Re-envisioning Neuro-Optometry by Brain Injury Professional

BRAIN INJURY professional vol. 15 issue 3

Re-envisioning

Neuro-Optometry

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Evaluations

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vol. 15 issue 3

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Editor in Chief Message Guest Editor’s Message BIP Expert Interview Glossary: Ophthalmic Terms

features

Evaluation and Management of Oculomotor, Trochlear and Abducens Paresis/Palsy Curtis Baxstrom, OD, MA • Thomas Lenart, MD Eugene May, MD

Efferent-Based Oculomotor Dysfunctions in Chronic Mild Traumatic Brain Injury (mTBI): Diagnostic and Treatment Aspects Kenneth J. Ciuffreda, OD, PhD • Jose E. Capo-Aponte, OD, PhD Angela Peddle, OD • Naveen K. Yadav, BS Optom, MS, PhD

Neuro-Optometric Rehabilitation for the SensoryTriggered Anomalies Associated with Mild Traumatic Brain Injury Barry Tannen, OD • Allen Cohen, OD

Evaluation and Management of Visual Processing, Visual Attention, and Visual Field Deficits in Individuals with Brain Injuries Derek Tong, OD • Marcel Ponton, PhD • Wei-Ching Lee, MD Tonya Umbel, OD • DeAnn Fitzgerald, OD

Brain Injury Professional is a membership benefit of the North American Brain Injury Society and the International Brain Injury Association

NORTH AMERICAN BRAIN INJURY SOCIETY CHAIRMAN Mariusz Ziejewski, PhD VICE CHAIR Debra Braunling-McMorrow, PhD IMMEDIATE PAST CHAIR Ronald C. Savage, EdD TREASURER Bruce H. Stern, Esq. FAMILY LIAISON Skye MacQueen EXECUTIVE DIRECTOR/ADMINISTRATION Margaret J. Roberts EXECUTIVE DIRECTOR/OPERATIONS J. Charles Haynes, JD MARKETING MANAGER Megan Bell-Johnston GRAPHIC DESIGNER Kristin Odom BRAIN INJURY PROFESSIONAL PUBLISHER J. Charles Haynes, JD EDITOR IN CHIEF Debra Braunling-McMorrow, PhD - USA EDITOR IN CHIEF Nathan Zasler, MD - USA ASSOCIATE EDITOR Juan Arango-Lasprilla, PhD – Spain DESIGN AND LAYOUT Kristin Odom ADVERTISING SALES Megan Bell-Johnston EDITORIAL ADVISORY BOARD Nada Andelic, MD - Norway Philippe Azouvi, MD, PhD - France Mark Bayley, MD - Canada Lucia Braga, PhD - Brazil Ross Bullock, MD, PhD - USA Fofi Constantinidou, PhD, CCC-SLP, CBIS - USA Gordana Devecerski, MD, PhD - Serbia Sung Ho Jang, MD - Republic of Korea Cindy Ivanhoe, MD - USA Inga Koerte, MD, PhD - USA Brad Kurowski, MD, MS - USA Jianan Li, MD, PhD - China Christine MacDonell, FACRM - USA Calixto Machado, MD, PhD - Cuba Barbara O’Connell, OTR, MBA - Ireland Lisandro Olmos, MD - Argentina Ronald Savage, EdD - USA Caroline Schnakers, PhD - USA Olga Svestkova, MD, PhD - Czech Republic Lynne Turner-Stokes, MD - England Olli Tenovuo, MD, PhD - Finland Asha Vas, PhD, OTR - USA Walter Videtta, MD – Argentina Thomas Watanabe, MD – USA Alan Weintraub, MD - USA Sabahat Wasti, MD - Abu Dhabi, UAE Gavin Williams, PhD, FACP - Australia Hal Wortzel, MD - USA Mariusz Ziejewski, PhD - USA EDITORIAL INQUIRIES Managing Editor Brain Injury Professional PO Box 131401, Houston, TX 77219-1401 Tel 713.526.6900 Email: mbell@hdipub.com Website: www.nabis.org ADVERTISING INQUIRIES Megan Bell-Johnston Brain Injury Professional HDI Publishers PO Box 131401, Houston, TX 77219-1401 Tel 713.526.6900 Email: mbell@internationalbrain.org NATIONAL OFFICE North American Brain Injury Society PO Box 1804, Alexandria, VA 22313 Tel 703.960.6500 / Fax 703.960.6603 Website: www.nabis.org ISSN 2375-5210 Brain Injury Professional is a quarterly publication published jointly by the North American Brain Injury Society and HDI Publishers. © 2018 NABIS/HDI Publishers. All rights reserved. No part of this publication may be reproduced in whole or in part in any way without the written permission from the publisher. For reprint requests, please contact, Managing Editor, Brain Injury Professional, PO Box 131401, Houston, TX 77219-1400, Tel 713.526.6900, Fax 713.526.7787, e-mail mbell@hdipub.com.

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from the

editor in chief

I am very excited that Dr. Neera Kapoor agreed to once again edit a special issue of BIP on the topic of neuro-optometry. As she noted in her introduction, it has been 13 years since we last addressed this important area of neurorehabilitation assessment and intervention in this publication. I have personally followed Dr. Kapoor’s career and her continued contributions to the field of neuro-optometry and TBI with great satisfaction. It is my hope that this issue with its varied topics including assessment of extraocular muscle function, efferent oculomotor dysfunctions in MTBI, neuro-optometric rehab interventions for sensory triggered anomalies in MTBI and lastly, neuro-optometric evaluation and management of visual field deficits will enhance practitioner expertise in these areas as well as provide a stimulus to explore the neuro-optometric literature in the field of brain injury medicine further. I was particularly pleased to see that Dr. Kapoor assembled a varied group of contributors across a number of different disciplines to author the articles in this issue. Readers will also find the expert interview with Dr. Ciuffreda of great interest given his long history of work in the field of neuro-optometry and TBI.

Nathan D. Zasler, MD, DABPM&R, FAAPM&R, FACRM, DAIPM, CBIST

About the Editor in Chief Nathan Zasler, MD, is founder, CEO & CMO of Concussion Care Centre of Virginia, Ltd. and Tree of Life Services, Inc.. He is board certified in PM&R, fellowship trained in brain injury and subspecialty certified in Brain Injury Medicine. Dr. Zasler has several academic appointments and lectures nationlly and internationally on topics related to brain injury. Dr. Zasler has published extensively on TBI related neuromedical issues. He is co-chief editor of Brain Injury Professional and NeuroRehabilitation and serves on numerous journal editorial boards. Dr. Zasler is active in local, national and international organizations dealing with acquired brain injury and neurodisability.

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Neera Kapoor, OD, MS

from the

guest editor

Re-envisioning Neuro-Optometry

Neera Kapoor, OD, MS, FAAO, FCOVD-A

In 2005, I had the pleasure of guest-editing a special issue of Brain Injury Professional on neurooptometry at Dr. Nathan Zasler’s invitation. Thirteen years later, I am humbled to find myself in a similar position, recruiting leaders in vision science, neuro-optometry, neuro-ophthalmology, physiatry, and clinical neuro-psychology. These experts provide updates on what we have learned, and have yet to learn, regarding neuro-optometric rehabilitation and its role in the inter-professional management of those with traumatic brain injury (TBI). The presentation of vision problems following TBI remains similar, occurring in 40% to 80% of these individuals depending upon the study criteria. These vision problems may impede overall rehabilitative progress and impair function for activities of daily living (ADLs). The more common, vision-related symptoms remain blur, diplopia, slowed reading, eyestrain, dry eye, visual field loss and restriction, visual-vestibular symptoms, photosensitivity, and increased sensitivity to visual motion. Treatment options may include prescribing lenses, fusional prisms, field-expanding lenses, yoked prisms, tints, and neuro-optometric rehabilitation therapy (NORT).

BIO: Author the • Guest Dr.Editor Neera Kapoor graduated with a Masters of Vision Sciences, Doctor of Op Residency in Vision Therapy and Rehabilitation, all at SUNY-College of Opt Dr. Neera Kapoor graduated with a Masters of Vision mid-1990s. Sciences, Doctor of Optometry, As evaluation and management of vision problems become increasingly integrated within interand Residency in Vision professional neuro-rehabilitative care, my goals for this special issue are four-fold. I hope to: and Rehabilitation, allas Chief of Vision Rehabilitation Services from June 2010 throu • Therapy She served at SUNY-College of Optometry First, share clinically-applicable updates to our knowledge base regarding: in the2015 mid-1990s.and remained at SUNY College of Optometry through early 2016. • Efferent (i.e., eye movements and accommodation) vision She served as Chief of Vision • Rehabilitation In early 2016, she transitioned from SUNY-College of Optometry to NY Services from • Afferent (i.e., sensitivity to light and visual motion) vision June 2010 through early July is Clinical Professor 2015 Medicine, and remained at SUNY where she • Integrity of visual field, Associate visual attention, and visual processing of Rehabilitation M College of Optometry through of eye movement-related cranial nerve palsies early provides 2016. clinical care• asManagement a neuro-optometrist at NYU-Langone Health's RUSK In early 2016, she transitioned Rehabilitation Medicine. Second, illustrate the collaborative, inter-professional nature of TBI management, which gradually from SUNY-College of continues to incorporate neuro-optometry in patient care. NYU-School • Optometry Dr.towhere Kapoor has co-authored over 30 peer-reviewed articles, 10 textbook cha of Medicine, she is Clinical Associate Professor Third, share insights from my mentor, colleague, and friend, Dr. Kenneth J. Ciuffreda, whose nearly of Rehabilitation posterMedicine presentations, presented over 110 regionally, na 50 years and of clinicalhas and research experience continue to pave the waylectures for advancing our knowledge and provides clinical care regarding vision deficits after TBI. as a neuro-optometrist at internationally, regarding vision and acquired brain injury. NYU-Langone Health's RUSK Institute of Rehabilitation Medicine.

