from the fact that clinicians are trying to squeeze patients into the DSM-IV/ICD-10 framework, which really requires that individuals with the syndrome should have been normal up until age three years. I have yet to meet a patient with the clinical presentation that Asperger described who was completely normal in his development early on. Another problem is that the actual symptom threshold for qualifying for a diagnosis is very low; only two social and one behavioural symptoms are required to reach diagnostic status. The ICD-10 has the additional problem that there is no specification that symptoms have to be handicapping in daily life.

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TABLE 1 Diagnostic criteria for Asperger syndrome (Gillberg & Gillberg) 1. Social impairment (extreme egocentricity) (at least two of the following): (a) difficulties interacting with peers (b) indifference to peer contacts (c) difficulties interpreting social cues (d) socially and emotionally inappropriate behaviour 2. Narrow interest (at least one of the following): (a) exclusion of other activities (b) repetitive adherence (c) more rote than meaning 3. Compulsive need for introducing routines and interests (at least one of the following): (a) which affect the individual’s every aspect of every-day life (b) which affect others 4. Speech and language peculiarities (at least three of the following): (a) delayed speech development (b) superficially perfect expressive language (c) formal pedantic language (d) odd prosody, peculiar voice characteristics (e) impairment of comprehension including misinterpretations of literal/implied meanings 5. Non-verbal communication problems (at least one of the following): (a) limited use of gestures (b) clumsy/gauche body language (c) limited facial expression (d) inappropriate facial expression (e) peculiar, stiff gaze 6. Motor clumsiness poor performance in neuro-developmental test

There are no universally agreed criteria for high-functioning autism, but it would seem reasonable to reserve this label for those individuals who meet full criteria for autistic disorder, and who, in addition, have full-scale IQs in the nonretarded range.

It would seem obvious from this overview of diagnostic criteria that (a) there is no clear consensus as to the diagnostic criteria that are most appropriate for Asperger syndrome, (b) there are major problems fitting DSM-IV/ICD-10 criteria for Asperger syndrome to real live patients/individuals, and (c) there is no clear borderline between Asperger syndrome and high-functioning autism (in fact, in many instances, the two terms are used interchangeably for the same kind of behavioural phenotype).

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TABLE 2 Diagnostic criteria for Asperger syndrome according to Szatmari et al. (1989) 1. Social isolation (at least two of the following): (a) no close friends (b) avoids others (c) no interest in making friends (d) a loner 2. Impaired social interaction (at least one of the following): (a) approaches others only to have own needs met (b) clumsy social approach (c) one-sided responses to peers (d) difficulty sensing feelings of others (e) indifference to the feelings of others 3. Impaired non-verbal communication (at least one of the following): (a) limited facial expression (b) impossible to read emotions through facial expression of the child (c) inability to convey message with eyes (d) avoids looking at others (e) does not use hands to aid expression (f) large and clumsy gestures (g) infringes on others people’s physical space 4. Speech and language peculiarities (at least two of the following): (a) abnormalities of inflection (b) over-talkative (c) non-communicative (d) lack of cohesion to conversation (e) idiosyncratic use of words (f) repetitive patterns of speech

The Clinical Presentation Asperger Syndrome There is always marked social impairment in Asperger syndrome, usually showing as extreme egocentricity. There is mostly a much decreased ability to interact with peers, often coupled with a lack of desire to interact with peers, a lack of appreciation of social cues, and socially and emotionally inappropriate behaviors. The social impairment may actually be just as marked in Asperger syndrome as in classic autism, but the overall better functioning and the higher level of skills in the former syndrome may go along way in obfuscating the major problems. However,

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TABLE 3 ICD-10, WHO, 1993 Diagnostic criteria for Asperger syndrome 1. There is no clinically significant general delay in spoken or receptive language or cognitive development. Diagnosis requires that single word should have developed by 2 years of age or earlier and that communicative phrases be used by 3 years of age or earlier. Self-help skills, adaptive behaviour, and curiosity about the environment during the first three years should be at a level consistent with normal intellectual development.

However, motor milestones may be somewhat delayed and motor clumsiness is usual (although not a necessary diagnostic feature). Isolated special skills, often related to abnormal preoccupations, are common, but are required for diagnosis.

2. There are qualitative abnormalities in reciprocal social interaction in at least two of the following areas: (a) failure adequately to use eye-to-eye gaze, facial expression, body posture, and gesture to regulate social interaction (b) failure to develop (in a manner appropriate to mental age, and despite ample opportunities) peer relationships that involve a mutual sharing of interests, activities, and emotions (c) lack of social-emotional reciprocity as shown by an impaired or deviant response to other people’s emotions, or lack of modulation of behaviour according to social context; or a weak integration of social; emotional, and communicative behaviours (d) lack of spontaneous seeking to share enjoyment, interests, or achievements with other people (e.g. lack of showing, bringing, or pointing out to other people objects of interest to the individual) 3. The individual exhibits an unusually intense, circumscribed interest or restricted, repetitive, and stereotyped patterns of behaviour, interests, and activities in at least on two of the following: (a) an encompassing preoccupation with one or more stereotyped and restricted patterns of interest that are abnormal in their intensity and circumscribed nature though not in their content or focus (b) apparent compulsive adherence to specific, non-functional routines or rituals (c) stereotyped and repetitive motor mannerisms that involve either hand- or fingerflapping or -twisting, or complex whole-body movements (d) preoccupations with part-objects or non-functional elements of play materials (such as their odour, the feel of their surface, or the noise or vibration that they generate

several years may pass before family, peers, relatives and teachers understand that something is seriously amiss, and it may only be with hindsight that they realize that there was never a period of normal development.

The narrow interest pattern, was something that Asperger himself put a lot of emphasis on. He felt that this interest pattern should lead to the exclusion of other activities, or be very repetitive, or be more relying on memory than underlying meaning. Even though the narrow interest pattern is highly characteristic of the most typical cases of males with Asperger syndrome, there are those, and particularly those females, who otherwise fit the criteria for the disorder, who do not demonstrate this feature. Some girls (and a very few boys) with the other core fea-

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tures of the condition have a strong tendency to avoid demands and to always say “no”. It is as though their main interest in life is to say no, negative things, and to go around “being bored”. They themselves cannot seem to find anything to interest them. Just occasionally, other people may find something to attract their interest, and they can then become totally absorbed for a while, whereafter the “boring state” returns.

In spite of the fact that “his” children, as he sometimes called them, were usually good with formal language, Asperger noted that they had language and speech peculiarities. He drew attention to the possibility that, even though they had this formal language level, which was usually very good, they were very often slightly delayed, particularly as compared to their brothers and sisters. It is common for a child with Asperger syndrome to have “delayed” expressive language development; they do not speak at an early age, even though you had the feeling that they would have been able to if they wanted to/felt the need to. I certainly see a number of kids who say nothing for two-three years and then suddenly start speaking because they “have something to say”. Some of them actually say: “Why should I speak before I have something important to say?”. There are also children who, are able to read before they start speaking. They have superficially expressive perfect language and they are very often formal and pedantic in their style and they have, most of them, this very odd prosody. More often than not there is impairment of comprehension, also, in the face of—sometimes extremely—good expressive skills. They sometimes have very mild, but often very marked comprehension problems.

There are also non-verbal communication problems in this group of individuals, and Asperger put a lot of emphasis on the odd gaze behaviors, in particular the staring gaze and the fixed gaze of the young boys that he saw. Incidentally, it was only towards the end of his life that he believed that the syndrome could occur in any form in females. He thought it was an exclusively male disorder. Odd and awkward gait, strange posturing (sometimes approaching catatonia) and a mask-like facial expression are all common features.

Asperger also noted the motor clumsiness. This may be most marked in social situations and be reflected in clumsy feeding behaviors, spilling, stumbling, tripping, or in inability to swim, ride a bike etc. Our own group always felt that this was an important part of the syndrome.

High-Functioning Autism The description of the typical presentation of Asperger syndrome is also one that would fit high-functioning autism in most domains. If there are differentitating features and the two conditions are separate from each other (at least in some cases), language competence and full scale IQ would probably be the most likely differentiators, both being at a lower level of functioning in high-functioning autism than in Asperger syndrome.

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Prevalence Asperger Syndrome The prevalence of this disorder, as diagnosed on the Gillberg criteria, has been in the range of 0.26 through 0.71 per cent (Gillberg & Gillberg, 1989, Ehlers et al., 1993, Magnusson & Gudjonsdottir, 1994, Landgren, et al., 1996, Kadesjö & Gillberg, 1999). The five prevalence studies—which have all come from the Nordic countries— are in relatively good agreement, and it would seem reasonable to conclude that the rate of the disorder is about half a per cent of the general population of school age children. Nevertheless, further prevalence studies from other geographical regions are clearly needed before firm conclusions can be drawn in this respect.

High-Functioning Autism The most recent studies of autistic disorder have quoted prevalence figures of about 0.1 per cent. About 30% of cases in those studies have had IQs over 70. These would constitue “highfunctioning” cases, meaning that the prevalence of high-functioning autism (not necessarily meeting criteria for Asperger syndrome) would be 0.03 per cent.

Mental Retardation Asperger Syndrome The vast majority of individuals who receive a diagnosis of Asperger syndrome have IQs in the normal or near normal range (or are of superior intelligence). Only a few per cent of all published cases have associated mental retardation.

High-Functioning Autism Almost by definition, cases with high-functioning autism would not have mental retardation. However, in clinical practice, it is not uncommon for individuals with this diagnostic label to have normal performance IQ, but verbal IQ may be in the retarded range, so that full scale IQ is just under 70.

The Rate of Mental Retardation in Autism If, as most authors seem to agree, Asperger syndrome is part of the autism spectrum, then we need to change our concepts as to how often mental retardation is associated with autism.

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Counting autistic disorder (low- and high-functioning cases) and Asperger syndrome, the rate of associated mental retardation in the autism spectrum would be about 15%, far different from the much quoted figures of 70–80% mental retardation in autism. Now, 15% is well above the prevalence of mental retardation in the general population, but certainly nothing near the level that we have been used to thinking about when discussing autism. Thus, the majority of individuals in the autism spectrum, are NOT mentally retarded.

Male:Female Ratios The boy:girl ratio in most studies of Asperger syndrome have been reported to be 5-10:1 (even up to 47:1). However, in the Nordic population studies, there are usually about 3–4 boys for every girl. If, instead, we go to our clinic, where all of the children are very severely impaired, the ratio of boys to girls goes up drastically.

It is likely that girls/women with the core features of Asperger syndrome/high-functioning autism may go unrecognised to a much larger extent than boys. This, in turn, may be due to the fact that both Asperger and Kanner described mostly prototypical boys, and that, therefore, our way of conceptualising the syndromes is based on the phenotypical expression in males, not in females. Interestingly, we have found a high rate of Asperger syndrome/high-functioning autism/PDD NOS in female teenagers/adults with anorexia nervosa (Wentz, et al., 2000) and selective mutism (Kopp & Gillberg, 1997). They had had core autistic features all their lives, but it was only when they were meticulously worked-up for the other condition that their autism spectrum disorder was really disclosed.

Comorbidity Asperger syndrome is very often comorbid with at least one other condition (Figure 1). The findings that apply to Asperger syndrome are probably translatable to high-functioning autism also.

According to the population-study by our own group, tics (including fullblown Tourette syndrome) and ADHD are the most common comorbidities (Ehlers et al., 1993), each occurring in more than half of all clear-cut or suspected cases. Developmental coordination disorder (DCD) is almost universal, but then, at least according to some of the diagnostic algorithms, clumsiness is part and parcel of Asperger syndrome, and it might therefore seem redundant to list DCD as a separate disorder. In the Nordic countries ADHD with DCD is usually registered as “DAMP” (“Deficits in Attention, Motor control and Perception”). Several studies have shown DAMP to be strongly associated with autism spectrum problems, and the rate of Asperger syndrome in DAMP is increased about thirtyfold compared with the general population (Gillberg & Gillberg, 1989, Kadesjö & Gillberg, 2000).

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FIGURE 1. Overlap of mild to moderate, and severe) DAMP (ADHD+DCD), autistic features, and Asperger syndrome (data from Gillberg C., 1983 and Gillberg I.C. and Gillberg C., 1989) and possible overlap with ICD-10 hperkinetic syndrome and DCD. (Adapted from Clinical Child Neuropsychiatry, Gillberg C., 1995, Cambridge: Cambridge University Press, by permission.)

However, there are many other conditions that sometimes can occur in Asperger syndrome. Some of these may be chance coincidences, but in many cases there appears to be a more meaningful link between the autism spectrum disorder and the other condition (Gillberg & Billstedt, 2000). This may be particularly true for obsessive-compulsive disorder (OCD) and obsessive-compulsive personality disorder (OCPD), for anorexia nervosa and selective mutism (Gillberg, 2000).

Depression quite often develops in the pre-adolescent or adolescent period in children who have high-functioning autism or Asperger syndrome. This may either be a reflection of comorbidity with manic-depressive illness (deLong, et al., 1986) or be seen as a reactive condition following in the footsteps of feeling socially awkward and of being an “outsider�.

Many adults with Asperger syndrome or high-functioning autism apply for psychiatric help but are only occasionally correctly diagnosed as having an autism

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spectrum disorder. We have seen our previous patients diagnosed with borderline personality disorder, antisocial personality disorder, paranoid disorder, psychosis, and schizophrenia. Only rarely would these diagnostic labels seem appropriate.

There is, of course, the occasional patient who, having had an autism spectrum disorder from the very first years of life, does develop schizophrenic symptoms in late adolescence, in which case both the autism spectrum disorder and schizophrenia should be diagnosed. However, much more often, the schizophrenia label is not really appropriate. It may be a matter of the adult psychiatrist not being familiar with the history and symptoms of an individual with Asperger syndrome/high-functioning autism which makes him/her liable to make a diagnosis of a condition with some overlapping symptomatology for which there is a well-known framework.

Alcoholism appears to be much overrepresented in Asperger syndrome as compared with the general population (Wing, 1981, Hellgren, et al., 1994), but the studies published to date have either been on potentially biased groups or included very small samples making it impossible to draw any generalized conclusions at this stage.

Learning disorders (including problems with reading, writing, mathematics, physical education) are probably overrepresented, particularly in high-functioning autism, but the systematic evidence in the field is limited. Even in Asperger syndrome (where IQ is usually normal or even very high, and hyperlexia is very common) there may be severe academic difficulties. However, these seem usually to stem more from the social and behavioural problems rather than from any basic cognitive deficit (physical education may be an exception though, and the problems encountered in this field might well be a consequence of underlying neurological dysfunction).

Genetic Factors There is good evidence that genetic factors account for a majority of all cases with autistic disorder, including those that are designated as high-functioning (Gillberg & Coleman, 2000). The evidence comes from population studies of twins, family studies, studies of sib-pairs and epidemiological studies of autism in the general population. The search for susceptibility genes is on, and it appears that certain chromosomal regions may be much more interesting than others.

There is widespread agreement that Asperger syndrome is probably a genetic disorder/variant in a majority of all cases. However, there is nothing near the amount of evidence that exists for classic autistic disorder. Autistic disorder and Asperger syndrome quite often appear in one and the same extended family. There is, quite possibly, a genetic link with manic-depressive illness in Asperger syndrome (deLong, et al., 1986), at least in a subgroup. Nevertheless, studies reporting on series of clinical cases have also found a high index of perinatal distress (Wing 1981, Gillberg 1989, Rickarby, et al., 1991), and one of these (Rickarby, et al., 1991) found no indication of familial loading. Perinatal stress may sometimes be a reflection of a genetic defect. However, in other cases, it may contribute to brain damage in itself.

Thus, any generalized conclusion in respect of the genetics of Asperger syndrome would seem premature.

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Neurology and Neuropsychology In classic autism, there is quite often an associated medical condition such as tuberous sclerosis or a chromosomal disorder. Population studies have indicated that such an association applies in about one in four of all cases, whereas in clinical studies the rate drops to about one in eight. (This may be because clinicians who work up and follow a child with tuberous sclerosis may not refer him/her for a separate diagnosis of autism since they feel that there is already an “established diagnosis”— tuberous sclerosis—that accounts for the child’s problems.)

The rate of associated medical conditions in the high-functioning cases—including Asperger syndrome—is lower (probably at or under one in eight cases) (Gillberg, et al., 1987). However, occasionally, you do come across Asperger syndrome phenotypic presentations with underlying tuberous sclerosis (Gillberg, I.C., et al., 1994), fetal alcohol syndrome (Aronson, et al., 1997), CATCH-22-syndrome (Niklasson, et al., 2000) or other chromosomal disorders (Annerén et al., 1998). In some instances, these underlying disorders provide clues as to the basic etiology of the autism spectrum disorder.

Epilepsy is common in autism spectrum disorders. Several studies indicate that about one in four to one in three of all individuals with autistic disorder has epilepsy, which can have its onset in the first two years or (usually much) later (Gillberg, 1991).

The rate is much lower in those with higher IQ: one study reported ten per cent of those with high-functioning autism and nobody with Asperger syndrome had epilepsy (Ehlers, et al., 1997).

Many studies have found indices of anatomical brain abnormality in Asperger syndrome. However, all of these have been on potentially selected clinical samples and it has not yet been possible to tease out whether referral factors/comorbid conditions rather than Asperger syndrome per se account for the findings. Our own group compared brain CT scans of 18 Asperger syndrome and 22 high-functioning children with autistic disorder and found some cerebral atrophy in 17% of the former and 22% of the latter group (Gillberg, 1989). Another group found MRI abnormalities (mostly rightsided cortical) in the brains of five out of seven individuals with Asperger syndrome and comorbid Tourette syndrome. Other MRI and PET-scan studies have yielded variable results (Piven, et al., 1992, Herold, et al., 1988, Horwitz, et al., 1988). Our own group studied adults with Asperger syndrome and compared them with normal adults on PETscan measures in connection with theory of mind tasks (Happé, et al., 1996). The Asperger group showed lack of activation of a relatively distinct area in the left frontal lobe, an area which was markedly activated in the normal group. In a SPECT-study of high- and low-functioning cases with autism (with and without epilepsy), all individuals showed temporal lobe hypoperfusion and frontal hypoperfusion in one in three cases regardless of IQ-level and presence of epilepsy (Gillberg I.C., et al., 1993).

Here are just some of the things that have been associated in a few studies with Asperger’s Syndrome. The study we just completed on Megalencephalus, that is large head size in Asperger’s and Autism suggest that it’s only in the very high functioning group that you’ll find a large excess of individuals with big heads. In fact 24% of classic Asperger’s cases we have consistently macrocephalus. They have it both at birth and later so we did not replicate the findings by a few other groups that we mega-

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lencephalus comes at a later age. It was there from the very beginning and it was there when we followed them up much later. No consistent findings have yet emerged in respect of other neurophysiological or neurochemical studies in the field of high-functioning autism or Asperger syndrome.

There is now an enormous wealth of data relating to the neuropsychology of autism (Happé, 2000). Conversely, there is a very limited neuropsychological literature that has attempted to differentiate high-functioning autism from Asperger syndrome (Nydén, 2000). In one study, children with high-functioning autism showed the typical autism profile on the WISC with a peak on Block Design and troughs on Comprehension and Picture Arrangement. Individuals with Asperger syndrome showed much better performance on Comprehension but relatively poor on Object Assembly, Digit Span, and Digit Symbol. These latter results were similar to those of an ADHD (attention-deficit/hyperactivity disorder group), placing Asperger syndrome in the middle of a spectrum with autistic disorder at one end and ADHD at the other (Ehlers, et al., 1997). According to another study, school age children with high-functioning autism and Asperger syndrome could not be differentiated from those with ADHD on most measures of executive functioning, even though they differed markedly from a normal comparison sample (Nydén et al., 2000).

Outcome Studies The results of the general population follow-up studies of individuals in the autism spectrum that we are now doing, and which are not yet completed, suggest that outcome is restricted, not only in low-functioning cases of autism but also in those that are most high-functioning. This may hold particularly true for those, who, at one or other time during development, applied for help. Now, that should not be taken to mean that if you apply for help you have a poorer outcome because the people who help you turn you into some kind of monster. But, it does imply that if you come to a hospital setting, for instance, or a clinic, you are more likely to have more severe problems. Some data (e.g. Ehlers & Gillberg, 1993) indicate that only about half of all individuals who meet full criteria for Asperger syndrome (and who are, in a sense, “clinically” impaired), actually apply for professional help in childhood or adolescence.

The follow-up studies reporting on outcome in clinical series of patients with highfunctioning autism also suggest that prognosis is not very good, even though about one in four may function relatively well in adult age (Rumsey, et al., 1985, Szatmari, 1989).

I have met many individuals with Asperger syndrome who have superficially excellent outcomes, who have had a university degree, an excellent job, and a family. Nevertheless, the spouses of the young Asperger syndrome men that we followed up still feel that their husbands have some terrible problems. The men themselves feel that they are fine and they’re doing well and there is not a major problem. Some of them have children. Unfortunately, at least in one case, that child has turned out to have severe autism.

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There is obviously a range of outcomes in Asperger syndrome and you will see that the variability is much broader than in so-called classical autism, where the range, although wide, is much more narrow.

The results from our ongoing follow-up study suggest that 50% do relatively well in adult age. There seems to be a relatively stable prognosis in that, if you had Asperger’s or high-functioning autism as a child, you are very likely to have those same problems when you’re 20 years older, even though you may get a very different diagnosis once you go to see adult psychiatrist.

High-Functioning Autism and Asperger Syndrome: Where are the Boundaries?

Lorna Wing, Judy Gould and I have recently done a study with Sue Leekam and others in London (Leekam, et al., 2000). We looked at 200 cases that attended the Center for Social and Communication Disorders in London over a period of years.

They were all referred with a suspicion of an autism spectrum disorder and were worked up using the DISCO, the Diagnosis of Social and Communication Disorders (Wing, et al., 2000). This instrument allows you to make an algorithm diagnosis by computer: you get a printout of exactly who meets what criteria. So we used all the possible criteria that were in the literature, ICD 10-Childhood Autism, ICD 10Asperger’s Syndrome, ICD 10-Atypical Autism, Gillberg-Asperger syndrome etc.

Out of those 200 cases, 174 met full Childhood Autism criteria by ICD-10 criteria.

(Parenthetically, I might add that we are currently doing a study in Gothenburg where we are comparing the results of the DISCO to those of the ADI-R and you get very similar results although the ADI-R tends to give a diagnosis of Childhood Autism slightly more often than the DISCO. Now, one thing that most people have not observed is that diagnostic algorithms for atypical autism and PDD-NOS do not rule out a diagnosis of Asperger’s, meaning that atypical autism and Asperger’s can be diagnosed in one and the same individual.) Only three individuals out of the 200 met full criteria for Asperger’s according to the ICD 10. That is only because of the criterion of normal development in the first three years of life. However, there were 91 that met the Asperger criteria according to our own group. We looked more carefully at this group, and found that they were more intelligent than the remaining 117 (two thirds of the Asperger’s group had normal IQ, whereas only 50% in the group of cases meeting Childhood Autism/Atypical autism criteria, but not our criteria for Asperger’s, had normal IQ). There was significant difference also with regard to language estimate (the Gillberg Asperger group had much better language development). These were really the only major findings that differentiated the Gillberg Asperger syndrome cases from the other cases of Autism and Atypical Autism in the whole study. Interestingly, the majority of those with Gillberg’s Asperger syndrome also met full criteria for childhood autism.

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So, in conclusion, there is no good evidence, I think, that so-called high functioning autism and Asperger’s are different disorders. When we use these concepts, we are probably referring to the same group of individuals, and depending on where we work, and what history we have, we tend to use one diagnosis more than the other. The only possible difference that we could tease out from this rather large scale study was in regard to IQ or verbal IQ, and even that could only distinguish between groups, not between individuals.

Conclusion Most cases of Asperger syndrome and high-functioning autism are unlikely to be caused by one set of identical factors. The terms are more likely synonyms than labels for different disorders. We may be looking for genetic factors or brain damage factors, or other factors, not yet studied, but it is unlikely, particularly with the range of comorbidity demonstrated that we are dealing with one set of identical factors.

Overlapping and shared brain circuitries are likely to be involved in autism and some of its overlapping and comorbid conditions. For instance, the link with ADHD, DCD and Tourette syndrome suggests a common dopamine abnormality, and the link with affective disorders and the obsessive compulsive symptoms suggests serotonin dysfunction. Specific disorders, such as tuberous sclerosis and certain chromosomal disorders may provide very important links when it comes to the location of the brain lesion and also to the fine mapping of genetic factors.

The label Asperger syndrome may, to some purists, present a major obstacle: why use it if it is only another word for high-functioning autism? Asperger syndrome was the term introduced by Lorna Wing at a time when very few people realised that autism stretches far beyond the boundaries of the condition outlined by Kanner. It has been very useful in that it has served as an eye-opener. In the old days, mere mention of the word autism produced images of extreme impairment, non-speaking, completely withdrawn individuals. You could not tell parents or teachers that this high-functioning child had that. Asperger syndrome was more “neutral”. By using the term Asperger syndrome for two decades now, we have moved forward in the field of autism. It is now seen as a spectrum of conditions in which there are severe and milder variants, and a wide variety of clinical presentations. I doubt that this leap forward would have been accomplished so quickly if the term had not been there to help us disregard the long shadow of the past that was cast by those who insisted on the old myths about “classic autism”.

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Annerén G, Dahl N, Uddenfelt U (1995) Letter to the Editor: Asperger syndrome in a boy with a balanced de novo translocation: t(17;19)(p13.3; p11). American Journal of Medical Genetics 56: 1–8.

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Aronson M, Hagberg B, Gillberg C. Attention deficits and autistic spectrum problems in children exposed to alcohol during gestation: a follow-up study. Developmental Medicine and Child Neurology 1997; 39: 583–587.

Asperger H. Die autistischen Psychopathen im Kindesalter. Archiv für Psychiatrie und Nervenkrankheiten 1944; 117: 76–136.

DeLong GR, Dwyer JT. Correlation of family history with specific autistic subgroups: Asperger’s syndrome and bipolar affective disease. Journal of Autism and Developmental Disorders 1988; 18: 593–600.

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Ehlers S, Nydén A, Gillberg C, Dahlgren-Sandberg A, Dahlgren S-O, Hjelmquist E, et al.

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Gillberg C. Asperger syndrome in 23 Swedish children. Developmental Medicine and Child Neurology 1989; 31: 520–531.

Gillberg C. Clinical and neurobiological aspects of Asperger syndrome in six family studies.

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Gillberg C. The Emanuel Miller Memorial Lecture 1991: Autism and autistic-like conditions: subclasses among disorders of empathy. Journal of Child Psychology and Psychiatry 1992; 33: 813–842 Gillberg C, Billstedt E. Autism and Asperger syndrome: the coexistence with other clinical disorders. Acta Psychiatrica Scandinavica 2000; 102: 1–10.

Gillberg C, Coleman M. The Biology of the Autistic Syndromes. Third Edition. London: Cambridge University Press, 2000.

Gillberg C, Ehlers S. High-functioning people with autism and Asperger syndrome. A literature review. In: Gillberg C and Ehlers S (ed(s)). Asperger Syndrome or High Functioning Autism? Special Issue of Journal of Autism and Developmental Disorders. New York: Plenum Press. 1998. 79–106.

Gillberg C, Steffenburg S, Jakobsson G. Neurobiological findings in 20 relatively gifted children with Kanner-type autism or Asperger syndrome. Developmental Medicine and Child Neurology 1987; 29: 641–649.

Gillberg IC, Bjure J, Uvebrant P, Gillberg C. SPECT (Single Photon Emission Computed Tomography) in 31 children and adolescents with autism and autistic-like conditions.