Dr. Kapoor has co-authored over 30 peer-reviewed articles, 10 textbook chapters, and 25 poster presentations, and has presented over 110 lectures regionally, nationally, and internationally, regarding vision and acquired brain injury.

Finally, dedicate this special issue of “Re-envisioning Neuro-Optometry” to the late Dr. Irwin B. Suchoff. Dr. Suchoff was my mentor, colleague, and friend, who forever changed my life in the summer of 1994 when he permitted me to observe him treating patients with TBI. He then took me under his wing, always encouraging me to look ahead and learn more about what underlies the vastly complex visual presentations following TBI. On behalf of Dr. Suchoff and the authors of these articles, I hope that this issue succeeds in updating and re-setting the reader’s understanding of neuro-optometric rehabilitation of vision issues after TBI and the associated impact on the rehabilitative regimen, ADLs, and overall quality of life.

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Evaluation and Management of Oculomotor, Trochlear and Abducens Paresis/Palsy Curtis Baxstrom, OD, MA • Thomas Lenart, MD • Eugene May, MD

Introduction Patients with neurologic conditions may present with decreased range of motion with or without diplopia secondary to dysfunction of cranial nerves III, IV, or VI. While unilateral occlusion may increase range of motion and reduce diplopia, it may decrease depth perception and may increase the risk of fall (RoF). This paper outlines a rehabilitative therapeutic approach addressing recovery of the range of motion, sector occlusion to control diplopia, and use of compensatory prism, all of which may reduce the RoF and potentially improve performance in other rehabilitative therapies. For larger-magnitude ocular misalignments without evident improvement in monocular range of motion with this rehabilitative approach, a surgical therapeutic approach for ocular re-alignment may be beneficial. Vision rehabilitation post-surgery may further improve the patient’s sensorimotor vision and associated impact on performance in other rehabilitative therapies, as well as activities of daily living (ADLs).

Background The oculomotor, trochlear and abducens nerves, which are all involved in extraocular (EOM) control, are susceptible to damage following a neurological event, such as traumatic brain injury (TBI) and stroke. When damaged, they are related to symptoms including diplopia and RoF. These symptoms require consideration as patients strive to reach their baseline abilities for ADLs. An example of impairment related to diplopia might be a person reaching for a glass of water, missing it, and knocking it over. Another example might be a person reaching for a bed rail, missing it, causing a fall, and resulting in further injury. Thorough evaluation of EOM conditions facilitates recommendations for appropriate treatment, thereby expediting recovery of visual function with the associated opportunity to reach a higher potential for return to work, school, and play.

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The incidence of palsies for cranial nerves III, IV, and VI was documented in a study of 4278 patients over a 30-year-period.1 This study identified sixth nerve palsy and undetermined cause as having the highest prevalence.1 Other studies have included a variety of etiological factors and a wide range of recovery rates.2 Most commonly sixth nerve palsy is caused by vascular conditions and fourth nerve palsy from a traumatic etiology. The recovery of a cranial nerve palsy is related to its etiology. While there is a paucity of research related to the functional recovery of third, fourth and sixth cranial nerve palsies, such knowledge might lead to more structured and consistently effective rehabilitative interventions. Park et al. investigated spontaneous recovery after 6 months for eye movement-related cranial nerve palsies. 3 They noted partial recovery in 85.2% of patients and complete recovery in 67.6% of patients. 3 The problem with this particular study is that it assessed eye alignment only in primary gaze. 3 Any palsy would likely manifest a strabismus in the direction of the palsy; hence, eye alignment should be assessed in all nine positions of gaze. Further, patients typically use many positions of gaze when localizing targets and ambulating in daily life, so diplopia in certain positions of gaze may increase RoF. An analogy would be regarding patients with hemiparesis who may be considered “recovered” because they can stand, but they remain unable to ambulate safely independently.

Case History for Paresis and Palsy of Cranial Nerves III, IV, and VI The case history includes the effects of eye movement-related cranial nerve palsies and the associated impact on ADLs. Inquiries regarding the following aid in diagnosis and management: the nature of the lesion, onset, prior visual conditions, constancy of the strabismus, alleviating factors, and exacerbating factors. A radiological report may aid in determining the location and status of the lesion.

Testing for Paresis and Palsy of Cranial Nerves III, IV, and VI A complete evaluation should include detailed sensorimotor vision testing, with monocular and binocular vision findings. In addition to determining the extent of monocular and binocular ROM, other aspects related to the deviation impacting diagnosis and management are assessed, such as: constancy, direction, magnitude, concomitancy (i.e., how similar is the magnitude of the deviation across all positions of gaze), correspondence, and extent of stereopsis with compensatory prism. The ROM monocularly and binocularly can be documented using a vision disk (see FIGURE 1). This disk provides an accurate documentation pre-, during, and post-treatment by measuring horizontal and vertical degrees using a penlight and observing the Hirschberg reflex (see FIGURE 2 and 3). Limitations of gaze may be assessed using a repeated Dollâ&#x20AC;&#x2122;s Eye test.4 A contracture may develop and manifest a false decreased ROM of the paretic muscle.

FIGURE 3: Vision Disk placed for measuring the vertical ROM Unilateral and alternating cover tests determine both the direction and magnitude of strabismus at far and near viewing distances. If a vertical deviation is present, the Parkâ&#x20AC;&#x2122;s 3-Step test is beneficial, but it is limited to isolating one muscle.5 The spread of concomitancy (i.e., similar magnitude of the deviation across all positions of gaze) may occur over time, making the Parkâ&#x20AC;&#x2122;s 3-Step test not necessarily valid for older lesions.6 In such cases or when multiple muscles may be involved, the Hess-Lancaster test may be more appropriate to better determine any under-action and over-action of the EOMs. Compensatory fusional prism neutralizing the angle would then be trialed with the patient for comfort, singleness of vision, and perception of stereopsis (i.e., relative depth perception).

Intervention

FIGURE 1: Measurement of horizontal ROM using the Vision Disk

A major concern with eye movement-related cranial nerve palsies is diplopia, which is also a significant impediment regarding mobility recovery with the potential for impaired spatial localization, reduced depth perception, and increased RoF. If diplopia is present in an off-axis position of gaze, it may not be manifest during primary gaze testing. Unilateral patching, while beneficial in eliminating diplopia, compromises depth perception leading to increased RoF. Hence, enhancing the general rehabilitative process involves early commencement of vision intervention to improve monocular ROM of the paretic eye and extend the binocular ROM across multiple positions of gaze. A second consideration is when to start treatment. While there is no definitive research study regarding the benefits of early versus later treatment for eye movement-related cranial nerve palsies, in general, vision rehabilitative interventions are initiated shortly after onset of the palsy.7 8 9 Multiple studies document that general rehabilitation improves outcomes, is cost effective, and provides the basis for neuroplasticity during recovery.10 11 12 Vision intervention (see TABLE 1 for categories of interventions) to reduce the visual sequelae of an eye movement-related cranial nerve palsy would also be expected to benefit the overall rehabilitative process.

FIGURE 2: View of the aligned Hirschberg reflex while measuring the binocular ROM

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Table 1: Categories of Vision Intervention for Palsies of Cranial Nerves III, IV, and VI TABLE 1: Categories of Vision Intervention for Palsies of Cranial Nerves III, IV, and VI

Categories of Vision Intervention 1. Visual guidance: educate the patient about their deficit and how to be safe 2. Lenses 3. Selective occlusion 4. Fusional prism 5. Vision therapy 6. Surgery

While the EOM function and eye alignment with associated fusion (i.e., singleness of vision under binocular viewing circumstances) in primary gaze may recover spontaneously,3 a persisting concern is the use of binocular vision in off-axis positions of gaze for basic and instrumental ADLs. In the ophthalmologic literature, there is generic support for orthoptic and rehabilitative intervention. Complete occlusion (i.e., patching) of the paretic eye is not recommended due to concern for possible EOM atrophy and contracture with further impairment of depth perception. This approach may negatively impact long-term outcomes and future surgical treatment. Hugonnier suggested that non-surgical treatment may benefit those with eye movement-related cranial nerve palsies,13 while Von Noorden recommended that non-surgical treatment be initiated on a case by case basis.14 Although no references were found suggesting that non-surgical intervention should not be initiated, there are references indicating that complete occlusion to eliminate diplopia, with no mention of vision rehabilitation, is sufficient for managing eye movement-related cranial nerve palsies.

In right gaze, nasal sector occlusion for the left lens would eliminate diplopia and provide passive therapy to improve the right eye’s ROM. Complete occlusion of the right eye would eliminate diplopia, but it would also eliminate the ability to use the right eye and decrease the opportunity to recover function. Another option for a patient with a unilateral sixth nerve palsy is to provide base-out prism in front of the paretic eye shortly after the palsy’s onset to facilitate binocular vision. While early application of fusional prism benefits eye alignment, it may deter monocular ROM recovery since fusional prism is a compensatory treatment. Therefore, nasal sector occlusion for the spectacle lens before the non-paretic eye in patients with unilateral sixth nerve palsies is the preferred option as it enhances full passive movement and concurrent treatment of the paretic eye, as well as binocular ROM, throughout the day. Extending ROM for EOMs involves using multiple ocular motor movements during recovery. 12 13 A protocol to improve eye movements should incorporate tasks with VOR, OKN, smooth pursuit, and saccades.15 16 Research by Ron et al. reported that vision therapy improved saccades by a factor of 4.5, OKN by a factor of 3.0, and pursuit eye movements by a factor of 2.5. 17 18 19 20 Another treatment approach is to occlude the non-paretic eye while the patient is seated on a chair.