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Gillberg IC, Gillberg C. Asperger syndrome—some epidemiological considerations: a research note. Journal of Child Psychology and Psychiatry 1989; 30: 631–638.

Gillberg IC, Gillberg C, Ahlsén G. Autistic behaviour and attention deficits in tuberous sclerosis. A population-based study. Developmental Medicine and Child Neurology 1994; 36: 50–56.

Happé F. An overview of the psychology of autism. Papers read at the 6th International Congress Autism-Europe. Glasgow, May 2000.

Happé F, Ehlers S, Fletcher P, Frith U, Johansson M, Gillberg C, et al. “Theory of mind” in the brain.

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Hellgren L. Psychiatric Disorders in Adolescence. Longitudinal Follow-up Studies of Adolescent onset Psychoses and Childhood onset Deficits in Attention Motor Control and Perception. M.D. Thesis. Göteborg University. 2000.

Herold S, Frackowiak RSJ, Le Couteur A, Rutter M, Howlin P. Cerebral blood flow and metabolism of oxygen and glucose in young autistic adults. Psychological Medicine 1988; 18: 823–831.

Horwitz B, Rumsey JM, Grady CL, Rapoport SI. The cerebral metabolic landscape in autism.

Intercorrelations of regional glucoseutilization. Archives of Neurology 1988; 45: 749–755.

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Kadesjö B, Gillberg C. The comorbidity of ADHD in the general population of swedish school age children. Journal of Child Psychology and Psychiatry 2000; In press.

Kadesjö B, Gillberg C, Hagberg B. Brief report: Autism and Asperger syndrome in SevenYear-Old Children. A Total Population Study. Journal of Autism and Developmental Disorders 1999; 29: 327–331.

Kopp S, Gillberg C. Selective mutism: A population-based study: Research note. Journal of Child Psychology and Psychiatry 1997; 38: 257–262.

Landgren M, Pettersson R, Kjellman B, Gillberg C. ADHD, DAMP and other neurodevelopmental/neuropsychiatric disorders in six-year-old children. Epidemiology and comorbidity. Developmental Medicine and Child Neurology 1996; 38: 891–906.

Leekam S, Libby S, Wing L, Gould J, Gillberg C. Comparison of ICD-10 and Gillberg’s criteria for Asperger syndrome. Autism 2000; 4: 11–28.

Magnusson P, Gunnarsdóttir K. The epidemiology of autism and Asperger syndrome in Iceland: A summary of a pilot study. Arctic Medical Research 1994; 53, Suppl. 2: 464–466.

Miller JN, Ozonoff S. Did Asperger’s cases have Asperger Disorders? A research note. Journal of Child Psychology and Psychiatry 1997; 38: 247–251.

Niklasson L, Rasmussen P, Óskarsdóttir S, Gillberg C. The chromosome 22q11 deletion syndrome (CATCH 22)—Some neuropsychiatric and neuropsychologic aspects.

Developmental Medicine and Child Neurology 2000; Submitted.

Nydén A. Autism spectrum disorders. Developmental, cognitive, and neuropsychological aspects. M.D. Thesis. Göteborg. Department of Child and Adolescent Psychiatry. Göteborg University. 2000. pp 63.

Nydén A, Gillberg C, Hjelmquist E, Billstedt E. Neurocognitive abilities in boys with Asperger syndrome, attention disorder, and reading and writing disorder: Stability over time.

Developmental Medicine and Child Neurology 2000; Accepted.

Piven J, Nehme E, Simon J, Barta P, Pearlson G, Folstein SE. Magnetic resonance imaging in autism: measurement of the cerebellum. Biological Psychiatry 1992; 31: 491–504.

Rickarby G, Carruthers A, Mitchell M. Brief report: biological factors associated with Asperger syndrome. Journal of Autism and Developmental Disorders 1991; 21: 341–348.

Rumsey JM, Rapoport JL, Sceery WR. Autistic children as adults: psychiatric and behavioral outcomes. Journal of The American Academy of Child Psychiatry 1985; 24: 465–473.

Ssucharewa GE. Die schizoiden Psychopathien im Kindesalter. Monatsschrift für Psychiatrie and Neurologie 1926; 60: 235–261.

Szatmari P, Brenner R, Nagy J. Asperger’s syndrome: a review of clinical features. Canadian Journal of Psychiatry 1989; 34: 554–560.

Wentz Nilsson E, Gillberg C, Gillberg IC, Råstam M. Ten Year Follow-up of Adolescent-Onset Anorexia Nervosa: Personality Disorders. Journal of the American Academy of Child and Adolescent Psychiatry 1999;38: 1389–95 Wing L. Asperger’s syndrome: a clinical account. Psychological Medicine 1981; 11: 115–129.

Wolff S. Loners. The Life Path of Unusual Children. London: Routledge, 1995.

Mailing Address Christopher Gillberg, M.D., Ph. D. Professor of Child and Adolescent Psychiatry Department of Child and Adolescent Psychiatry Göteborg University Kungsgatan 12 411 19 Göteborg Sweden

A System of Classification for Autism Spectrum Disorder

Peter E. Tanguay, M.D., Julia Robertson, M.D., Ann Derrick, A.R.N.P., M.S., C.S.

Abstract. Although there is no conclusive evidence that autism is a spectrum disorder, the concept can be clinically useful in classifying persons who show a broad range of social communication deficits. We have used the Autism Diagnostic Interview—Revised and the Autism Diagnostic Observation Schedule to assess affective reciprocity, joint attention and theory of mind in persons diagnosed as having autism, Asperger’s Disorder and Pervasive Developmental Disorder—Not Otherwise Specified. Persons with more severe forms of autism show marked deficits in all three domains, while milder forms of autism may primarily show handicaps in social cognition and joint attention. We present a case study of an autistic child who had some affective reciprocity, but poor joint attention and imaginative play. Based on his skills and handicaps, we suggest what specific interventions would be indicated. A social communication model may help to quantify core social communication deficits in the autism spectrum.

Although case descriptions of children whom we recognize as possibly autistic have appeared from time-to-time in the early psychiatric literature of the last hundred years (Barr, 1898), it was only in 1943 that a description of what would come to be known as autism was independently delineated by Kanner (1943) and by Asperger (1991). Descriptions of “psychotic” children were presented in the 1950’s and 1960’s under the terms autism, childhood schizophrenia, atypical psychosis and various other labels. The first official classification of autism did not appear in DSM systems until into the 1970’s (American Psychiatric Association, 1980). This classification was based upon a small number of well-executed epidemiological studies of children with early onset psychoses. Although the clinical description of autism has been refined through further epidemiological work into the DSM-IV classification (American Psychiatric Association, 1994), its current official definition is similar to that reported in DSM-III. Like other conditions in DSM-III and DSM-IV, the diagnosis is a categorical one, based upon a person’s meeting a set of diagnostic criteria whose number and degree of severity are specified. The category of autism has been found to be one of the most robust in the DSM system in terms of its diagnostic specificity and sensitivity (Volkmar et al., 1994), and it continues to serve us well for research purposes.

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Over the past twenty years there has been a growing recognition among clinicians that some persons might have symptoms and handicaps similar in nature to those found in autism, but in a way that does not meet the full DSM criteria for the diagnosis. Other categories, both official and unofficial, have been suggested in the DSM-IV and ICD-10. These include Pervasive Developmental Disorder—Not Otherwise Specified (PDD-NOS) and Asperger’s Disorder, while “high-functioning autism” (Eisenmajer et al., 1996), Non-Verbal Learning Disorder (Klin, Volkmar, Sparrow, Cicchetti, & Rourke, 1995), Pragmatic-Semantic Disorder (Mayes, Volkmar, Hooks, & Cicchetti, 1993), Multiple Complex Developmental Disorder (Van-der et al., 1995) and “atypical autism” are used unofficially among clinicians and scientists. The persons so designated may not be fully autistic, but they are usually so handicapped that they often cannot function in society and require a lifetime of special services. Recently, population-based studies have suggested that the “broader” classification of autistic-like disorders may have a prevalence rate of 1/1000 or even 1/500, as compared to a rate of 1/2000 for “classical” autism (Fombonne, Du, Cans, & Grandjean, 1997; Honda, Shimizu, Misumi, Niimi, & Ohashi, 1996).

If we are to move ahead in understanding these early-onset developmental disorders, we may need to re-think the categorical approach of the DSM-IV and the ICD-10 in favor of an approach which would allow classification of autism in terms of a spectrum of severity. Although some family studies of persons with autism have suggested that there might be a range of social oddities or increased cognitive and language problems in the relatives of persons with autism (Bailey et al., 1995; Boutin et al., 1997; Piven et al., 1994; Szatmari et al., 1996), there are no data to prove that autism is, in fact, a spectrum disorder. It might be that what we see as a “spectrum” is a number of distinct conditions whose apparent overlap is clinically artificial. Only when we have a much better understanding of the underlying genetic and environmental factors which influence the clinical manifestations of autism will it be possible to know whether at least some forms of Pervasive Developmental Disorder (PDD) may be described along a spectrum of severity, or whether most forms of PDD will be found to represent specific conditions such as Fragile-X Syndrome, Rett’s Disorder or other genetically-influenced entities wherein a small set of genetic abnormalities can lead to a variety of broad clinical outcomes.

The results of recent multi-center family pedigree studies have been reported to be compatible with a model in which genetic defects in autism occur at a large number of loci, perhaps 15 or more (Risch, Spiker, Lotspeich, Nouri, & Hinds, 1999). If this is true, then it may be unlikely that we will be able to closely match phenotypic expressions of autism with specific gene abnormalities. The outcome of this research may be a system in which a specific gene abnormality will be understood as conferring a degree of susceptibility to a specific deficit or symptom in autism.

Currently, our best practical approach to characterizing autism may be as a spectrum disorder. Aside from its immediate clinical usefulness, study of the “spectrum” model might lay the groundwork for defining those phenotypic characteristics of the

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population which might eventually be linked to those genes and gene products which do play a role in autism.

But a spectrum of what? One suggestion derives from studies of social communication in childhood which have been carried out in the past several decades (for a review see Sigman & Capps, 1997; Baron-Cohen S, Tager-Flusberg, & Cohen, 1993). This literature is already well-developed, and while there are many arguments as to the nature of the phenomena in question, certain observations are agreed upon. Children are born with what appear to be innate behavioral propensities to interact with others, using facial expression, gesture, prosody and “body language”. Within the first year of life, and before the development of speech or of propositional thought, children learn a rich repertory of spontaneous social interactions with their caregivers. Children with severe autism, even if they have apparent normal intellectual capacity, fail to show these behaviors (Charman, 1997; Mundy, 1995; Lewy & Dawson, 1992). Possibly they come into the world without the necessary behavioral propensity, or perhaps they have the propensity but their threshold for perceiving facial, gestural and verbal cues is so high that the latter are ineffective.

For the past several years, we have been attempting to develop a method to clinically conceptualize and measure social communication in children who have autism and related forms of PDD. Our measurement instruments have been the Autism Diagnostic Interview—Revised (ADI-R) (Lord, Rutter, & Le, 1994) and versions of the Autism Diagnostic Observations Schedule (ADOS) (Lord et al., 1989; DiLavore, Lord, & Rutter, 1995). We chose these instruments because both contain many questions about or observations of the elements of social communication in children. We found (Tanguay, Robertson, & Derrick, 1998; Robertson, Tanguay, L’Ecuyer, Sims, & Waltrip, 1999) that a factor analysis of a subset of the social-communication items from each of the instruments yielded three domains.

The factors mirrored phenomena described in the social communication literature: affective reciprocity, joint attention and theory of mind. We believe that the three domains are not specific stages in development, but merely a way which the field has chosen to characterize the salient characteristics seen in what is otherwise a seamless developmental trajectory.

Affective Reciprocity This encompasses the extent to which the person sends various social signals to others, through facial expression, tone of voice and social and emotional gestures. It could be seen as a type of instinctual drive whose function is to cause a child to send social signals to others and to look for social signals. The more the child is driven to interact with others, the more he or she can learn the meaning of such signals. Affective reciprocity is also shown by affectionate and empathic behaviors, greeting others with pleasure and spontaneously offering to share toys or food with others.

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Joint Attention By 15 months of age, children are eager to share their interests with others. They show things to others, they try to share their enjoyment, they babble reciprocally and they direct others’ attention to objects which interest them. Later, when they have language, they ask about others’ interests and ideas, and they share others’ enjoyment.

Theory of Mind Pragmatic skill represents knowledge about the “rules of social communication”.

In its simplest form, this includes knowing how to begin a conversation, how to continue a conversation, how to end a conversation and how to choose topics of conversation which are appropriate to the situation at hand. Theory of mind implies the ability to correctly infer what another person’s intentions may be. It allows one to automatically and successfully respond to others while furthering, through the interaction, one’s own needs and goals. One must have an adequate theory of mind in order to use “good common sense”. Theory of mind is learned through years of interacting with others. Those who lack pragmatic skills and an adequate theory of mind are completely at sea when it comes to conversing, chatting and negotiating with others.

The nature of “theory of mind” has been hotly debated (Baron-Cohen S et al., 1993). Is it the ability to empathically put oneself into another person’s frame of mind?

Or is it a product of logical cognitive operations operating on known observations?

There is evidence that the phenomena is first seen early in life (Sorce, Emde, Campos, & Klinnert, 1985). By age three it has been shown that children have a strong propensity to classify the world of people and the world of objects in very different ways (see Baron-Cohen’s article elsewhere in this issue). By age four children believe that people act as a result of “motives,” while they understand that objects do not have a mind of their own and can only respond to mechanical actions. The former phenomena has been called “folk psychology,” while the latter has been referred to as “folk physics.”

High-functioning autistic persons appear to have a serious lack of understanding of “theory of mind” or of a propensity to think in terms of “folk psychology” even if their understanding of “folk physics” may appear advanced or even hypertrophic.

We have observed that children with poor affective reciprocity do not develop good joint attention or good imagination/play; but persons with reasonable affective reciprocity may develop variable degrees of joint attention and imagination/play.