Proposed Rehabilitative Model for Diplopia Management From an optometric perspective, the first therapeutic goal is to improve or recover as much (if not all) of the ROM for the paretic FIGURE 4: Right cranial nerve VI paresis. Left binasal eliminates diplopia into right gaze without eye muscle(s). One can use sector or partial loss of binocular vision to the left. This allows the right eye to passively improve monocular ROM occlusion until full range is recovered, to the right. followed by the possible application of temporary prism to facilitate fusion and The chair would then be rotated to initiate a vestibularly-driven eye improved binocular ROM of EOMs. Along with occlusion, active movement. As an example, for a patient with a right sixth nerve therapy activities to improve ROM would involve tasks utilizing the palsy, the left eye would be occluded with the patient seated on a vestibulo-ocular reflex (VOR), optokinetic nystagmus (OKN), smooth chair that is then rotated leftward. This action provides a subcortical pursuit, and saccades. Over time, another goal is to gradually reduce stimulus for the right eye to abduct, which can then be sustained the magnitude of temporary prism until it is minimal, or no longer with multiple rotations. Pursuit and OKN therapy may be created required, in conjunction with the patient’s spectacles. laterally in a similar fashion. Saccadic treatment would consist of moving the patient’s paretic eye toward its abduction limitation. As an example, a person with a right sixth nerve palsy may manifest Over time, the target being viewed would be moved gradually limited monocular right gaze and diplopia at farther viewing beyond its ROM towards the paretic side of the patient. distances as well as to the right of midline. Incorporating nasal The patient’s task would be to look in the non-paretic direction and sector occlusion for the left lens (see FIGURE 4) would allow the then saccade back to the new extended demand position in the patient to maintain binocular vision into left gaze while facilitating paretic direction. Therapy would involve multiple repetitions daily. binocular depth perception for reaching of targets and mobility.

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Once ROM of the affected EOM (s) has been improved, compensatory prism may be incorporated to promote fusion by providing the patient with an opportunity to slowly reduce eye alignment by a small amount every two to three weeks through vergence adaptation. There are two means of decreasing the vergence angle: vestibular input and jump duction therapy. Jump duction vergence therapy may aid in gradually reducing the ocular mis-alignment over time. Since a patient is rarely able to reduce the magnitude of a large-angle eye mis-alignment all at once, patients usually reduce the magnitude of the ocular mis-alignment in slow, step-wise manner. For those who are unable to completely remove the temporary prism, they may be prescribed a small-magnitude, compensatory prism to be ground in with the current spectacle prescription. An example of the gradual reduction of ocular mis-alignment was reported by Baxstrom involving a case of Arnold Chiari malformation.18 He reported that the patient initially presented with a constant alternating 45-prism-diopter esotropia.21 Over a period of 3.5 months, a patient’s magnitude of eye mis-alignment slowly decreased from 45 prism diopters to 0 at farther viewing distances. No binocular vision therapy for fusion was included. The treatment began well over a year following the onset of double vision; hence, spontaneous recovery was ruled out. 18 From an ophthalmologic perspective, it is common to invoke a “wait and see” approach for eye movement-related cranial nerve palsies, often with the waiting period being up to 12 months prior to a surgical intervention. 22 23 24 25 26 27 28 During this 12-month period, a rehabilitative approach may benefit patients with paresis. Then, if the paresis remains recalcitrant such that vision therapy is unable to improve the range of motion in a reasonable time frame, surgery may be considered.

Summary Patients with palsies of cranial nerves III, IV and VI should be evaluated to determine the neurological condition. Intervention should be immediately considered to help the patient regain any loss of function. This can be achieved with visual guidance, lenses, prisms, selective occlusion, and/or visual rehabilitation. If unable to obtain a full functional recovery, surgery should also be considered as part of the treatment armamentarium.

References 1. Richards B, Jones R and Younge B. Causes and prognosis in 4,278 cases of paralysis of the oculomotor, trochlear and abducens cranial nerves. Am J Ophthalmology 1992;113:489-916. 2. Tiffin PAC, MacEwen CJ, Craig EA and Clay G. Acquired palsy of the oculomotor, trochlear and abducens nerves. Eye 1996;10:377-84. 3. Park UC, Kim SJ, Hwang JM and Yu YS. Clinical features and natural history of acquired third, fourth, and sixth cranial nerve palsy. Eye 2008;22:691-696. 4. Roberts TA, Jenkyn LR and Reeves AG. On the notion of dolls eye. Arch Neurol 1984;41:1242-1242. 5. Torfeeq A. A simple method to identify isolated vertical ocular muscle palsy through Park’s 3-step test. JAAPOS 2010;14(4):363. 6. Brazis AW, Masdeu JC and Biller J. Localization in Clinical Neurology. Philadelphia,PA:Lippincott, Williams and Wilkens, 2011. 7. Maulden S, Gassaway J, Horn S, Smout R, et.al. Timing of initiation of rehabilitation after stroke. Arch Phys Med Rehabil 2005;86:S34-40. 8. Dettmers C, Teske U, Hamzei F, Uswatte G, et.al. Distributed form of constraint induced movement therapy improves functional outcome and quality of life after stroke. Arch Phys Med Rehabil 2005;86:204-08. 9. Shallert T, Fleming S and Woodlee M. Should the injured and intact hemisphere be treated differently during the early phases of physical restorative therapy in experimental stroke or parkinsonism? Phys Med Rehabil Clin N Am 2003;14:S27-46. 10. Cowen T, Meythaler J, DeVivo M, Ivie C, et.al. Influence of early variables in traumatic brain injury on functional independence measure scores and rehabilitation length of stay and charges. Arch Phys Med Rehabil 1995;76(9):797-803. 11. Cramer S, Sur M, Dobkin B, O’Brien C, et.al. Review article: harnessing neuroplasticity for clinical applications. Brain 2011;134:1591-1609. 12. Kleim J and Jones T. Principles of experience-dependent neural plasticity : implications for rehabilitation after brain damage. J Speech Lang Hear Res 2008;51:S225-239. 13. Hugonnier R and Clayette-Hugonnier S. Strabismus, heterophoria, ocular motor paralysis-clinical ocular muscle imbalance. St. Louis, MO:C.V. Mosby, 1969. 14. Von Noorden GK. Paralytic strabismus. In binocular vision and ocular motility-theory and management of strabismus 2nd Edition. St. Louis,MO:C.V. Mosby, 1980. 15. Ciuffreda KJ, Suchoff IB, Marrone MA and Ahmann E. Oculomotor rehabilitation in traumatic braininjured patients. JBO Volume 7 - Issue 2, 1996 16. Kapoor N, Ciuffreda KJ and Han Y. Oculomotor rehabilitation in acquired brain injury: a case series. Arch Phys Med Rehabil 2004;85:1667-78. 17. Ron S. et.al. Can training be transferred from one oculomotor system to another? In Physiological and pathological aspects of eye movements. Roucoux and Crommelinck, Eds. 1982:83-98. 18. Ron S, et.al. Eye movements in brain damaged patients. Scand J Rehab Med 1978;10:39-44. 19. Ron S. Plastic changes in eye movements of patients with traumatic brain injury. In Progress in Oculomotor Research. Fuchs and Becker Eds. 1978:233-40. 20. Ron S, et.al. Training oculomotor tracking. Israel J of Medical Sciences 1992;28:622-628. 21. Baxstrom CR. Nonsurgical treatment for esotropia secondary to Arnold Chiari malformation: a case report. Optometry 2009;80:472-78. 22. Holmes J, Beck R, Kip K, Droste P, et.al. Predictors of nonrecovery in acute traumatic sixth nerve palsy and paresis. Ophthalmology 2001;108:1457-60. 23. Holmes J, Droste P and Beck R. The natural history of acute traumatic sixth nerve palsy or paresis. JAAPOS 1998;2:265-8. 24. Holmes J, Beck R, Kip K, Droste P, et.al. Botulinum toxin treatment versus conservative management in acute traumatic sixth nerve palsy or paresis. JAAPOS 2000;4:145-9. 25. Brazis P. Isolated palsies of cranial nerves III, IV and VI. Semin Neurol 2009;29:14-28. 26. BAheri A, Babsharif B, Abrishami M, Salour H, et.al. Outcomes of surgical and nonsurgical treatment for sixth nerve palsy. J Ophthalmic Vis Res 2010;5(1):32-37. 27. Altintas A, Arifoglu H, Dal D and Simsek S. Are most sixth nerve palsies really paralytic? J Ped Ophthalmol Strab 2011;48:187-91. 28. Advani R and Baumann M. Bilateral sixth nerve palsy after head trauma. Ann Emer Med 2003;41:27-31.