Persons with the least degree of social communication handicap, who might be classified as Asperger’s Disorder or PDD-NOS in DSM-IV, have greater deficits in imagination and play than in joint attention. It should be noted that non-autistic mentally retarded children, as well as children with deafness, have been shown by previous investigators to have poor “theory of mind” and poor imagination and play skills (Yirmiya, Solomonica-Levi, Shulman, & Pilowsky, 1996; Russell et al., 1998). It has also been our clinical impression that while social communication can be a useful

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dimension for classifying persons with autism and Asperger’s Disorder, it is inadequate unless it is supplemented by specific information about intellectual level and verbal (semantic-syntactic) language skills. It is also crucial that the presence of other developmental phenomena, e.g. hypersensitivity to sensory input, poor gross and fine motor skills and unusual motor stereotypies be included in individual case descriptions.

Case Presentation Developmental and Social History from the Autism Diagnostic Interview—Revised (ADI-R) William Jones is a 45-month-old child who lives with his mother and grandmother. His father and mother are divorced. He attends a day care program. The program is not staffed to care for children with special needs. He runs away from the class, ignores the other children and “refuses” to play games. Based on what she read on the Internet, Willie’s mother suspected that he might be autistic.

When Willie was six months of age his mother recalls that he seemed responsive: he played baby games with her and looked her in the eye. But by twelve months of age he had stopped interacting with others. He no longer paid any attention to his mother, was not interested in sharing objects or events with her and did not develop social language or even social babble. By three years of age he would have periods when he would be excited by some repetitive action he saw on TV, at which time he would flap his hands while staring at the TV out of the corner of one eye. Currently, he has no interest in other children and avoids their social overtures. When frustrated, he engages in tantrums in which he bangs his head against objects. He does not talk spontaneously and is echolalic. He is fascinated with the Seven Dwarfs which he watches on videos over and over again. He tries to order all his toys or objects which he finds about the house in sevens, and he repeats fragments of what he heard on the videotapes. These vocalizations have very limited social use.

In her replies to questions on the ADI-R, William’s mother indicated that he has little evidence of affective reciprocity, i.e., drive or skills that would indicate that he reaches out to others using eye contact, facial expression or gesture. What speech he has is echolalic, with sing-song prosody. He does not nod his head yes or shake his head no.

He does not reach up to others when he wishes to be picked up, though he did sometimes echo his mother’s gesture of reaching out to him. He ignores others in distress and fails to respond to excitement in other children, even at his own third birthday party.

His joint attention is similarly deficient. Even children who do not have language can show extensive social interaction with their caretakers, but Willie does not. He does not show things that interest him to others, nor does he point to others to show them things which interest him. His lack of joint attention was said to be profound.

He appears to have little social imagination or theory of mind, inasmuch as he engages in no imaginative play. He is described as lining up objects and being very upset if others disturbed his lines. He is also upset if others do not put his toys away

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in a particular order. He has been upset by changes in routine. A teacher who is absent from school can send him into a state of acute anger and despondency.

Family History A maternal uncle is quite certainly autistic by Ms. Jones’ description. His parents have refused to have him evaluated, however; and he lives at home as an adult. He is not employed. He has good language and is a walking encyclopedia of baseball statistics and information about recorded music. He does not use this knowledge to interact normally with others. There is also an 18-year-old paternal cousin who may have autistic traits. He also has low intelligence and has dropped out of school.

ADI-R Algorithm Scores The data gathered on the ADI-R were subjected to analysis using algorithms which come with the ADI-R for the diagnosis of autism. William’s scores were within the range for autism in all three DSM-IV domains: impairment in reciprocal social interaction, impairment in verbal and non-verbal communication and presence of a markedly restricted repertoire of activities and interests.

Observations Based on the Autism Diagnostic Observation Schedule (ADOS) William was an attractive, well-groomed boy, looking a bit older than he is.

When the examiner greeted him and introduced herself in the lobby, he looked at her and said “Hi.” He was playing with a Tarzan cause-and-effect toy, making a monkey go up and down the tree; he brought a slide over for the monkey to slide on. He ran down the hall once then reluctantly held the examiner’s hand and his mother’s on the way to the playroom. In the playroom he ran right to the toys to close and open the Poppin’ Pals.

From the outset it was clear that Willie was quite echolalic, using various phrases and words in a rote way. Despite his lack of conversational ability, however, he was capable of using rote phrases and greetings in a way which made him initially appear more socially in touch than he was. His echolalic phrases included “want to play with the blocks?” and “all the little pieces.” Spontaneous phrases included: “Let’s play the bunny,” “Here, Mom,” “I’ve got a three,” “Hey, where the bubbles go?” and “Let’s put it on the plate.” Willie also repeated a number of apparently spontaneous phrases, e.g., during the birthday party, he said, about five times: “Let’s play with the cake.” His prosody was quite good (the tone, rhythm, volume, rate of his speech). His articulation varied from crystal clear to mumbling

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Affective Reciprocity Willie demonstrated affective reciprocity but not consistently. He frequently emitted normal facial expressions of affect but failed to direct them to anyone. He had a beautiful smile and very expressive face. When the examiner inflated a balloon, he imitated the manner in which she opened her mouth, and when she released the balloon, he ran enthusiastically to pick it up and hand it back to her to blow up again.

Willie enjoyed social routines like Ring-around-the-Roses and anticipated the “all fall down” right on cue. He enjoyed the make-believe birthday party and knew to place the candles on the cake, sing the song and blow out the candles. He showed eager anticipation for the routines. He was not the least bit interested in feeding or playing with the doll, however. With much encouragement he started to give the doll a drink but then pretended to drink himself. He did offer his mother a drink, and he initiated a play interaction with her, saying, “Here, Mom,” and handed her a stacking cup, meshing gesture and vocalization, although he did not look at her.

Although Willie clearly enjoyed some of the activities, the examiner was unable to elicit a social smile from him. He did not point, nor did he use any other gestures.

He did not wave goodbye even with many prompts. When the examiner said “the doll is sleepy. What’s she going to do now?”, he looked at the doll, waved his hand around and said, “Hey, baby, wake up now.”

Joint Attention Willie had major deficits in joint attention. Occasionally he made eye contact but only in a fleeting and unsustained way. Even during peak activities of enjoyment, such as blowing bubbles, he never looked to his mother to share the event with her, nor did he make eye contact with her. He made no attempts to direct the attention of the examiner or of his mother to what he was doing or what caught his interest. If he needed something, he indicated it mechanically, e.g., when he wished the examiner to blow up the balloon, he handed it to her without sending or looking for any facial signals. When he wished to leave the room, he hung onto the door but did not otherwise attempt to communicate his wish.

Theory of Mind William readily played with the cause-and-effect toys: the Poppin’ Pals, remote control bunny and the toy phone. He rang the bell on the phone but did not try to use it symbolically, even when he was urged to do so with examples and gestures.

He lined up the stacking toys mechanically and recited the number printed on the bottom of each cup. He ignored the doll, truck and cars.

As Willie and his mother left the ADOS session, he raced down the hall towards the escalator. His mother caught him and held his hand. The examiner shouted,

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“Bye, Willie.” He turned and looked at her and shouted back, “Bye, Ann,” in a burst of reciprocal social interaction.

ADOS scores: Willie’s scores on the autism algorithm of the ADOS were better than they had been for the ADI-R but were still within the range required for the diagnosis of autism.

Observations from the ADOS Despite his having fairly good affective reciprocity on the ADOS, Willie is severely impaired in reciprocal social interaction and in theory of mind. It is not that he failed entirely to engage with others, but he did so obliquely, using echolalic phrases, rote routines and simple requests for help without accompanying eye contact, body language or gesture. He did not seek to read meaning in the facial expression or gesture of others. His play behaviors indicated that he had some familiarity with how objects work and an interest in manipulating them, but little propensity to use objects in a social way. At his age children might be expected to run the cars about on imaginary roads or feed the baby doll with the bottle. They show objects to others and expect a response; they act as if they know that others have minds which differ from their own and that they can be interested, amused or otherwise reactive in response to social overtures.

Willie’s initial greeting to the examiner, as well as his farewell response (“Bye, Ann”) were somewhat out-of-keeping with his lack of joint attention during the session. Clearly, he could show joint attention under certain circumstances. We speculate that his realization that the session was over may have led to the sudden release of his best interactional skills as he left the scene. We have noted many times that anxiety can be a potent inhibitor of affective reciprocity and joint attention. The fact that under certain circumstances Willie could engage in such behaviors may have salutary implications in terms of his being able to benefit from treatment. It doesn’t mean that he is not autistic but that his degree of autism is not profound.

There are important differences in Willie’s mother’s perceptions of him as recorded on the ADI-R and our observations on the ADOS. Ms. Jones described Willie as seriously impaired in all three domains of social communication on the ADI-R. In contrast, we found him to have good affective reciprocity, as reflected in his having normal facial expression (though he failed to direct the expression at others); normal prosody; good use of instrumental gestures (handing the balloon to be blown up again) and good greeting behaviors, both to the examiner and to his mother. In our experience this difference between the ADI-R and ADOS observations is unusual, in that the differences are usually in the opposite direction: the parents describe the child as more functional than we observe on the ADOS. This latter could be a result of the child’s failing to perform on the ADOS because of anxiety or shyness, or they might be due to the parent’s having an overly optimistic view of the child’s abilities and behaviors. In the present instance, Willie’s mother seems to have been overly pessimistic in her appreciation of his skills.

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Other Skill Domains Willie’s language skills (vocabulary and grammar) are delayed. He is echolalic when it would be expected that he use socially meaningful phrases to interact with others.

Non-verbal IQ testing indicated that Willie was functioning in the low normal range. This is a positive prognostic sign in terms of his future schooling, especially if his language skills improve.

Temperament: Willie is easy-going. He is not especially negative and intense, which will make it easier for him to fit into a classroom. He likes routines, which we attribute to his lack of social knowledge. Routines allow a person with autism to anticipate what may be expected in a social situation, and they provide a framework around which to build a response.

Willie is not hyper-responsive to auditory, visual or tactile sensations. This is good, as such difficulties can add to whatever other impairments a person may have.

Diagnosis Willie meets the diagnostic criteria for autism, but where does he fit on the autism spectrum? This is difficult to answer, given that our nosology does not currently address this issue. We suggest that a four-year-old with good affective reciprocity and beginning joint attention behaviors may be said to have a moderate degree of social communication disorder. If Willie had had good affective reciprocity and good joint attention, plus some imaginative play, then we might have considered him as being mildly impaired. We are far from having a classification of social communication that would resemble that for intellectual impairment with its mild, moderate, severe and profound degrees.

The positive family history of autism in a maternal uncle, and perhaps in a cousin, would be consistent with Willie’s diagnosis. His history of apparent normal social development prior to six months can be noted but not explained.

Treatment Willie should receive speech therapy aimed at improving his language skills. He should leave his private preschool where there are no special education teachers and enroll in a therapeutic preschool. In his home town the school district operates a preschool programs for children with developmental disabilities. It is important that Willie’s mother participate in the program since she seems to have a somewhat overly pessimistic view of the degree of his handicaps. Parents usually find it helpful to observe others with their child. The teacher may have play materials and techniques that Ms. Jones could use at home.

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If Willie were profoundly autistic and had no affective reciprocity skills, it would be necessary for him to be in a program that focused mainly on catching his attention and engaging him at a sensory-motor level, much as mothers do with their normal three- to six-month-old infants in what has been called “motherese.” Willie does not need this in that he is already responsive to others, though he has no theory of mind and little knowledge about the rules of social interactions or interest in imaginative play. His teachers, and his family, will need to focus on joint interactions which capitalize on his interest in toys such as the toy telephone, the trucks and the cars. They will need to interact with him using games involving songs, gestures, dance and gross motor activities. He is ready for what has been called intense socialpragmatic teaching, as opposed to massed discrete-trial learning (see Prizant & Wetherby, 1998, for a discussion of these contrasting approaches). The latter emphasize learning such things as words, facts and specific skills. Later, when Willie has better language and joint attention skills, he will be ready for more didactic and traditional learning approaches.

Prognosis Though we hope that Willie’s affective reciprocity skills augur well in terms of his learning language, joint attention and social knowledge, there are few studies which have followed children’s progress in terms of their earlier level of affective reciprocity and joint attention skills. Does a four-year-old with good affective reciprocity have a better prognosis than one who has poor affective reciprocity? We don’t know, although common sense would suggest that this might be so.

The system of classification outlined above is of interest to us because it fits with our notions of inborn behavioral propensities and because it is oriented to what seems to be useful clinical observations. It does not appear to stray too far from what we conceive to be the core problems of PDD and autism. We believe the concept deserves debate and further study.

References American Psychiatric Association (1980). Diagnostic and Statistical Manual of Mental Disorders (3rd Edition). Washington, D.C.: American Psychiatric Association.

American Psychiatric Association (1994). Diagnostic and Statistical Manual of Mental Disorders (4th Edition). Washington, D.C.: American Psychiatric Association.

Asperger, H. (1991). ‘Autistic psychopathology’ in childhood. In Frith Uta (Ed.), Autism an Asperger Syndrome (pp. 37–92). Canbridge: Cambridge Univerity Press.

Bailey, A., Le, C. A., Gottesman, I., Bolton, P., Simonoff, E., Yuzda, E., & Rutter, M. (1995).

Autism as a strongly genetic disorder: evidence from a British twin study. Psychol Med, 25, 63–77.

Baron-Cohen S, Tager-Flusberg, H., & Cohen, D. (1993). Understanding Other Minds. New York: Oxford University Press.

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Barr, M. W. (1898). Some notes on echolalia, with the report of an extraordinary case. Journal of Nervous and Mental Diseases, 25, 21–30.

Boutin, P., Maziade, M., Merette, C., Mondor, M., Bedard, C., & Thivierge, J. (1997). Family history of cognitive disabilities in first-degree relatives of autistic and mentally retarded children. Journal of Autism & Developmental Disorders, 27, 165–176.