Author Bios Curtis R. Baxstrom, OD, MA, FAAO, FCOVD, FNORA, practices in Federal Way specializing in vision rehabilitation for those with special needs, learning disabilities, traumatic brain injuries, and stroke. He has privileges and consults at multiple rehabilitation hospitals. He is adjunct faculty at Pacific University College of Optometry (PUCO) where he guest-lectures and is Director of the Vision Northwest-Vision Rehabilitation Residency Program. Dr. Baxstrom received his Doctor of Optometry in 1984 from PUCO, after which he completed a Master’s degree in Reading at Seattle Pacific University. He is a fellow of the College of Optometrists in Vision Development, American Academy of Optometry, and Neuro-Optometric Rehabilitation Association, where he serves as Immediate Past President of the Neuro-Optometric Rehabilitation Association. Eugene May, MD, is a neuro-ophthalmologist at the Swedish Neuroscience Institute in Seattle, Washington. He received his medical education at the Pritzker School of Medicine at the University of Chicago and completed a neurology residency as well as a neuro-ophthalmology fellowship at Walter Reed Army Medical Center in Washington, DC. He is a clinical assistant professor of neurology and ophthalmology at the University of Washington and a fellow of the North American Neuro-ophthalmology Society as well as of the American Academy of Neurology. He serves on the Board of the National Multiple Sclerosis Society and participates in neuro-ophthalmic research. Thomas Lenart, MD, has been practicing ophthalmology at The Children’s Eye Doctors since August 1999. Dr. Lenart graduated from Hiram College, a small liberal arts university in Ohio, with a major in Biology and a minor in Physics. After volunteering for two years with the Peace Corps in Benin, West Africa, he completed an MD-PhD program at the University of Pennsylvania. After completing a one-year internship at Lankenau Hospital in Wynnwood, Pennsylvania, he began a three-year residency in ophthalmology in Rochester, Minnesota at the Mayo Clinic followed by a fellowship in pediatric ophthalmology and adult strabismus at the Emory Eye Center in Atlanta, Georgia.

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Efferent-Based Oculomotor Dysfunctions in Chronic Mild Traumatic Brain Injury (mTBI): Diagnostic and Treatment Aspects Kenneth J. Ciuffreda, OD, PhD • Jose E. Capo-Aponte, OD, PhD • Angela Peddle, OD • Naveen K. Yadav, BS Optom, MS, PhD

Introduction Individuals with mild traumatic brain injury (mTBI)/concussion frequently manifest a range of residual visual dysfunctions1, 2. In this brief paper, we overview the primary visual sensory and motor deficits that the neuro-optometrist might uncover in this population.

Diagnostic Aspects

Clinically, this deficit is most evident by the higher number of errors and longer test times than found in normals using the Developmental Eye Movement (DEM) test4, which clinically assesses global saccadic tracking. When applied to reading, a major problem in this population (TABLE 1), an excessive number of saccades are executed, which directly reduces the reading rate and indirectly adversely impacts the comprehension level, as well as produces cognitive fatigue. Typically, the reported “reading problem” is of an oculomotor and not linguistic nature. Pursuit movements are used to track smoothly-moving targets, such as a bird in flight. In these patients, pursuit eye velocity is typically less than target velocity by approximately 20% (i.e., “low gain”), thus requiring additional saccades to correct the residual, accumulating positional error to foveate the target. Clinically, this is manifested as “jerky” pursuit.

Over the past decade or so, one of the primary areas of visual dysfunction following an mTBI has been the oculomotor system2. This includes the versional system, as well as the near triad, namely the interactive vergence, accommodative, and pupillary systems. Versional, or conjugate, eye movements include fixation, saccades, and pursuit, among others3. The versional system is used to track objects in space. Each of the aforementioned versional subsystems has been found to manifest many abnormalities in both the clinical and laboratory settings. Fixation is used to assess target attributes and to derive object meaning. It exhibits increased positional error and variability in mTBI, typically being 1-2 degrees in extent, relative to and centered about the intended fixational position (FIGURE 1). These increased fixational errors (5-10 times greater than found in normals) are typically comprised of large drifts and saccadic intrusions. Saccades, the most rapid eye movements (up to 900 deg/sec), are used to search for and track discrete objects in space. In mTBI, saccades FIGURE 1: Two-dimensional plot of binocular central fixation before (left) and exhibit relatively large, positional undershooting errors of after (right) true oculomotor training in a typical mTBI subject. Data presented approximately 20-30% (i.e., hypometria, or “low gain”), from the right eye (from Thiagarajan P. Oculomotor rehabilitation for reading in thus requiring additional, smaller corrective saccades to mild traumatic brain injury. PhD. dissertation, SUNY/Optometry, 2012). acquire the target foveally.

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sample size (n) % of war fighters Reading problem Vergence Version Accommodation Strabismus CN Palsy Nystagmus General oculomotor dysfunction

Ciuffreda Goodrich et al (2007) et al (2007) Non-blast Blast 160 25 21 0 100 100 75 (est) 60 62 56 36 24 51 32 5 41 20 24 26 50 (est) 30 (est) 7 50 (est) 30 (est) 0.6 4 0 90

at least 50 at least 50 (est) (est)

Lew et al (2007)

Stelmack Brahm et al (2009) et al (2009) Non-blast Blast 62 88 12 112 94 88 100 100 70 50 83.3 87.5 46 28 63.6 46.8 25 6 16.7 24.1 21 47 71.4 45.7 11 8 8.3 7.1 not listed 0 5 not listed 0 7.1 70

50 (est)

Lastly, the vestibulo-ocular reflex (VOR)/vestibular system is used to maintain visual stability during head movement. In many with mTBI (about 80%)2, the VOR gain may be reduced and variable. This results in the perception of oscillopsia, namely the illusory movement of the world, which can be quite disabling, as well as causing related problems with ambulation and balance. In contrast, vergence, or disjunctive, eye movements are used to track and binocularly fuse objects moving in depth.3 The primary vergence subcomponents comprising the overall response are disparity-based fusional vergence and blur-driven accommodative vergence, being interactive and non-linearly summative in nature. The vergence system has a dual-mode control process. There is the initial, nearly one second “transient” phase to alter the vergence angle from one object to another in depth in an attempt to obtain fusion, and a subsequent “sustained” phase to complete the fusional process and to maintain single vision. In both the clinical and laboratory settings, the overall vergence response has been found to be slowed dynamically, delayed, at times reduced in magnitude, and also to exhibit more steady-state error and variability. Clinically, this manifests primarily as a receded near point of convergence, increased fixation disparity (i.e., steady-state vergence error), increased heterophoria magnitude, reduced vergence ranges, and slowed dynamic responsivity at distance and at near (i.e., reduced horizontal prism flipper facility), among others.5, 6 This has been confirmed in the laboratory. For example, one of the most critical and consistent findings has been reduced convergence peak velocity5, 6, being approximately 50% less than found in normals. Thus, this vergence parameter may serve as an objective, visionbased biomarker for the presence of mTBI/concussion.7, 8 Lastly, during reading, in addition to the excessive and inaccurate saccades (of normal velocity), slow and inaccurate vergence is present, therefore also negatively impacting on the reading process. Now, the allocation of general and visual attention must also be directed to compensate and correct for the dysfunctional oculomotor aspects rather than being directed primarily on the linguistic and information processing aspects to promote comprehension. This divided allocation of attentional resources results in slow and inaccurate reading, as well as cognitive fatigue and attentional overload. Accommodation, or “ocular focusing”, refers to the crystallinelens process of maximizing perceived retinal-image contrast at the fovea to obtain clear retinal imagery (i.e., to optimize visual acuity and contrast perception) of objects at different distances.2, 9 Similar to the vergence system, the accommodative system also has two control aspects: an initial “transient” phase of nearly one second to alter focus from one object to another, and a subsequent

40 (est)

Capo-Aponte et al (2015) Non-blast Blast 157 343 100 100 67 60 30 24 30 21 32 32 6 10 not listed not listed 6 5 not listed not listed

TABLE 1: Summary of data from the retrospective studies showing frequency of occurence (%) of the different types of oculomotor dysfunctions. Nystagmus - includes unidentified fixation instability. (est. - estimate), (-data not available). (Actual percentages are rounded off for simplicity).

“sustained” phase to complete the process and to maintain clear vision. Again, similar to the vergence system, accommodative responsivity is delayed, slowed, reduced, and ill-sustained in these patients. Clinically, this is reflected in a reduced amplitude of accommodation, reduced lens flipper facility, and a larger “lag”, or error, of accommodation, among others.9, 10 These clinical findings have been confirmed in the laboratory.9, 10 For example, accommodative peak velocity was reduced by approximately 50% in every person with mTBI tested as compared to normals, thus resulting in overall slowed dynamics. Hence, it too may serve as an objective, vision-based biomarker for the presence of mTBI/ concussion. Again, as related to the major problem of reading in patients with mTBI9, the combination of slowed accommodation and slowed vergence, as well as inaccurate and excessive saccades, makes reading an arduous and frustrating process11, as described earlier. The pupillary system controls the amount of light entering the eye (i.e., the pupillary light reflex, or PLR).12 In addition, it indirectly assists in the accommodative process: the smaller the pupil (as found for nearwork), the less accommodation required via depthof-focus compensation. Again, as is true for the vergence and accommodative systems, the dynamic PLR has a transient and sustained phase but with lengthier overall dynamics (~6 sec) for the latter. In mTBI, the PLR has been shown to be reduced, delayed, slowed, and slightly more variable as compared to normals.12 Some specific parameter abnormalities included increased latency, reduced response amplitude (i.e., “low gain”), reduced peak constriction and dilation velocity, and smaller baseline pupillary diameter, among others. Unfortunately, with the possible exception of uncovering an afferent pupillary defect (APD), none of these deficits can be readily detected clinically, unless a dynamic pupillometer is used as a part of the “special”, or “advanced”, clinical diagnostic test protocol. Several of these dynamic pupillary parameters (e.g., peak dilation velocity) can also serve as objective, vision-based biomarkers for the presence of mTBI/concussion.7, 12 Visual and oculomotor dysfunctions following an mTBI produce a number of visual symptoms that in many cases can adversely affect one’s QOL. Therefore, the assessment of post-concussive visual symptoms is an important component of the initial clinical evaluation, as well as serving as a baseline to monitor remediation of visual deficits during the neuro-optometric rehabilitation intervention, or simply to assess any natural recovery. Numerous visual symptom questionnaires are available to document postconcussive symptoms; however, no gold standard has been identified.

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Two common tools are the Brain Injury Vision Symptom Survey (BIVSS) Questionnaire and the College of Optometrists in Vision Development Quality of Life (COVD-QOL) assessment. The BIVSS is a 28-item questionnaire incorporating a 0-6 Likert scale designed to survey vision symptoms following mild-to-moderate brain injury, with 82.2% sensitivity and 90.4% specificity13. In contrast, the COVDQOL is a 30-item questionnaire using a 0-4 Likert scale. The COVDQOL survey scores showed significant improvement after vision rehabilitation for TBI-related visual dysfunctions.14

Treatment Aspects

Evaluation of patients with mTBI and possible efferent-based oculomotor deficits should commence with careful assessment of the afferent, or sensory, system (See paper by Tannen and Cohen in this issue), as well as a detailed ocular health examination. Then, the oculomotor-based, treatment options are many (TABLE 2): distance and near spectacle lenses, prisms, full and selective occlusion, tints, and neuro-optometric rehabilitation (NOR)2, 15. Many patients do well with a combination of the aforementioned treatments, particularly when the near triad is affected, as typically found in patients with brainstem-related mTBI and visual symptoms.

Frequently, plus lenses at near are dispensed concurrent with NOR to improve further the interactive aspects of the oculomotor system, to reduce visual symptoms, and also to create greater visual efficiency and visual stamina during sustained near tasks.

Prisms Prisms of different powers (prism diopters, pd) are prescribed for a range of oculomotor problems in those with mTBI, as they optically reduce the vergence stimulus and the resultant vergence fusional demand. They are prescribed for vergence dysfunctions, which are common in this population (about 50%), including horizontal and vertical heterophorias/concomitant heterotropias (i.e., the same deviation magnitude regardless of gaze position), as well as non-concomitant heterotropias. Base-in prisms are used to assist those with exophoria, and base-out for those with esophoria. Base-up/down prisms are prescribed for vertical deviations. Diplopia is a common visual symptom, and the application of the minimum amount of prism to create an initial point of fusion in the visual field is the starting position for subsequent NOR. In cases of non-concomitant deviations, flexible press-on prisms (Fresnel), frequently of relatively large magnitudes (e.g., 30 pd), can be used during the initial recovery phase to immediately regain single vision, and enhance patient comfort, without poor cosmesis. Then, NOR can commence. However, when prisms are prescribed, they optically create a visuomotor mismatch1. Since they deviate light towards the prism base (about 1 degree per 2 pd), there is a sensory-motor mismatch between the shifted, perceived optical image of the object and the visuomotor/proprioceptive information/signals used to grasp the physical object. With some practice at pointing and reaching, however, the mismatch is rapidly and totally reduced, assuming it is noticed at all.

Full and Selective Occlusion Selective occlusion is often used if the constant diplopia cannot be eliminated by other means, such as lenses, NOR, etc., and the patient is unhappy with the cosmetic aspect of full occlusion. This involves occlusion of only a TABLE 2: Signs, symptoms, and treatment option for efferent visual deficits. VOR = specific part or parts of the spectacle lens where vestibulo-ocular reflex; NOR = neuro-optometric vision rehabilitation the diplopia is most problematic (e.g., in the left field of gaze with temporal occlusion of the left portion of the left lens) using either graded intensity membranes Lenses (e.g., Bangerter foils) or tape (e.g., translucent tape) to reduce visibility of the diplopic image while retaining reasonably good A careful refraction at distance is the baseline for all lens (or other) cosmesis (FIGURE 2A). Use of selective occlusion rather than full applications and related techniques. Near addition lenses (e.g., +1D, occlusion also allows the patient to retain good balance, peripheral diopter) are highly recommended for those with accommodative vision, peripheral fusion, and visual comfort, with the greatest problems, or more typically vergence-accommodative interactive amount of symptomatic relief and minimal visual annoyance. dysfunctions, with it functioning as a â&#x20AC;&#x153;balanceâ&#x20AC;? lens between Furthermore, the presence of diplopia may result in falls or spatial the two systems.12 These are typically prescribed as single-vision misjudgments that could result in serious injury, especially amongst lenses (SVL) at near. Traditional bifocal and progressive addition the elderly with mTBI where naturally-occurring, age-related balance lenses (PALs) create visual discontinuities and non-uniform optical deficits are common and may already be manifest2. distortions, respectively, that are problematic in many of these patients, especially in those with the symptom of visual motion Another type of selective occlusion is either binasal occlusion (BNO) sensitivity (VMS) (about 40%).2 It has also been found by some (FIGURE 2B) or bitemporal occlusion (BTO). This is used in some optometrists that relatively small amounts of plus lens at near (e.g., patients who are strabismic to initially eliminate the diplopia present +0.5D) may be helpful, presumably by improving the vestibuloin a specific region of the visual field, by forcing divergence in the ocular reflex (VOR) gain via the overall accommodative and disparity esotrope and convergence in the exotrope, to obtain eye alignment vergence/VOR interaction. with fusion.

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It also allows for peripheral awareness that assists in the overall fusional and visual-perceptual process, as well as overall balance and stability. Thus, BNO/BTO also function as an effective, simple, and inexpensive fusional training technique. FIGURE 2A: Selective occlusion.

FIGURE 2B: Binasal occlusion (BNO).

Tint Various achromatic/grey and chromatic tints are typically prescribed for afferent vision problems in this population (see paper by Tannen/ Cohen in the issue), such as photosensitivity and visual motion sensitivity15. However, tints may be used in some cases of diplopia to reduce the intensity of the offensive image when any sort of occlusion is rejected by the patient.

Neuro-optometric Rehabilitation (NOR) Neuro-optometric rehabilitation (NOR) refers to a sequential and specific set of procedures/ techniques of a sensory, motor,

and perceptual nature used to remediate oculomotor, and other (e.g., perceptual figure-ground problems), vision dysfunctions that occur in those with mTBI.2 NOR represents an extension of conventional optometric vision therapy (FIGURE 3). It too involves the scientifically-sound principles of perceptual and motor learning/ planning16, with its neurological basis being general/visual system neuroplasticity of the brain, being present even in older adults with brain damage and abnormal brain function. Furthermore, NOR incorporates the concepts of neural reprogramming and long-term potentiation via repetition, feedback, reinforcement, and selfawareness. This is consistent with the Hebbian, neural-network notion of stimulating stronger/renewed/new synaptic connectivity by appropriate activation and repetition—"the brain that fires together, wires together" concept.16 Initially, this is accomplished through a series of relatively “lower-level” techniques that involve improving basic vergence, accommodation, and versional responsivity, first in relative isolation, and then in an interactive manner for optimal visual efficiency and oculomotor coordination, especially at near. Once this is accomplished, then “higher-level” techniques involving integration with other sensory modalities are performed, such as proprioception, balance/vestibular, and audition, along with gross visuomotor actions, as well as other "tasking loading" techniques such as performing accommodative training on a balance board while sequentially reading off letters on a Snellen chart. That is, the newly-learned NOR abilities must transcend the relatively-controlled clinical environment and be readily performed in naturally-occurring complex situations, such as on a busy street or in a large classroom, in which distractions are present. Thus, the long-term goal of NOR is to provide the individual with mTBI with improved visual and visuomotor abilities leading to enhanced functional abilities, such as reading with comfort, visual efficiency, attentional awareness, and visual stamina in all environments.