Charman, T. (1997). The relationship between joint attention and pretend play in autism.

[Review] [110 refs]. Development and Psychopathology, 9, 1–16.

DiLavore, P. C., Lord, C., & Rutter, M. (1995). The pre-linguistic autism diagnostic observation schedule. Journal of Autism & Developmental Disorders, 25, 355–379.

Eisenmajer, R., Prior, M., Leekam, S., Wing, L., Gould, J., Welham, M., & Ong, B. (1996).

Comparison of clinical symptoms in autism and Asperger’s disorder. Journal of the American Academy of Child and Adolescent Psychiatry, 35, 1523–1531.

Fombonne, E., Du, M. C., Cans, C., & Grandjean, H. (1997). Autism and associated medical disorders in a French epidemiological survey. Journal of the American Academy of Child and Adolescent Psychiatry, 36, 1561–1569.

Honda, H., Shimizu, Y., Misumi, K., Niimi, M., & Ohashi, Y. (1996). Cumulative incidence and prevalence of childhood autism in children in Japan [see comments]. British Journal of Psychiatry, 169, 228–235.

Kanner, L. (1943). Autistic disturbances of affective contact. Nervous Child, 2, 217–250.

Klin, A., Volkmar, F. R., Sparrow, S. S., Cicchetti, D. V., & Rourke, B. P. (1995). Validity and neuropsychological characterization of Asperger syndrome: convergence with nonverbal learning disabilities syndrome. Journal of Child Psychology and Psychiatry, 36, 1127–1140.

Lewy, A. L. & Dawson, G. (1992). Social stimulation and joint attention in young autistic children. Journal of Abnormal Child Psychology, 20, 555–566.

Lord, C., Rutter, M., & Le, C. A. (1994). Autism Diagnostic Interview-Revised: a revised version of a diagnostic interview for caregivers of individuals with possible pervasive developmental disorders. Journal of Autism & Developmental Disorders, 24, 659–685.

Lord, C., Rutter, M., Goode, S., Heemsberen, J., Jordan, H., Mawhood, L., & Schopler, E. (1989). Autism Diagnostic Observation Schedule: a standardized observation of communicative and social behavior. Journal of Autism & Developmental Disorders 19, 185–212.

Mayes, L., Volkmar, F., Hooks, M., & Cicchetti, D. (1993). Differentiating pervasive developmental disorder not otherwise specified from autism and language disorders. Journal of Autism & Developmental Disorders, 23, 79–90.

Mundy, P. (1995). Joint attention and social-emotional approach behavior in children with autism. Development and Psychopathology, 7, 63–82.

Piven, J., Wzorek, M., Landa, R., Lainhart, J., Bolton, P., Chase, G. A., & Folstein (1994).

Personality characteristics of the parents of autistic individuals. Psychological Medicine, 24, 783–795.

Prizant, B. M. & Wetherby, A. M. (1998). Understanding the continuum of discrete-trial traditional behavioral to social-pragmatic developmental approaches in communication enhancement for young children with autism/PDD. [Review] [98 refs]. Semantics Speech Language, 19, 329–352.

Risch, N., Spiker, D., Lotspeich, L., Nouri, N., & Hinds, D. (1999). A genomic screen of autism: evidence for a multilocus etiology. American Journal of Human Genetics, 65, 493–497.

Robertson, J., Tanguay, P., L’Ecuyer, S., Sims, A., & Waltrip, C. (1999). Domains of social communication handicap in autism spectrum disorder. Journal of the American Academy of Child and Adolescent Psychiatry, 38, 738–745.

Russell, P. A., Hosie, J. A., Gray, C. D., Scott, C., Hunter, N., Banks, J. S., & Macaulay, M. C. (1998). The development of theory of mind in deaf children. Journal of Child Psychology and Psychiatry, 39, 903–910.

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Sigman, M. & Capps, L. (1997). Children with Autism - A Developmental Perspective. Harvard University Press, Cambridge.

Sorce, J., Emde, R., Campos, J., & Klinnert, M. (1985). Maternal emotional signaling: its effect on the visual cliff behavior of 1-year olds. Developmental Psychology, 21, 195–200.

Szatmari, P., Jones, M. B., Holden, J., Bryson, S., Mahoney, W., Tuff, L., MacLean, White, B., Bartolucci, G., Schutz, C., Robinson, P., & Hoult, L. (1996). High phenotypic correlations among siblings with autism and pervasive developmental disorders. American Journal of Medicine & Genetics, 67, 354–360.

Tanguay, P. E., Robertson, J., & Derrick, A. (1998). A dimensional classification of autism spectrum disorder by social communication domains. Journal of the American Academy of Child & Adolescent Psychiatry, 37, 271–277.

Van-der, G. R., Buitelaar, J., Van-den, B. E., Bezemer, M., Njio, L., & Van, E. H. (1995). A controlled multivariate chart review of multiple complex developmental disorder.

J.Am.Acad.Child Adolesc.Psychiatry, 34, 1096–1106.

Volkmar, F. R., Klin, A., Siegel, B., Szatmari, P., Lord, C., Campbell, M., Freeman, B. J., Cicchetti, D. V., Rutter, M., Kline, W., Buitelaar, J., Hattab, Y., Frombonne, E., Fuentes, J., Werry, J. S. , Stone, W. L., Kerbeshian, J., Bregman, J. D., Loveland, K. A., Szymanski, L., & Towbin, K. (1994). Field trial for autistic disorder in DSM-IV. Am J Psychiatry, 151, 1361–1367.

Yirmiya, N., Solomonica-Levi, D., Shulman, C., & Pilowsky, T. (1996). Theory of mind abilities in individuals with autism, Down syndrome, and mental retardation of unknown etiology: the role of age and intelligence. Journal of Child Psychology & Psychiatry & Allied Disciplines, 37, 1003–1014.

Mailing Address Peter E. Tanguay, M.D., Julia Robertson, M.D., Ann Derrick, A.R.N.P., M.S., C.S. Department of Psychiatry and Behavioral Sciences Division of Child and Adolescent Psychiatry University of Louisville Bingham Child Guidance Center 200 E. Chestnut St. Louisville, KY 40202 Email: ptanky@aol.com

The Core Deficit in Autism and Autism Spectrum Disorders

Nancy J. Minshew, M.D.

Abstract. This paper reviews the evidence that autism is a disorder of complex information processing with intact simple information processing. This constellation explains why these particular symptoms travel together as a syndrome, the failure of intact skills to predict higher order skills, and the common “co-occurrence” of mental retardation with autism. Complex information processing does not refer to a particular ability, but is a concept that identifies a common characteristic shared by all deficits. This concept is important because it highlights the fundamental importance to educational and behavioral treatment of simplifying tasks to reduce information processing demands. It also is equally applicable in characterizing structural and functional abnormalities of the brain, aiding in making links across levels from genes to behavior. The neural basis of this cognitive profile was investigated in eye movement studies, which demonstrated that deficits are the result of the selective failure of the most advanced levels of brain circuitry to develop.

Ever since autism was determined to be of neurobiologic origin theories regarding the core deficits and their neural origin have abounded. In the 1960’s and into the 1980’s, theories hypothesized a single primary cognitive deficit as the underlying cause of the behavior in autism. The prevalent theories proposed deficits in the acquisition of information, i.e., in elementary sensory perceptual, attentional, and memory abilities, and localized dysfunction of brainstem and hippocampus (Minshew & Payton, 1988 for review). Because phenylketonuria, fetal rubella, and tuberous sclerosis had been discovered as causes for some cases, it was also hypothesized that other diseases would ultimately be discovered that were responsible for the remaining cases. Subsequent research greatly altered these views. It is now generally but not entirely appreciated that the behavioral syndrome of autism is the result of multiple primary deficits and that these deficits involve the processing of information and are the result of the underdevelopment of the neural systems of the forebrain and not regional dysfunction (Minshew, 1997 for review). Although 5–10% of cases will be found to be the result of other diseases, the majority of cases are thought to be the result of 4–6 or more abnormal genes coding for or regulating brain development (Cook, 1998; Rutter et al, 1994). It is also likely that it will not be the

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F IGURE 1. same 4–6 genes in each case and that there will be a large number of genes that can lead to autism. The diseases that cause that 5–10% of cases are thought to produce the same neurologic and cognitive abnormalities triggering the same pathophysiology but by a different mechanism. This concept of the cause of autism is depicted in Figure 1. The gene abnormalities produce a protein or proteins that alter brain development (developmental neurobiology). The outcome of this is the structural and functional abnormalities of the brain studied by researchers. These underlie the cognitive and neurologic deficits that cause the abnormal behavior that is called autism, autism spectrum disorder, or pervasive developmental disorder.

Cognitive & Neurologic Basis of Behavior The purpose of this discussion is to consider the cognitive and neurologic basis of behavior. The importance of this issue is multi-fold. First and foremost is that clarification of the cognitive and neurologic basis of behavior empowers behavioral, pharmacologic and academic intervention. The efficacy of behavioral and pharmacologic intervention is greatly improved by understanding the motive or drive behind the behavior. Interventions can then be designed to address the cause of the behavior in the individual. Improving the understanding of the cognitive and neurologic basis of behavior also leads to improvements in diagnostic criteria, as evidenced by the evolution of the diagnostic criteria for autism in the last three versions of the Diagnostic and Statistical Manual for Mental Disorders (DSM). The improved characterization of the deficits will also stimulate the development of new assessment instruments to guide the evaluation of behavior problems. Third, the definition of the cognitive and neurologic deficits identifies the abnormalities that must be explained by the genetic and developmental neurobiologic mechanisms; these mechanisms hold the key to the development of biologic interventions aimed at restoring brain development. In order for that goal to be achieved, each of the levels involved in the cause of this disorder (see Figure 1) and their inter-relationships must be precisely and accurately defined or researchers will identify the wrong gene or wrong developmental brain mechanism.

The end result of imprecision is that we will be “on the right street but in the wrong garage” in the search for a definitive treatment for autism.

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A Neurologic Overview Neurologists typically begin their assessment of a disease process by asking where in the brain are the abnormalities and what is the mode of onset and progression. The first step is a quick orientation based on basic principles about structuralfunctional relationships in the brain. The first distinction is between gray and white matter dysfunction and cortical and subcortical dysfunction. Autism is characterized by mental retardation, deficits in language, abnormalities in complex behavior, and seizures. This constellation is classic for dysfunction of cerebral cortical gray matter.

The absence of deafness and blindness eliminates primary sensory cortex, leaving association cortex. The absence of long tract signs (alterations in tone and reflexes) eliminates white matter involvement. Thus, a brief neurologic appraisal of this clinical syndrome points to deficits in higher order cognitive abilities and to association cortex. The mode of onset is developmental.

The Pattern of Deficits & Intact Abilities The next step involves the definition of all the deficits and intact abilities and the determination of the pattern these follow. This pattern is critical because it identifies a basic or defining characteristic of the brain abnormality in autism. If correctly identified, this pattern or common denominator will explain why this cluster of symptoms occurs or “travels together.�

A number of patterns have been proposed in autism over the years. Some of these are still debated in one arena or other. The issues debated have included: a single primary cognitive-single neural system deficit versus multiple primary co-existing cognitive-multiple neural systems deficit, auditory and not visual information processing deficit, information acquisition deficit versus information processing deficit, and simple versus complex information processing deficit(s).

These issues could be addressed with a comprehensive neuropsychologic test battery. Such a battery requires individuals who have a Full Scale and Verbal IQ score of 70 or higher. Thus, this study spanned nearly 10 years because of the difficulty at the time of identifying verbal individuals with autism. The addition of the Asperger’s category and the emphasis on early intervention programs has since greatly improved the identification of autism in verbal individuals. Table 1 contains the tests and results used in the discriminant function analysis. Tables 2 and 3 provide the results of the discriminant function analysis for 33 individually age, IQ, gender, and race matched pairs of autistic and normal control adolescents and young adults.