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The above clinical ideas related to NOR have been documented in the research laboratory in a range of studies, 5, 6, 9, 10, 17 including a relatively recent randomized clinical trial in adults with mTBI17. The laboratory findings support and extend the aforementioned clinical results and observations, in which objective recordings of version, vergence, and accommodation were assessed before and after nine hours of NOR. Nearly all oculomotor parameters showed significant improvements, with relatively long-term persistence.17, 18 In addition, reading improved, symptoms reduced, and attention increased. Thus, the positive effects of NOR encompass a wide range of functional aspects. Related to the above, Yadav et al.19 investigated the effect of NOR objectively on the visual-evoked FIGURE 3: Proposed underlying basis for vision therapy (from Thiagarajan P. Oculomotor potential (VEP) amplitude and on rehabilitation for reading in mild traumatic brain injury. PhD. dissertation, SUNY/Optometry, 2012). visual attention in patients with mTBI. The results suggested that the oculomotor-based NOR, which â&#x20AC;&#x192; is primarily efferent in nature, also enhanced and improved early References afferent visuo-cortical processing. Furthermore, NOR also has an 1. Suter PS and Harvey LH, editors: Vision Rehabilitation: Multidisciplinary Care of the Patient Following embedded visual/general attentional training aspect2, 16 which was Brain Injury. New York, New York: Taylor and Francis Group, 2011. shown to improve attention in these patients both objectively (i.e., 2. Ciuffreda KJ, Ludlam DP, Yadav NK, et al., Traumatic brain injury: visual consequences, diagnosis, and treatment. Adv Ophthal and Optom. 1: 307-333, 2016. VEP alpha power) and subjectively (i.e., VSAT test scores). Most 3. Ciuffreda KJ and Tannen B: Eye Movement Basics for the Clinician. New York, New York: Mosby Inc., 1995. importantly, this study revealed that nine hours of NOR (i.e., the version, vergence, and accommodation systems) over a six-week 4. Kapoor N and Ciuffreda KJ, Assessment of neuro-optometric rehabilitation using the Developmental Eye Movement (DEM) test in adults with acquired brain injury. J Optom. 11 (2): 103-112, 2018. period were sufficiently effective to produce positive changes at the 5. Szymanowicz D, Ciuffreda KJ, Thiagarajan P, et al., Vergence in mild traumatic brain injury: a pilot study. J afferent, or sensory, visuo-cortical level, as well as at the efferent Rehabil Res Dev. 49 (7): 1083-1100, 2012. oculomotor level as described earlier. Additional hours of NOR 6. Thiagarajan P and Ciuffreda KJ, Effect of oculomotor rehabilitation on vergence responsivity in mild traumatic brain injury. J Rehabil Res Dev. 50 (9): 1223-1240, 2013. would likely have an even more robust effect. In summary, many efferent-based, oculomotor deficits are present in the patient with chronic mTBI/concussion. Fortunately, all of these vision deficits can be remediated, at least to some extent, by the range of neuro-optometric treatment options available. By doing so, it would facilitate patients achieving their vocational and avocational goals. Lastly, many of these deficits may also act as objective, visionbased biomarkers for the early identification of mTBI/concussion, a valuable clinical goal. Acknowledgements: We thank Drs. A. Cohen and I. B. Suchoff, as well as Diana P. Ludlam, for their helpful comments on an earlier draft. The first author would like to dedicate this paper to his mentor, colleague, and friend: the late Dr. Irwin B. Suchoff.

7. Ciuffreda KJ, Ludlam DP, Thiagarajan P, et al., Proposed objective visual system biomarkers for mild traumatic brain injury. Mil Med. 179: 1212-1217, 2014. 8. Ciuffreda KJ, Ludlam DP, and Yadav NK, Convergence peak velocity: an objective, non-invasive, oculomotorbased biomarker for mild traumatic brain injury (mTBI)/ concussion. Vis Dev and Rehab. 4: 6-11, 2018. 9. Green W, Ciuffreda KJ, Thiagarajan P, et al., Accommodation in mild traumatic brain injury. J Rehabil Res Dev. 47(3): 183-200, 2010. 10. Thiagarajan P and Ciuffreda KJ, Effect of oculomotor rehabilitation on accommodation responsivity in mild traumatic brain injury. J Rehabil Res Dev. 51(2): 175-192, 2014. 11. Ciuffreda KJ, Simulation of oculolotor-based reading dysfunctions. YouTube link: https://www.youtube. com/results?search_query=Ciuffreda+eye+movements (Accessed 20th May 2018). 12. Truong JQ and Ciuffreda KJ, Comparison of pupillary dynamics to light in the mild traumatic brain injury (mTBI) and normal populations. Brain Inj. 30: 1378-1389, 2016. 13. Laukkanen H, Scheiman M, and Hayes JR, Brain injury vision symptom survey (BIVSS) questionnaire. Optom Vis Sci. 94: 43-50, 2017. 14. Scharnweber AR, Palmer GA, Ampe HJ, et al., Vision rehabilitation for traumatic brain injury and posttraumatic stress disorder. Vision Dev and Rehab. 2: 132-9, 2016. 15. Ciuffreda KJ, Ludlam DP, and Yadav NK, Conceptual model pyramid of optometric care in mild traumatic brain injury (mTBI): a perspective. Vision Dev and Rehab. 2: 105-108, 2015. 16. Ciuffreda KJ, The scientific basis for and efficacy of optometric vision therapy in nonstrabismic accommodative and vergence disorders. Optom. 73:735-762, 2002. 17. Thiagarajan P, Oculomotor rehabilitation for reading in mild traumatic brain injury. Ph.D. dissertation, SUNY College of Optometry, NY, USA. SUNY DSpace: https://dspace.sunyconnect.suny.edu/ handle/1951/60654 (2012). 18. Thiagarajan P and Ciuffreda KJ, Short-term persistence of oculomotor rehabilitative changes in mild traumatic brain injury (mTBI): a pilot study of clinical effects. Brain Inj. 29: 1475-1479, 2015. 19. Yadav NK, Thiagarajan P, and Ciuffreda KJ, Effect of oculomotor vision rehabilitation on the visual-evoked potential and visual attention in mild traumatic brain injury. Brain Inj. 28: 922-929, 2014.

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The U.S. Consumer Products Safety Commission found more than 750 deaths and 25,000 hospitalizations in its 10-year study of the dangers of portable electric generators. https://www.cpsc.gov/es/content/briefingpackage-on-the-proposed-rule-safety-standard-forKenneth J. Ciuffreda received his B.S inportable-generators biology from Seton Hall University in

Author Bios

1969, from theguidelines: Massachusetts For his theODcurrent http://wedocs.unep. College of Optometry in 1973, and his org/bitstream/handle/20.500.11822/8676/Select_ pollutants_guidelines.pdf?sequence=2 PhD degree in physiological optics from of carbon California/School of 9. the In University an April 2017 monoxide poisoning at a hotel Optometry at Berkeley in 1977. He has had to be in Niles, Michigan, several first responders been a faculty member at the hospitalized because they were notSUNY/ wearing masks while State Optometry New YorkIn a recent they College treated of severely poisonedin children. Detroit the first City sincepoisoning, 1979, where he isresponders presentlydid a not have carbon monoxide detectors and also He might Distinguished Teaching Professor. hashave been poisoned.internationally CO was not determined to be the cause for 20 lectured and authored to 30 minutes. over 400 research papers/chapters, and books related to his research interests Source: 10. 10http://www.corboydemetrio.com/news-121.html “This paper was presented at the Proceedings including amblyopia, strabismus, reading,of the 1st Annual Conference on myopia, eye movements, accommodation, applications to optometry, 11. bioengineering Environmental Toxicology, sponsored by the SysteMed and visual sequelae brainoninjury. Corporation and heldof m acquired Fairborn, Ohio 9, 10th and He11has received many awards and honors September 1970.“ from the AAO, NORA, COVD, and various state optometric associations and colleges. 8.

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ABOUT ColonelTHE José EAUTHOR Capó-Aponte received his

Gordon Johnson is a leading Doctorate of Optometry fromattorney, the Inter- advocate andAmerican author on brain injury. HeRico, is aSchool 1979 cum University of Puerto of Optometry in 1998 and earned his in laude graduate of the University of PhD Wisconsin Sciences State University of New lawVisual school and a from journalism grad from NorthYork, University. State CollegeHe of Optometry in 2007. western has authored some of the While has served in abrain varietyinjury. of clinical, most readheweb pages in He is the administrative, and research positions Pastwithin ChairtheofUSthe Traumatic Army, he is the Brain currentInjury Chief Litigation Group, American Association of Justice. of the Department of Optometry and the He Director was appointed by Wisconsin’s Governor to of Neuro-Optometry Residency the Program state’s sub-agency, the TBI TaskCenter Force from at Womack Army Medical in Fort Bragg. interests 2002 – 2005. HeHisisprimary also theresearch author of two novels visual performance and visual on include brain injury, Crashing Minds and Concussiondysfunctions is Forever. resulting from traumatic brain injury. Having received numerous research grants, he has published over 40 journal articles and book chapters. Angela Peddle, OD, FCOVD, graduated with a Doctorate of Optometry from the Pennsylvania College of Optometry. She completed a Residency in Vision Therapy and Rehabilitation from SUNY State College of Optometry where she was awarded the distinguished Dr. Martin Birnbaum Memorial Award for outstanding knowledge and skill in behavioral optometry. Dr. Peddle currently owns a private practice, vision therapy clinic in Toronto, Canada, where she teaches optometric interns and residents. She is a fellow of the College of Optometrists in Vision Development and the founding President of Canadian Optometrists in Vision Therapy and Rehabilitation. Dr. Peddle has lectured internationally and co-authored journal articles on oculomotor dysfunctions, binocular vision, and the novel research in strabismus/amblyopia therapy. Naveen Yadav, BS Optom, MS, PhD, received a BS degree with honors in Optometry from the All India Institute of Medical Sciences, a Masters in Vision Science from the University of Waterloo, and a PhD in Vision Science from SUNY State College of Optometry. His clinical research areas and teaching interests include acquired brain injury, clinical electrophysiology, visual perception, pediatric vision, and special needs populations. He is presently an Assistant Professor at the Western University of Health Sciences, College of Optometry, Pomona CA. 22 BRAIN INJURY PROFESSIONAL

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Neuro-Optometric Rehabilitation for the Sensory-Triggered Anomalies Associated with Mild Traumatic Brain Injury Barry Tannen, OD • Allen Cohen, OD

Financial Disclosure: The first author receives royalties for the Pocket CFF Tester (FIGURE 2) and the Bernell-Tannen Prism Flipper Test (FIGURE 3), which are both sold by the Bernell Corporation.

Introduction Visual deficits are common in those with mild traumatic brain injury (mTBI) /concussion,1,2 including blur, double vision, generalized photosensitivity, and selective photosensitivity to fluorescent lights, computer screens, and other electronic devices with reduced flicker rates.3,4 Conversely, these patients may experience difficulty in reduced visual environments such as driving at night and walking in dimly lit rooms. Other visually-related symptoms include visual motion sensitivity triggered by multiple visually-stimulating environments such as shopping malls, supermarkets. Exaggerated "visual crowding" effect with text may also cause re-reading, and loss of place when reading.5

A comprehensive NOR evaluation for those with mTBI involves assessing the accommodative, versional, and vergence systems (TABLE 1), as well as ocular health (TABLE 2). There is ample evidence demonstrating the occurrence of oculomotor deficits of accommodation, versions, and vergence in those with mTBI .2,7,8 Current updates regarding the mostly efferent-based oculomotor deficits in those with mTBI are explored by Ciuffreda et al. in this issue.9 Given that afferent vision symptoms experienced in mTBI are not as easily assessed by these standard diagnostic tests, the authors developed, present, and advocate for a more specific diagnostic NOR and treatment approach, which is described in this paper. Table 1: Suggested vision evaluation of the accommodative, versional, and Distance Visual Acuity (uncorrected and corrected) Near Visual Acuity (uncorrected and corrected) Distance Cover Test (pd) Assessment of Smooth Pursuit

These unusual and disturbing sensory-based (afferent) vision symptoms may result in the patient seeking care from multiple healthcare providers including but not limited to eye doctors (optometrists, ophthalmologists, and neuro-ophthalmologists). Often, these vision symptoms do not correlate with standard diagnostic ophthalmic tests, nor do they respond necessarily to conventional treatment approaches.

Assessment of Saccades

Neuro-optometric rehabilitative evaluation and treatment offers specific clinical insight and advanced diagnoses and treatment options to address these issues. Neuro-optometric rehabilitation (NOR) can be defined as “a specialized area of optometry, which addresses the oculomotor, accommodative, visuomotor, binocular, vestibular, perceptual/, visual information processing, and specific ocular/neurological sequelae of the acquired brain injury population… NOR includes standard optometric modalities such as corrective lenses, prisms, tints and coatings, selective occlusion, and optometric visual therapy.”6

Near Divergence Break/Recovery (pd)

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Near Cover Test (pd) Near-point of Convergence Break/Recovery (cm) Distance Divergence Break/Recovery (pd) Distance Convergence Break/Recovery (pd) Near Convergence Break/Recovery (pd) Minus lens amplitude of accommodation (D) Monocular accommodative facility (cpm) Near Vergence facility (cpm) Stereopsis (sec arc)

TABLE 1: Suggested vision evaluation of the accommodative, versional, and vergence systems

Table 2: Suggested ocular health examination for the patient with mTBI External examination of the eyes and adnexa Extraocular motility (range of motion and comitancy) Pupillary examination Visual field analysis Biomicroscopy Tonometry Dilated fundus examination Other tests as indicated

TABLE 2: Suggested ocular health examination for the patient with mTBI FIGURE 1: Peripheral Optokinetic Nystagmus (OKN) Test

Diagnostic Approaches Three specific aspects of afferent vision function being assessed include visual motion sensitivity/selective photosensitivity, distance fusional vergence facility, and reading-related difficulties. Descriptions of, as well as diagnostic approaches for, each of these three aspects are noted below.

1. Visual motion sensitivity/selective photosensitivity Description and Symptoms Visual motion sensitivity (VMS) describes a condition characterized by dizziness, disequilibrium, headaches, or asthenopia when in “busy” visual environments (e.g., supermarkets, malls). VMS may also be triggered by objects moving in the periphery (e.g., in a moving car) or when viewing scrolling on a computer screen. Photosensitivity, or general photosensitivity, refers to increased sensitivity to all lights and is reported by up to 50% of those with mTBI.10 Selective photosensitivity refers to visual discomfort triggered by fluorescent lights, computer screens, and other electronic devices and indoor lighting with reduced flicker rate.11 Diagnostic Tests Peripheral optokinetic nystagmus (OKN) test involves assessing the patient’s subjective response to a rotating peripheral OKN drum (FIGURE 1), which is an adaptation of a technique first described by Ciuffreda.12 During this test, the OKN drum is rotated slowly within several inches from the patient’s face, but approximately 30 degrees to the periphery (left, right, above, and below). The drum is rotated for about 15 seconds and the patient is asked if they have any feelings of discomfort. They are asked to attempt to describe the type of discomfort (e.g. dizziness, headache, or nausea) and grade it on a 1-10 scale to assist in monitoring the patient’s symptoms pre- and post-intervention. Critical flicker fusion (CFF) testing in those with mTBI having light and/or motion sensitivity revealed a higher CFF threshold relative to those without mTBI.13 A clinically-available CFF device (FIGURE 2), one can ascertain the average CFF threshold. While CFF testing is not a formal diagnostic test, it provides adjunctive clinical insight.

2. Distance Fusional Instability Description and Symptoms Some individuals with mTBI experience intermittent diplopia,2, 3 which may occur without a large heterophoria or intermittent strabismus FIGURE 2: as the underlying etiology. Critical Flicker Fusion (CFF) Device Further, this same cohort may also perceive visual motion sensitivity.14 Diagnostic Test Distance fusional facility (DFF) testing, which involves assessing horizontal relative dynamic vergence facility in prism diopters (pd) at farther viewing distances, may be reduced in this cohort of mTBI reporting intermittent diplopia and VMS. Using the College of Optometrists in Vision Development (COVD) Quality of Life (QOL) Symptom Survey14 to distinguish symptomatic from non-symptomatic patients, Tannen et al. found significantly reduced distance horizontal vergence facility in symptomatic post-concussion patients when compared to non-symptomatic patients without history of concussion.14 The DFF test involved the patient viewing a 20/30 Snellen letter at a 15-foot viewing distance. Then, using a 4pd base out /2pd base in prism flipper (FIGURE 3), the patient is instructed to try to fuse the letter as quickly as possible once each side of the prism is placed in front of them. The number of successful cycles completed in one minute is recorded. Tannen et al. reported that a cohort of patients who were non-concussed and asymptomatic averaged 16.90 cpm (+/-1.32), whereas those who were concussed and symptomatic averaged 11.44 cpm (+/-.54).14

FIGURE 3: Distance Fusional Facility (DFF) Prism Flipper

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Visagraph II Eye Movement Recording SystemTM

FIGURE 4A: Developmental Eye Movement (DEM) Test

The Visagraph II Eye Movement Recording SystemTM is an objective eye movement recording test in which patients read gradelevel paragraphs that are cognitively appropriate while their eye movements are recorded with infrared eye movement sensor goggles.19 (FIGURE 5). In the standard protocol, eye movements are recorded while the patient reads a paragraph approximately at their independent reading level.19 We recommend a revision to this standard protocol in which the text level is first recorded at the patient’s independent reading level (IRL) and then up to five grade levels below the IRL.20 This may help in differentiating more language-based versus oculomotor-based reading deficits both in those with and without mTBI.

3. Reading/Scanning Difficulties Description and Symptoms Oculomotor-related symptoms such as skipping of lines, rereading words and sentences, reduced reading speed, and difficulty scanning are commonly reported in patients who have suffered mTBI.2,3,7,9 Ciuffreda et al. using objective eye movement recordings documented deficits in fixation, smooth pursuit, and saccades and their response to oculomotor treatment.15 In a retrospective study, Tannen et al. reported that, out of 25 patients with concussion without a prior history of reading difficulties, 68% who were visually symptomatic also manifested a slowed reading speed (via objectively-recorded eye movements), placing them at least two grade-levels below average.16 Diagnostic Tests Developmental Eye Movement (DEM) test and King-Devick (KD) test are rapid number-naming tests of global saccadic efficiency, which are presented in a visual-verbal format. In one study, the DEM test (FIGURE 4A) was found to be useful in documenting improvement after computer-based oculomotor training in 9 participants with mTBI.17 There is also evidence that the KD Test (FIGURE 4B) can be used as a “removal from play” concussion test when combined with other sideline tests.18

FIGURE 5: Visagraph II Eye Movement Recording SystemTM

Treatment Approaches Neuro-optometric rehabilitative intervention when treating those with mTBI per Ciuffreda et al.9 involves a careful baseline refraction with prescription of lenses to eliminate small refractive errors as well as appropriate near vision correction. Additionally, the authors recommend consideration for incorporating therapeutic tint, binasal occlusion, and fusional prism in spectacle prescriptions as indicated. Further, for those with mTBI that are particularly visually-symptomatic, neuro-optometric rehabilitation therapy (NORT, overviewed later in this paper) may restore function and improve their QOL.

1. Spectacle prescription (lenses, prisms, selective occlusion, tints) Therapeutic Tint

FIGURE 4B: King-Devick (KD) Test

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Therapeutic tint is different than typical gray or brown polarized tints and other standard sunglass tints, which are helpful for generalized photosensitivity in mTBI. A bluish-purple tint (Omega), which is available from Brain Power Incorporated (BPI) 21 (FIGURE 6) and is typically prescribed at about 80-85% transmission mostly for indoor use, has been shown to reduce symptoms of visual motion sensitivity and selective photosensitivity for fluorescent lights and computer screens 22. The reasons for the often dramatic reduction in symptoms remain unclear.