Table 2 contains the cognitive domains that did not reveal deficits. The first two domains on the list were the attention and sensory perception domains. Neither domain demonstrated differences between autistic and control groups, and thus deficits in these areas were not the cause of autism. This does not mean that some autistic children do not have attention deficit disorder with or without hyperactivity or sensory symptoms, just that these are not causing their autism. The absence of deficits in attention, sensory perception, and associative memory means that infor-

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TABLE 1 Psychometric Data Used for Discriminant Analysis CONTROL GROUP Tests Entered into Prediction Equations Pa Attention Domain WAIS-R Digit Span .424 Serial Digit Learning-Correct Responses .648 Continuous Performance Testb .487 Letter Cancellation-Omissions .061 Number Cancellation-Omissions .342 Sensory Perception Domain Luria-Nebraska Tactile Scale: Simple Touch Errors .407 Stereognosis Errors .096 Sharp-Dull Discrimination Errors .189 Position Sense Errors .328 Finger Position Errors .535 *Halstead-Reitan: Fingertip Number Writing-Errors .019* Motor Domain Finger Tapping-Dominant Hand .805 DVMI-Total Pointsc .465 *Grooved Pegboard-Dominant Hand-Seconds .000* *Trail Making A-Time in Seconds .001* Simple Language Domain WAIS-R Vocabulary .713 K-TEA Reading Decoding .078 Controlled Oral Word Association (FAS)D .586 K-TEA Spelling .642 Woodcock Reading Mastery-Word Attack .273

AUTISTIC GROUP

M

SD

M

SD

9.88

3.81

10.52

2.46

16.52

8.17

17.42

7.91

0.34

0.62

0.23

0.66

1.09

1.63

0.45

1.00

3.27

4.03

4.39

5.38

0.29

0.55

0.17

0.48

0.46

0.59

0.21

0.42

0.88

0.80

0.58

0.72

0.00

0.00

0.08

0.41

0.67

1.27

0.46

1.02

5.38

4.30

2.79

2.84

44.27

13.78

45.19

16.24

15.42

32.43

22.18

31.69

86.73

18.30

70.67

16.03

31.52

15.81

20.45

7.99

9.45

3.02

9.70

2.26

97.48

13.60

102.79

10.19

36.00

13.31

34.00

16.18

102.58

16.93

100.91

11.50

107.24

11.55

103.52

15.53

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TABLE 1 (Continued) CONTROL GROUP Complex Language Domain *Woodcock Reading Mastery-Passage Comprehension .002* *K-TEA Reading Comprehension .001* *Test of Language Competence Metaphoric Expression .004* *Binet Verbal Absurdities-Raw Score .001* Token Test-Number Correct .690 Simple Memory Domain Paired Associate Learning-Number Correct .690 3 Word Short Term Memorye .663 Maze Recall-Correct/Incorrect .534 CVLT A List-Trial 1 Number Correct .072 Complex Memory Domain Paired-Associates-Delayed-Recall .390 CVLT A List-Long Delay .146 *Nonverbal Selective Reminding-CLTR .000* *WMS-R Logical Memory-Delayed Recall .052* *Rey-Osterrieth Figure-Delayed Recall .012* Reasoning Domain Trail Making B-time in Seconds .093 Halstead Category Test-Errors .388 Wisconsin Card Sorting Test-Perseverative Rrrors .342 *Binet Picture Absurdities-Raw Score .002* a

AUTISTIC GROUP

92.27

15.04

104.27

14.34

91.36

14.43

103.06

12.45

6.85

3.25

9.42

3.70

9.30

3.64

12.48

3.97

18.03

2.19

18.42

5.19

42.55

23.13

48.76

24.21

3.24

3.04

2.9`1

3.15

0.42

0.61

0.52

0.57

4.50

3.90

6.30

3.90

16.00

7.46

17.45

6.13

7.00

5.49

9.00

5.55

19.94

15.09

37.39

16.09

5.58

5.79

8.45

6.02

16.83

8.58

21.94

7.49

65.48

37.19

52.42

23.31

46.24

28.71

40.73

22.46

16.45

15.48

13.27

11.13

20.00

11.46

27.52

6.12

t-test results are provided to identify domains not entered into the equations but still demonstrating a significantly different performance between groups; bMean reaction time Correct Responses; cDevelopmental Test of Visual-Motor Integration; dNumber of Words; eNumber of Correct Sequences; *Tests with statistically significant results

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TABLE 2 Discriminant Function Analysis: Domains Without Deficits DOMAIN

TESTS PASSING TOLERANCE

Attention Sensory Perception Simple Language

Letter Cancellation; Number Cancellation Finger Tip Writing; Luria-Nebraska Sharp/Dull Tactile Scale item K-TEA Reading; K-TEA Spelling WRMT-R Attack; Controlled Oral Word Association CVLT Trial 1 WAIS-R Block Design

Simple Memory Visuo-Spatial

%CORRECT

KAPPA1

66.7 64.6

.33 .29

71.2

.422

65.2

.30

56.1

.12

1

Kappa below .40 indicates poor agreement beyound chance 2 Significant Kappa reflects superior performance by autistic subjects

TABLE 3 Discriminant Function Analysis1: Domains With Deficits DOMAIN

TESTS PASSING TOLERANCE

Motor Complex Language

Grooved Pegboard; Trail Making A K-TEA Reading Comprehension; Verbal Absurdities; Token Test Nonverbal Selective Reminding-Consistent Long Term Retrieval; WMS-R Story Recall-Delayed Recall; Rey-Osterrieth Figure-DelayedRecall 20 Questions; Picture Absurdities; Trail Making B

Complex Memory

Reasoning

%CORRECT

KAPPA

75.8 72.7

.52 .45

77.3

.55

75.8

.52

1

Based on 33 individually matched pairs of autistic and control subjects (Neuropsychologic Functioning in Autism: Profile of a Complex Information Processing Disorder, JINS, 3:303-316, 1997)

mation acquisition is intact. They also did not have deficits in visuospatial processing. The remaining domain, simple language, is essentially what is called formal language or the capacity to speak freely, spell, and read words or sounds without comprehension. It is notable that the autism group did significantly better than age, IQ, and gender matched controls. Thus, their formal language abilities were superior to their age and IQ. This higher expressive language ability will cause listeners to over-estimate the language abilities of autistic individuals. This will exacerbate their language comprehension deficit, which is revealed in Table 3.

Table 3 contains the domains that revealed deficits in the autism group. The first of these is the motor domain and the tests responsible were those involving complex motor actions or motor sequences as opposed to isolated motor movements such as finger tapping. This domain was included not only to complete the survey of major

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cognitive domains but also because dysfunction in higher brain regions often produces problems with complex motor sequences. This is generally called motor apraxia. This motor deficit has been found by many other investigators and motor skills deficits are now being recognized as an integral part of autism and the other disorders in this category. In young children, motor apraxia causes the problems with operating mechanical devices such as door knobs and wind up toys, whereas button pressing is not a problem. Later, motor apraxia is responsible for difficulty holding pencils, cutting with scissors, and tying shoe laces. In school age children, it is responsible for the problems with handwriting, either slowness or sloppiness. In the gross motor area, it is responsible for the lack of coordination in sports and contributes to the inability of many to ride bicycles or rollerblades. It is likely also responsible for the stilted quality to facial expressions.

The second domain revealing deficits in the autism group is that of complex language, i.e., the interpretative aspects of language. These include reading comprehension, story comprehension, comprehension of idioms and metaphors, verbal inference making, and comprehension of complex sentence structure. The latter is particularly important because it is the language of everyday life. It typically involves sentences like: before you do this, I want you to do that and then do thus and so.

These sentences place particularly heavy demands on information processing because they require processing of each segment and then a second stage of processing to determine the meaning of each bit to the next bit. Understanding the gist of such a sentence requires yet a third level of processing. A similar process occurs with the understanding of a story. The combination of superior formal language abilities and inferior comprehension produces a wide gap between the listener’s estimate of the autistic individual’s language comprehension and his or her actual comprehension. The failure to understand what the person with autism understands is a major contributor to their dysfunction in many settings.

The next affected domain is that of memory for complex information.

Complexity can result from increasing amounts of simple information or increasing inherent complexity of the information. In essence, individuals with autism have difficulty with recall of complex material, because they fail to make use of cognitive organizing strategies or to benefit from the meaning of the material. Secondly, this pertained to both visual and auditory information. The ramification of this deficit is that they remember less from the material presented to them than age and IQ matched peers; this has also been shown to reduce the amount of information they remember from recently experienced events. Thus, this memory impairment is likely to contribute to the social, language, and problem solving deficits. Knowledge of this impairment can be used to improve learning. Memory and learning can be improved by reducing the amount of material presented (smaller chunks), preprocessing the information (give the bottom line rather than exemplars that require deduction of the bottom line), and increasing the processing time. Visual presentation of information often accomplishes all of these, and likely explains why they benefit from such adaptations. Visual material is constantly present for reference and re-reading, to guide behavior.

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The last domain revealing deficits is that of abstract reasoning. This has long been known to be an area of deficit in autism. The notable finding of this study is the dissociation between intact performance on rule-learning tasks and deficits on concept formation tasks. Rule-learning tasks are ones in which there is a rule to solve the problem and the task is to discover the rule. Although the individuals in this study typically identified the rule correctly, they had difficulty changing rules when the context changed. Changing the rule to fit changing contexts adds to the information processing demands of the task, and is the basis of generalization. Concept formation tasks have no set solutions but require the individual to create one. Concept formation tasks are essentially problem solving in novel situations. This pattern is consistent with the behavior typical of autism, which is typically rule-dependent, lacking in flexibility, failing to consider the implications of context, and inability to cope with novel situations.

These were the findings by domain and the next issue was to determine the pattern or common denominator to the deficits and to the intact abilities. Some features of the pattern were relatively obvious. Information acquisition and visuospatial processing were intact. Second, there were multiple co-existing deficits in information processing abilities in both the visual and auditory modalities. The challenge was to determine what the significance was of having intact abilities within the same domains as deficits. That is, elementary motor, associative memory, formal language and rule-learning abilities were intact in the presence of deficits in skilled motor, complex memory, interpretative language, and concept formation abilities. The common denominator of the intact abilities was that they involved the more basic abilities in each domain and the deficits selectively involved the highest order abilities within the same domains. Thus, it appeared that the deficits were in abilities with the highest information processing or computational demands. The intact abilities corresponded to abilities that were deficient in the prototypic simple information processing disorder, i.e., selective language impairment. Thus, the neuropsychologic profile in high functioning autistic individuals was the predictable converse of that seen in selective language impairment, which attested to its validity. Thus, the pattern in autism was that of selective deficits in complex information processing with intact simple information processing. Complex information processing provided an explanation for why the symptoms of autism “travel� together and also for the pattern of deficits within domains.

Implications of the Pattern The implications of this pattern were several. First, it differentiates autism from general mental retardation in which both simple and complex abilities are more evenly affected. This pattern also distinguishes autism from dyslexia and the other learning disabilities. The traditional learning disabilities involve the simple abilities but spare the complex abilities, which often provide top-down compensation for the deficits. The pattern also distinguishes autism from the nonverbal learning disability syndrome, which has deficits in visuospatial and arithmetic abilities. Third, this

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pattern answers the frequently asked educational question of why they can do some things well but do other things poorly. This is not so different from dyslexia, in which there are intact and deficient skills; it is just that there is little familiarity with the cognitive pattern associated with autism.

This pattern also explains some common clinical phenomena in autism. It has long been known that as IQ scores decline across the autistic population, there is a disproportionate or selective decline in social, communication and abstraction abilities. It also explains the dissociation between IQ scores and Vineland scores, which measure adaptive behavior or real life behavior. The corollary of this pattern is that intact abilities cannot be used to predict the status of higher order abilities. And, most importantly, it explains the common co-occurrence of mental retardation and autism. Mental retardation is the predictable consequence of a progressive reduction in complex information processing abilities, i.e., the capacity to attach meaning to information.

Generalizability of the Pattern The demonstration of this pattern necessitated the assessment of verbal individuals with autism. However, this pattern is equally apparent in lower ability autistic individuals as revealed by the studies of Rapin and colleagues (1996). The particular tests that are failed will change such that lower ability autistic individuals may have deficiencies on tests that non-mentally retarded autistic individuals do well on, because their overall level of function is lower. If the concept of the pattern is retained, though, it can be applied across the ability range with ability and age appropriate tests; if the pattern is defined in terms of specific tests, then it cannot be applied to younger or lower ability subjects. Also, if only one domain is assessed or only a few tests are given within each domain, then the pattern will obviously not be discernable.

Complex Information Processing As A Construct Complex information processing is not a specific ability but a term for a class of abilities that place high computational demands on the brain. It is a conceptual construct. Deficits in specific abilities such as theory of mind and executive function that are commonly discussed in connection with autism all fall under this general construct. The value of this construct is that it emphasizes the need to evaluate tasks autistic individuals cannot do in terms of the computational demands on the brain. This approach provides guidelines for modifying the demands of tasks that individuals are unable to do. However, the scientific value is that this term is also used in the neurophysiology to characterize the late or cognitive potentials. This construct also makes it possible to think in terms of developmental processes in the brain involved in the emergence of the intricate circuitry of the forebrain that underlies these abilities. Thus,

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the complex information processing construct makes it easy to relate or link findings across several levels of the pathophysiology of autism. Such links are critical if the cause of autism is to be understood.

Neural Basis of Behavior A second issue of great importance in understanding autism is the demonstration of the brain abnormalities that are responsible for the cognitive deficits underlying behavior. There have been a great many theories, many of them very appealing, but few with any supporting data. One particular debate has been over the cognitive and neural basis of the abnormal shifting attention behavior in autism.

Courchesne and colleagues have contended that this deficit relates to abnormalities at the attentional level and dysfunction of the cerebellum. However, Ozonoff and many others have demonstrated deficits in the executive control over attention and intact basic attentional abilities. Executive abilities reside in the frontal lobes of the brain, not the cerebellum.

Resolution of this debate depends on decomposing tasks into their component cognitive processes and examining each individually. This has been done using three different methods, all with the same results. Ozonoff et al (1994) decomposed the Wisconsin Card Sorting Test into its individual components and found that autistic individuals had no difficulty with simple shifts of attention but did have trouble with the cognitive abilities of flexibility and with inhibition of prepotent responses, which are related to frontal lobe function. In a detailed examination of shifts of attention, Pasavalqua et al (1998) found no deficits in shifting attention abilities in autism but did find deficits in the executive control of attention. In a review of attention research in autism, Burack and colleagues (1997) reported that deficits in shifting attention or orienting pertained to difficulties processing the directional cues and not the basic capacity for shifting attention.

Saccadic eye movements provide an excellent method for addressing these controversies. Visually guided saccades involve simple shifts of attention which reflect cerebellar input. Volitional saccades to antisaccade and oculomotor delayed response tasks assess the executive control over attention and are subserved by the frontal lobes. The value of these methods is that localization is exceedingly well documented, the tasks are similar to real life behavior, and the data are a rigorous measure of the abilities and brain regions assessed. In the first such study in autism, deficits were documented in high functioning autistic individuals on the volitional saccade tasks but no deficits were found on the visually guided saccade task (Minshew, Luna, & Sweeney, 1999). This study provided rigorous evidence that the difficulty in life with shifting attention in autism relates to deficits in higher order control over attention by higher brain regions and not to basic deficits in attention subserved by the cerebellum. These data are also important for having demonstrated that there are selective abnormalities in the highest order circuitry of the brain and that lower levels of circuitry are intact.

This pattern is analogous to that seen in the study of the neuropsychologic profile.

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In summary, these studies provide evidence that autism is a selective disorder of complex information processing abilities with intact simple information processing abilities. The common denominator of deficits in autism is the high demands placed on information processing or computation by the brain. The complex information processing construct explains why these particular symptoms travel together as a syndrome, the failure of IQ scores and intact abilities to predict the status of higher order abilities, the common co-occurrence of mental retardation in autism, and the difference between autism and general mental retardation. The validity of this characterization of cognitive functioning in autism is supported by its reciprocal relationship with the neuropsychologic profile described for the prototypic simple information processing disorder. The presence of this same dissociation between deficient complex and intact simple abilities in the motor domain further attests to the validity of this construct. The relationship of deficits in autism to their computational demands on the brain is helpful clinically in understanding and analyzing behavioral and academic difficulties.

The saccadic eye movement studies investigating the neural basis of cognition and behavior in autism provide evidence that these difficulties are the result of the selective failure of the most advanced levels of brain circuitry to develop. The findings of these studies, like the findings using other methods, indicate that difficulties with shifting focus of attention relate to executive dysfunction and the frontal lobes, and not to a deficit in the basic attentional capacity to shift attention.

The complex information processing construct does not refer to a particular ability but is a construct that identifies a common characteristic shared by all the deficits in autism. In addition to the contributions it makes to the clinical understanding of this disorder, this construct also provides a connection to brain function and structure. These links across levels are key to defining the sequence between genes and behavior that will empower all intervention.

References Burack, J. A., Enns, J. T., Stauder, J. E. A., Mottron, L., Randolph, B. (1997). Attention and autism: behavioral and electrophysiological evidence. In: Cohen D. J., Volkmar, F. R., eds. Handbook of autism and pervasive developmental disorders. New York: John Wiley & Sons, 226–247.

Boucher, J. (1981). Memory for recent events in autistic children. Journal of Autism and Developmental Disorders, 11, 293–302.

Cook, E. H., Jr. (1998). Genetics of autism. Mental Retardation and Developmental Disabilities Research Reviews, 4, 113–120.

Minshew, N. J. (1997). Autism & the pervasive developmental disorders: the clinical syndrome. In Behavior Belongs in the Brain: Neurobehavioral Syndromes, B. K. Shapiro, P. J. Accardo, & A. J. Capute, eds. pp. 49–68, York Press, Baltimore, Maryland.

Minshew, N. J., Payton, J. B. (1988). New perspectives in autism: Part 1: The clinical spectrum of infantile autism. Current Problems in Pediatrics, 18:561–610.

Minshew, N. J., Luna, B., & Sweeney, J. A. (1999). Oculomotor evidence for neocortical systems but not cerebellar dysfunction in autism. Neurology, 52:917–922.

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Ozonoff, S., Strayer, D. L., McMahon, W. M., et al. (1994). Executive function abilities in autism and Tourette syndrome: An information processing approach. Journal of Child Psychology and Psychiatry, 32:1081–1105.

Pascualvaca, D. M., Fantie, B. D., Papgeogiou, M., Mirsky, A. F. (1998). Attentional capacities in children with autism: is there a general deficit in shifting focus? Journal of Autism and Developmental Disorders, 28:467–478.

Rapin, I. (1996). Preschool children with inadequate communication: Developmental language disorder, autism, low IQ. London: Mac Keith Press.

Rutter, M., Bailey, A., Bolton, P. & Le Couteur, A. (1994). Autism and known medical conditions: myth and substance. Journal of Child Psychology and Psychiatry, 35, 311–322.

Mailing Address Nancy J. Minshew, M.D. Associate Professor of Psychiatry and Neurology University of Pittsburgh School of Medicine Department of Psychiatry Western Psychiatric Institute and Clinic 3811 O’Hara Street Suite 430 Bellefield Towers Bldg.

Pittsburgh, Pennsylvania 15213 minshewnj@msx.upmc.edu

Neural Mechanisms In Autism

Andrew W. Zimmerman, M.D. and Barry Gordon, M.D., Ph.D.

Abstract. Autism is a heterogeneous disorder and can be associated with many coexisting genetic and acquired diagnoses. The underlying defects that lead to it continue to elude us.

Various autistic syndromes share disruptions in several neural pathways that develop and function at different levels of organization within the central nervous system. Brain development proceeds through cascades of different processes that tend to rely on and interact with previously established ones. While certain degrees of individuality in maturation may occur normally, there are critical thresholds for disturbing orderly, synchronized development. As a result of evolution, the increased complexity of the human brain may have increased its vulnerability to fetomaternal immune reactions, potentially resulting in incompatibility that disturbs recently developed functions, such as language and social skills.

Artificial neural networks, as in computational modeling, can be a useful theoretical approach to explain how under- or over-innervated networks in persons with autism may affect their abilities to discriminate and generalize, as one sees in autistic regression.

Neural Mechanisms in Autism1 Currently there is no reliable evidence as to exactly what are the neural bases for autism. There are no accepted genetic markers, even though there are several candidates (Ingram JL, et al., 2000, Bailey, Palferman, Harvey, & Le Couteur, 1998; Folstein, Bisson, Santangelo, & Piven, 1998; Szatmari, Zwaigenbaum, & MacLean, 1998). It is also increasingly clear that autism is a heterogeneous disorder, even if it is genetic. There are no objective tests in vivo that are specific for the condition. There have been no structural, metabolic, or neuropathologic abnormalities that have been reliably linked to autistic features. There is no accepted animal model of the condition, although infant monkeys with selective brain lesions (Bachevalier, 1991; Bachevalier & Merjanian, 1994) show behavioral features suggestive of autism.

Acknowledgments: Preparation by Andrew W. Zimmerman was supported in part by the National Alliance for Autism Research and the East Tennessee Chapter, Autism Society of America. Barry Gordon was supported in part by the New York Community Trust—Hodgson Fund, the Hodgson Family, the Benjamin A. Miller Family Fund, and by gifts made in memory of Bernard Gordon.

The authors thank Martha Bridge Denckla, M.D., for her helpful discussions regarding neural pathways in autism, and James Marcum, who contributed to the artwork (Figure 1). Susan L. Connors, M.D., gave helpful advice.

1 Condensed with permission from a chapter in Pasguale Accardo (Ed.), Autism: Clinical and research issues. Towson, MD: York Press. (2000).

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F IGURE 1. Putative neural networks in autism. Solid arrows indicate direction of neual transmission, based on current information; large striped arrow depicts uncertain cerebellar effects. Large scissors depict cellular “lesions” in important structures that might contribute to network dysfunction or a “disconnection syndrome.” Small scissors show potential sites for disconnection within networks and an example of “functional’ (correct: globus pallidus to thalamus) or “dysfunctional” (aberrant) repair that might occur from bypassing the globus pallidus. In schizophrenia, a disconnection is thought to occur between the dorsolateral prefrontal area and the anterior cingulate cortex (Benes, F. M. 1993. Relationship of cingulate cortex to schizophrenia.

In The Neurobiology of Cingulate Cortex and Limbic Thalamus, eds. B. A. Vogt and M. Gabriel. Boston: Birkhauser.).

Neurobiologic Studies Although no neuropathologic features have been found yet to be characteristic of autism, a number of abnormalities have been reported. Bauman and Kemper (1994) found consistent neuronal changes (“too many, too small”) in the hippocampus, amygdala, and other areas of the limbic system, as well as decreased Purkinje cells in the lateral cerebellum. More recently, Bailey, et. al., (1998) reported cerebellar, neocortical, and olivary (but not limbic) changes. These findings may reflect “developmental curtailment” of the cellular connections in the developing cortex (neuropil) that affects information processing and representational memory (in the hippocampal complex); recognition of facial gestures and cross-modal memory (amygdala);

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and shifting attention, language processing, and motor function (cerebellum). In spite of the limitations of traditional methods inherent in light microscopic studies of autism so far (Rapin & Katzman, 1998), and the paucity of postmortem tissue available for study, these studies have fostered a new era in neurobiological research in autism by other investigators who are using recently developed genetic, neurochemical, and morphological techniques.

Diverse Causes for Similar Defects of “Higher Cortical Functions�

Autism can be caused by a number of different insults and etiologies. These causes may be as diverse as viral infections, dysmorphic syndromes, or genetic abnormalities of intracellular metabolism. In any individual, these would produce a fairly unique pattern at the neural level, even though their behavioral outcomes are more similar.

There are some aspects of function in which it is possible to make a fairly direct correlation to neuroanatomy, particularly in the fully developed organism. The elementary sensory and motor systems are the best examples. However, higher cognitive abilities, by their very nature, are the product of a number of different underlying mental functions. Each of these functions may have very complex relationships to neural structures. These mental functions may not even be products of structures per se, as much as of their internal dynamics or the dynamics of other systems and structures. Moreover, many of the functions considered to be higher abilities are actually chains of abilities that unfold over time. The higher functions considered to be most important were unlikely to have sprung up full-blown in phylogeny. More likely, they have been cobbled together out of refined and rearranged combinations of other functions. Therefore, such functions may not have very direct brain correlations. The situation is even more complicated in the case of developmental disorders. Normal mental development proceeds through a cascade of many different processes, which tend to bootstrap each other. The interruption, or just simple delay, in any part of this sequence, can and often does have major effects on the final components and their assembly into a functional whole.

The genetic deficits of autism may be expressed in peculiar patterns that can be related to neurobiologic organization, but not to the functional organization of the nervous system. They also may be expressed at different times in the developing nervous system. Some of these effects may be visible at the time they occur, whereas some may take a long period of subsequent development to be expressed. It is still a reasonable strategy to look as early in development as possible for clues to the neurobiologic problems. A recent example is the study by Teitelbaum, Teitelbaum, Nye, Fryman, & Maurer (1998), which showed that movement disorders could be retrospectively detected in autistic children as early as ages 4 to 6 months. Of particular relevance to the issues raised here is that the movement disorders were expressed in different movements, and in different ways, among the different children.

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Neural Networks Neuropathological findings in the limbic system, cerebellum, and frontal cortex in autism suggest that disorders in these structures may be important contributors to the autism deficit. Variations in clinical expression among autism spectrum disorders may relate to different types of effects-as well as their distribution-in related structures, such as the basal ganglia (important for motor planning) and prefrontal cortex (motivation, executive functions) (see Figure 1). These regions may be dysfunctional by themselves (e.g., following closed-head injury, stroke, or encephalitis) or may be come disconnected from their interactive partners within networks due to their failure to develop, modify, or prune their connections during the development of the neuropil (Zilbovicius et. al., 1995). For example, the basal ganglia (caudate and globus pallidus) and thalamus are essential subcortical integrating way-stations in networks with prefrontal and anterior cingulate cortex. Abnormalities in subcortical neurotransmission to or from the prefrontal cortex are likely to contribute to executive dysfunction, disinhibition and irritability, and apathy and inertia (Denckla & Reiss, 1997).

The capacity for repair of, or compensation for, brain lesions (plasticity) is maximal during the early years of development ( Jacobson, 1991). Therapeutic programs in autism may take advantage of this potential for repair (Greenspan & Wieder, 1997; Lovaas, 1987). Although its biological basis is poorly understood, clinically effective repair may depend on the regulation of multiple neurotransmitters, growth, and other trophic factors in the brain while training programs are taking place. (Repair also may occur to some degree with or without training.) Compensation for defective way-station processes (e.g., hippocampal or cerebellar), or disconnection within networks, probably depends on correct forms of rerouting (“functional plasticity,” see Fig. 1). Plasticity is functional if it compensates for a disconnection between waystations (e.g., between globus pallidus and thalamus). “Dysfunctional plasticity” (e.g., from caudate to thalamus) may reduce efficiency of the repair or even negate its effects if the new route bypasses critical parts of the network (e.g., globus pallidus).

Evolution, the Immune System and Fetal-Maternal Interaction Several concepts from human evolution may offer alternative insights into the origins of autism. Human language functions probably emerged in the past 50–100,000 years, although their neural substrates were evolving for at least several million years before that (Pinker, S. J., 1995; Smith & Szathmáry, 1999).

Chimpanzees, our closest primate relatives from whom our primate ancestors diverged 4 to 10 million years ago, are able to perceive and respond to human languages up to the level of human 3 year-olds. However, they are unable to use grammar or complex constructions that children begin to acquire rapidly by this age.

Despite their capacity for communication, chimpanzees do not approach humans in their ability to understand the mental states of others through language (Tomasello,

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1999). Although non-human primates’ social skills and organization are advanced compared to other mammals, humans are (arguably) advanced by comparison. The evolution of brain networks (and their interactions) that made possible the expansion of language (with syntax) and social skills, as well as mental capacity, in humans most likely have been cobbled together over millions of years (Calvin and Bickerton, 2000). However, the pace of their evolution seems to have increased rapidly with the appearance of art, communication and tool use in the past 50,000 years. These networks were certainly well developed by the advent of agriculture (10,000 years) and recorded history (5,000 years ago; Diamond, 1992).

Two important driving forces behind evolution of the brain and its fourfold increase in cortical surface area, in humans compared to chimpanzees, are likely to include both immune adaptation and mate selection. Bacteria, parasites and viruses are still the most abundant (and rapidly evolving) organisms on Earth. Despite our multicellular complexity, humans are slowly evolving and static in comparison to these infectious organisms (Allman, 1999). Our ancestors survived in this immunologically challenging environment because they developed complex immune systems that were able to react effectively, by both innate and adaptive immune mechanisms, to a wide array of organisms. This immune diversity continues today to be directed, in large part, by the major histocompatibility complex (MHC; represented by human lymphocyte antigens or HLA, individual tissue types that are represented on most cell surfaces), the most polymorphic of our genes, located on the short arm of chromosome 6 and expressed in most of our cell types. Along with their obvious benefits for diversifying our immune reactivity, a mismatch of HLA types also leads us to readily reject “foreign” tissue transplants. One’s HLA types must be carefully matched in order for an organ transplant to survive (an identical twin or a sibling match is usually most successful). An enduring mystery, however, is that during pregnancy, the developing fetus itself is able to survive as a “foreign tissue transplant” to the mother (due to the fetus’s different HLA types that are inherited from the father). Two possible explanations for this paradoxical immune tolerance include decreased expression of HLA types by the placenta, and the appearance of HLA-G, a special type of HLA produced by the fetus and placenta, that serves to down-regulate maternal immune responses to the “fetal transplant” (Hunt, et al., 2000). In addition to fetal reactions, maternal responses may include antibodies against the fetus (Warren, et al.,1990), as well as interactions of maternal genes with dietary and environmental factors that act as teratogens to the fetal brain ( Johnson, 1999).

HLA types are also important for mate selection, a form of natural selection that drives evolution. They may function to increase dissimilarity between mates through mutual attraction to olfactory cues for differing HLA types, and thereby increase immune diversity within couples and survivability among their children. In humans, mate choice appears to be mediated by HLA (Ober, et al., 1997), although pheromones have not been demonstrated to mediate the process. Darwin (1871) found that mate selection is an important epigenetic mechanism for natural selection that rapidly amplifies traits over time, such as the peacock’s tail and the finch’s

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beak. Miller (2000) has suggested that the human drive to select mates may underlie many of our gender-related behaviors as well as our enthusiasm for the arts, creativity and cultural development. Mate selection and HLA diversity, therefore, may be driving (and perhaps, accelerating) our recent (and continuing) evolution of brain networks that support our most “human” attributes (language and social skills). By extension, variants of HLA (Warren, et al., 1996) and other fetal-maternal epigenetic mechanisms, as evolutionary adaptations, also may give rise to autism in human beings. Autism, in its various forms, can therefore be seen as expressions of human evolution.

Several prenatal complications of pregnancy appear more commonly, in retrospect, when the child later develops autism. These findings have not been well defined or explained, and may also occur in other neurodevelopmental disorders (Nelson, 1991). The increasing incidence of autism with late birth order in some families (Tsai & Stewart, 1983) may reflect maternal-fetal immune incompatibility and production of maternal antibodies (to paternal antigens and against the fetus). In addition, an increased incidence of autoimmune disorders in the mothers and close relatives of autistic children suggests that abnormal immune reactivity may predispose the fetus to maternal “toxic” immune effects (Comi, et al., 1999). HLA associations occur commonly in autoimmune disorders, and if confirmed in children with autism (or their mothers), may signify that both types of disorders may share genetic mechanisms related to HLA or neighboring genes. Maternal reactivity may result from paternal (as well as maternal) genetic components through the fetus, which has been described recently in maternal preeclampsia (Esplin, et al., 2001).

Maternal-fetal immune interactions might produce effects in the developing human brain that are novel to humans, and specific to unique networks that are “recently evolving.” HLA antigens may specify network formation during critical periods of brain development. Based on the recent work of Shatz (Huh, et al., 2000), the MHC antigens in mice are important for cellular contact recognition (and activity-dependent synaptic plasticity) in the developing visual system, as well as other areas: they are especially rich in the limbic system and may be tied to the activity of glutamate and other neurotransmitters in the developing brain. If it can be shown that human brain networks that have recently evolved depend upon the expression of specific HLA types, then the expression of these antigens on cell surfaces might be inappropriately down-regulated due to maternal-fetal intolerance during critical periods of their development in utero. Such reactions would initiate a cascade of downstream effects that would continue postnatally, and selectively disrupt “recently evolved” networks and functions that support language and social development.

Fundamental Cognitive And Behavioral Deficits In Autism There have been a number of attempts to tease apart the cognitive and behavioral deficits that occur in autism, and to hopefully identify some as more funda-

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mental than others (for reviews, see Bailey, Phillips & Rutter, 1996; Happe & Frith, 1996; Rapin 1997; Rumsey, 1996; and Litrownik & McInnis, 1982). A recent example has been attention to the lack of theory of mind in autism. Theory of mind was the term used by Premak & Woodruff (1978) to describe an individual’s understanding of the motives, knowledge and beliefs of others. Frith, Baron-Cohen and others (BaronCohen, 1995; Baron-Cohen & Swettenham, 1997; Frith & Happe, 1994) have noted that autistic individuals do not seem to have such understanding, nor are they able to develop it. Consequently, these authors have posited that a deficit in the primitive functions that form the basis for having theory of mind could be a major cause of the difficulties in autism. However, just what constitutes a theory of mind, who has it, and whether it is truly impaired in autism has been debated (see, for example, Povinelli & Preuss, 1995).

A different, perhaps more fundamental deficit should be entertained as being present in many persons with autism, particularly if they are low-functioning: a deficit in the ability to selectively manipulate sensory representations, concepts, and thoughts themselves (although these may also be deficient). In basic terms, this is a problem with the ability to imagine. However, it is not a deficit in simple visual imagery; there is self- reported evidence that high-functioning persons with autism not only have visual imaginations but rely upon them (Grandin, 1997). Instead, what is referred to here is the ability to select elements of mental states and manipulate them. Normally, humans are able to focus on different aspects of an object or experience, and even seem to break these aspects away from the original experience and manipulate them separately. A person can see a red cup and separate out its redness from its shape. Persons with autism, however, are notorious for not being able to do this. They are notorious for context-dependence and for apparently focusing on the “wrong� features of everyday objects.

There is some evidence that, in normal individuals, this ability to select features from otherwise unitary representations is dependent upon the prefrontal cortex (Thompson-Schill, Esposito, Aguirre, & Farrah, 1997). A deficit in such functions would certainly fit with many of the other noted behavioral characteristics or persons with autism: their rigidity, repetitive behavior, and perseveration; their lack of symbolic play; and more elaborately, a theory of mind. (Deacon (1997) and others have suggested that this type of mental manipulation, which is essentially symbolic, is one of the important mental prerequisites of humanness.

Within the subgroups of autism, much still needs to be explained. Each of the sub-groups (described in Zimmerman & Gordon, 2000) is known to be associated with at least two paradoxes. One is that autistic individuals often have disproportionate mental abilities and skills, in addition to their obvious disabilities. The other paradox is that, despite the clear cognitive and behavioral abnormalities in each of the autistic categories, the underlying neural pathology still seems to resist a consistent description. Going back and reclassifying the pathology of autism into clinical subcategories does not yet result in a more coherent picture. According to published studies, even within these clinical subcategories, reported abnormalities may be present in some individuals and absent (or different) in others. The inability

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to find beneficial effects of any categorization scheme may simply reflect how conflated these categories have been in reported studies, and in the impossibility of reconstructing them from the published accounts. It is also very possible that some heterogencity-in mental functions as well as in neuropathology-will prove to be a fundamental characteristic of each category of autism.

Behavioral Heterogeneity One of the most striking features of autism is that it is often accompanied by relative strengths in some areas of cognition, in addition to disabilities in others (Happe & Frith, 1996; O’Connor & Hermelin, 1989). Such patterns are well known in developmental disorders. In Williams syndrome, speech, surface language abilities, and (at times) musical ability, are typically far superior to visual-spatial abilities and to general cognitive abilities (Capirci, Sabbadini & Volterra, 1996; Tager-Flusberg, Boshart, & Baron-Cohen, 1998). Many of the developmental syndromes of mental retardation have relative preservation of visual-perceptual ability (Pulsifer, 1996). However, supranormal islands of ability are much rarer in other conditions compared to autism spectrum disorders (Happe & Frith, 1996). It has been claimed that 10% of the autistic population has “special abilities” (Rimland & Fein, 1988). The supranormal skills that have been described in both autistics and in individuals with other diagnoses include lightning calculation, calendar skills, list learning (Mottron, Belleville, Stip, & Morasse, 1998), visual memory, hyperlexia, puzzle construction, drawing ability, musical memory, and playing by ear and improvisation. (For more complete lists, see Happe & Frith, 1996; O’Connor & Hermelin, 1989.) Regardless of the exact proportion having such abilities, the overabundance of such skills demands some explanation and might even shed some light on the nature and neurobiology of autism itself, as Frith (1989), O’Connor (1989), and others have suggested.

Not all of the apparently superior skills that have been reported are difficult to explain. Restricted attentional focus, repetitiveness, and the lack of competing thoughts or abilities (Frith, 1989), can certainly account for many apparent abilities. A recent study of recent atypical memory abilities in one individual (Mottron et. al., 1998) is perhaps an example of how superior performance in one area may be accounted for, in some instances, by actual cognitive deficiencies in other areas.

However, there are other examples of apparently superior ability that seem to arise spontaneously (e.g., Selfe, 1977) and do not seem to be easily explained by the absence of normal mental impediments. These often seem to involve implicit learning of rules and patterns (Hermelin & O’Connor, 1986). They also often seem to be remarkable circumscribed. An individual who can do lightning calculations of dates may not even be able to multiply numbers (Happe & Frith, 1996). It may not be unreasonable to ask that any unified account of the neural basis for autism account for these abilities as well as autism’s documented disabilities.

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Neural Network Theories It may be possible to unify both the behavioral herterogeneity-the abnormalities and the supernormalities-as well as the possible neural heterogeneity. To do so requires a digression into neural networks theories. (It should be noted that Cohen, 1994 raised many of the same hypotheses proposed here.) Neural networks theories of cognitive processes posit that many mental operations are carried out through successive sets (layers) of neuronal processing elements. (For a brief overview, see Gordon, 1997.) With the proper input and training criteria, and the proper learning of rules, such networks have proven to be extremely adept at embodying rules and patterns that are implicit in the data presented to them. However, the accuracy of this extraction is very dependent on the number of processing elements in the active learning layer (Baum & Hausler, 1989). If there are too few elements then the network does not learn with very good accuracy: it, in fact, tends to over-generalize. If there are too many elements, then the network learns each specific situation presented to it and doesn’t generalize enough. If some number of working elements leads to adequate performance, a somewhat greater number can result in truly superior performance in learning implicit rules and patterns, as long as it avoids becoming too specific.

This observation might be tied in to normal development, and to the abnormal development(s) that occur in autism, in the following way: the normal development of higher cerebral functions in a child’s cortex appears to be driven by at least two major influences. One is predetermined connections; the other is activity and use.

It has often been noted that the number of genes coding for the brain and neural tissue (~50,000) are insufficient to specify all the connections of the mature brain.

Thus, the development of these connections must be guided in part by experience.

Edelman (1987) and Intrator and Edelman (1997) have suggested that whether an uncommitted area develops connections with one region or another is based on the outcome of a competition for use. The developing child’s brain normally has several primary sensory inputs, including vision, audition, and touch. These inputs are hardwired and fairly compelling. Such sensory inputs will do all they can to recruit whatever upstream neuronal processing resources are not yet committed.

Normally, the multiple influences on a child lead to a balance of forces, with the normal balance of lower and higher processing abilities (and neuroanatomic maps) as a result. The amount of neural tissue that is devoted to each higher function therefore represents a tradeoff between several forces: an attempt to optimize processing, the practical limits on optimization (because of lack of enough experience and training time), and competition with other functions for those same neuronal processing elements.

What if a developing brain had all those same forces at work, but for some reason some processing systems were impaired or delayed in their development?

What if the systems in question were those involved in speech perception and speech production? Specific genetic deficits in speech production have been tentatively identified. It is conceivable that there are other deficits or combinations of

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deficits with more widespread effects on both speech production and speech perception. If the systems related to speech perception and speech production were developmentally impaired, then many higher abilities dependent upon appropriate auditory input and output would never develop properly. Whatever cerebral tissue would have been devoted to those higher functions would then be free to be incorporated into other processes (assuming the tissue itself was not too badly affected by the same defects). If vision were intact, then visual-related abilities would be expected to appropriate extra cerebral tissue. The result would be a child’s brain that was not capable of all of the normal functions of a child, but that was capable of performing some functions superlatively well. The brain would not be capable of those abilities that are related to speech and language capability, such as a longterm component of working memory (the part normally dependent upon an articulatory loop), and perhaps even such higher functions as the “inner voice” aspects of consciousness. It would, however, be extraordinarily good at wordless visual perception and analysis. Neuropathologically, such a brain might have only a few, apparently nonspecific, abnormalities. It would not have to have fewer neurons than normal. Autistic brains are, if anything, average or larger-than-average in size (Courchesne, Muller & Saitoh, 1999; Lainhart et al., 1997). It might be possible to detect additional territory devoted to visual-related functions, but perhaps not with current behavioral tasks and instrumentation. Autism may therefore represent disorders of activity-dependent plasticity during brain development that occur at several different levels: gene, synapse, neuron, network, and neuronal group.

Hypothesis of Activity-Dependent Plasticity In broader outline, the hypothesis is this: Either because of genetics or external influences, several regions or neuronal networks of the developing brain are damaged or delayed in their development. Regions involved in social connection and those involved in speech and language seem to be particularly susceptible. (It is not too speculative to imagine that they have a functional linkage and perhaps, therefore, a genetic one as well.) There are two consequences of this primary pathology.

Functions that require these inputs cannot develop fully. Functions that were not dependent upon these impaired routes can develop normally, and might well develop supranormally. They would develop supranormally if these functions were normally kept constrained by a competition for neural resources from the functions that were now impaired (with the competition being either in functional space or perhaps just through simple anatomic proximity).

This hypothesis has several testable consequences. There will be forme frustes of autistic disorder—in speech and language and in socialization—representing less extreme forms of the autistic pathology. These types of deficits should be familial.

The domino effect on functions should be predictable after research establishes a better understanding of what functions depend upon other functions, in both

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development and in operation. Finally it should be possible to identify some in vivo correlates of the extra neural tissue that has been adopted for processing (e.g., vision) in these individuals.

This hypothesis does not explain the primary cause or causes of the deficits. It would, however, help to explain why persons with autism tend to have the patterns of disabilities and abilities that they do, and why their neuropathology (in the broadest sense) has been so variable from individual to individual. It might also suggest ways in which functional retraining can try to ameliorate some of their disabilities or take advantage of their particular strengths.

Conclusion The next stages of investigation of neural mechanisms in autism spectrum disorders should first focus on the selection of subjects and clinical definition of subsets.

Although well-studied animal models are desirable, high-functioning subjects with autism are more likely to reveal the essential abnormalities in this very “human” disorder. Multiple investigative techniques, from cellular to neurochemical to cognitive neurophysiology, and quantitative and functional neuroimaging, will help to define the neural networks that contribute to autism.

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