However, there is evidence that the magnocellular visual pathway may be impaired for some with mTBI. This impairment may cause an imbalance between the magnocellular and parvocellular visual processing systems, thereby also impacting the dorsal and ventral cortical streams of visual processing.9 This may lead to the sensation of a visually overwhelming periphery (e.g. increased sensitivity to flicker and visual motion sensitivity) due to an impaired dorsal stream of visual processing. One possible explanation for this is that the short wavelength cones (S-cones) in humans have a peak spectral sensitivity of 442nm. This wavelength is similar to the color violet, which is the approximate color of the Omega tint.21 Perhaps, the preferential stimulation of the S-cone pathway by the Omega tint holds the key to the visual comfort clinically perceived with these tinted lenses in significantly visually-symptomatic persons with mTBI. Essentially, the shorter wavelength tint (evident with the Omega tint) may reduce the sensation of feeling "overwhelmed” by better balancing the dorsal and ventral streams of visual processing.23

FIGURE 6: Brain Power Incorporated (BPI) Omega Tint Binasal Occlusion Binasal occlusion refers to black, colored, or translucent tape typically oriented diagonally at the nasal limbus on the patient’s glasses (FIGURE 7). This selective occlusion technique has been successfully used as a treatment for VMS in mTBI.5,9 The placement of this selective occlusion with regard to width and color of the binasal occluder is a matter of trial and error.5 Regarding the mechanism of action, one hypothesis involves cortical areas V6/ V6a, which are responsible for the processing of visual object motion and self-motion across the entire visual field. Damage to areas V6/ V6a may cause a mismatch in object motion and self-motion signals, thereby causing visual instability. This may be a key element in the genesis of visual motion sensitivity. In this scenario, the binasal occlusion serves to reduce the mismatch of the signal by occluding a region of the retinal periphery of each eye.5

2. Neuro-Optometric Rehabilitation Therapy (NORT) NORT is a specialized optometric intervention, which addresses the symptoms and deficits associated with TBI,8,24 by incorporating the contemporary neuroscience research to modify and enhance classic optometric vision therapy procedures.25-27 Chang et al.27 recommends a three-phase NORT program which utilizes the research of Kandel28 on brain learning and the suggestions of Kleim25 in developing their model for enhancing and developing neuro-optometric visual therapy procedures. Chang et al..27 refer to five components which, when incorporated in visual therapy procedures, optimize the participant’s performance: motivation, feedback, repetition, sensory-motor mismatch, and intermodal integration.27-29 Each component involves some degree of topdown, intermodal processing. Incorporating these components into a NORT program with lenses, prisms, filters, and specialized equipment enhances neuro-plasticity and efficacy of treatment. 29 The following overviews a typical NORT protocol for managing typical visual symptoms associated with mTBI.

Phase I: Enhance the stability of the visual input system Mild TBI often results in different levels of afferent and efferent vision deficits affecting the accuracy and efficiency of visual information processing and, more specifically, intermodal sensory processing as discussed by Ciuffreda et al. in this issue.9 For this reason, it is important for the first level of visual input to be as accurate as possible since this provides the basic foundation for higher-level visual information processing. The prescribing of lenses, prisms, tints, as well as neuro-optometric rehabilitation therapy procedures are important in this phase of therapy to address the basic ocular motor functions comprising the visual sensory input (TABLE 3). An example of a phase I procedure is outlined in TABLE 4. Table 3: Basic visual input skills to be improved with a “bottom up” vision th 1. 2. 3. 4. 5. 6. 7.

Visual acuity Accommodative amplitude and facility Quality of fixation Range of ocular motility The quality of the ocular motor system to sustain a match to the visual input Accurate saccades (bottom up and top down) Binocular stability

TABLE 3: Basic visual input skills to be improved with a “bottom up” vision therapy approach

Prism Fusional prism correction is commonly employed to reduce fusional demand as a result of large heterophorias and intermittent strabismus in those with mTBI. We have found that patients with a large-angle horizontal heterophoria or a small vertical deviation respond well to low amounts of compensatory prism.22 FIGURE 7: Example of There are numerous “formulas” or rules Binasal Occlusion to help decide the amount of prism to prescribe, but we have found that trial and error with the smallest magnitude of prism to achieve symptom relief, sensory, and motor fusion, is usually the best approach.

Phase II: Enhancing binocular control alignment and sustenance Diplopia and blur, whether constant or intermittent, are possible symptoms following mTBI. While they are typically associated with accommodative and binocular deficits, their presence may exacerbate higher-level processing deficits associated with mTBI. Unstable binocularity and the inability to sustain clear, comfortable vision for extended time periods may contribute to the symptoms of motion sensitivity triggered by reading, as well as reduce one’s ability to read with comfort and comprehension. Additionally, unstable binocular vision may influence the vestibulo-ocular reflex (VOR) resulting in disequilibrium when in multiply visually-stimulating environments.29 The goals of this phase of treatment are to develop adequate alignment, control, stability, and facility of accommodative vergence, as well as enhance the speed of recovery of fusion for both static and dynamic ocular alignment.

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This will ensure that the two eyes are aligned appropriately and on command to the target of regard with sustained fusion. An example of a phase II procedure is given in TABLE 5. Phase III: Developing Speed of Visual information Processing: Stability of Output In response to complex incoming sensory information, the afferent and efferent components of the brain processing system must selectively attend, filter, and organize this information to a specific task. The speed and accuracy of this process is facilitated by two parallel streams: ventral and extended dorsal processing streams. Often, the response to an object being viewed and its resultant movement require a recalibration of sensorimotor control. The extended dorsal stream and its integration with the frontal and pre-motor lobes are important for the control of visually-guided movements. It has been shown that the speed by which information is processed, calibrated, and recalibrated can be enhanced through training.26,29 An example of a phase III procedure is given in TABLE 6.

Table 4: Example of a Phase I Neuro-Optometric Rehabilitative Therapy (NORT) Procedure 1.

2. 3.

The patient fixates 2 golf tees inserted into spaced holes on a rotating vertically mounted pegboard holding a loop with arm extended in a comfortable position, approximately at arm’s length and eye level, and aims the loop so that one of the golf tees is sighted through the loop. The goal is to visually track the golf tee as it rotates for several cycles, simultaneously re-adjusting the position of the loop so that the golf tee is always centered in the loop. The patient is directed to follow one peg for several cycles, then to visually aim their eye to the other golf tee and readjust the loop to center the tee and track this tee for several cycles. This sequence is repeated for several repetitions. Once this basic level is achieved, the procedure can be “loaded” to incorporated multisensory triggers, by having the patient stand on a balance board, switch fixation after several beats of a metronome, and match the visual shift created by a prisms place in front of the eyes.

TABLE 4: Example of a Phase I Neuro-Optometric Rehabilitative Therapy (NORT) Procedure Table 5: Example of a Phase II NORT Procedure 1. 2. 3.

The patient fixates a projected light with both eyes open, wearing red and green goggles. For the initial stage, the patient should see one light with a mixture of red and green color. A prism lens of selected powers is sequentially place over one eye and the goal is for the patient to sustain the fusion of the light. If the light doubles, the patient is encouraged to use the awareness of the two colors to readjust their eyes and refuse the light to one combined red green projection. Once this level is achieved, the procedure can be “loaded” by: increasing prism power, standing on a balance board, sustaining fusion of the light with head shaking and finally, enhancing speed of fusion recovery after closing their eyes for a few seconds and then readjusting their eye alignment to refuse the light when their eyes re-open.

TABLE 5: Example of a Phase II NORT Procedure Table 6: Example of a Phase III NORT Procedure 1. 2. 3.

The patient is balanced on a WiiTM balance board with a WiiTM remote in one hand. Wearing red and blue goggles, the patient views a screen with a projected maze of blue lines with gaps, as well as red letters. Both targets are filtered by the respective goggle lenses. The program directs the patient, using a verbal command, to select a specific red letter and to guide letter with the WiiTM remote through the gaps in the blue mazes without touching the edges of the gap. Because of the filtering of the red blue goggles, the eyes must maintain alignment and fusion. The task demand requires initiating a saccadic movement, followed by a coordinated visual-motor response, as the letter is guided through the maze. If the eyes misalign during this dynamic process, the patient will not be able to guide the letter accurately through the gaps and will hit the edges of the opening resulting in an auditory feedback. To continue with task, the patient uses the auditory feedback to re-adjust eye alignment to continue this task accurately. This therapy sequence can be “loaded” by: decreasing the width of the gaps, adding prism lenses, and finally projecting a video with peripheral movement such as a scene of a crowded street over the projected maze. The goal is for the patient to use skills developed in phases I and II to accurately guide their visual and visuomotor systems while filtering the peripheral and auditory triggers.

TABLE 6: Example of a Phase III NORT Procedure

Summary Individuals with mTBI may present with an array of sensory symptoms and anomalies, often involving vision, which may pose challenges to healthcare providers. Incorporating neuro-optometric rehabilitation as a treatment option, including the diagnostic tests and treatment approaches discussed, may aid clinicians in helping these symptomatic individuals with mTBI achieve improved visual comfort and quality of life. References 1. Suchoff IB, Ciuffreda KJ, and Kapoor N, editors: Visual and Vestibular Consequences of Acquired Brain Injury. Santa Ana (CA): Optometric Extension Program Foundation, Inc, 2001. 2. Ciuffreda KJ, Ludlam DP, Yadav NK, et al., Traumatic brain injury: Visual consequences, diagnosis, and treatment. Adv Ophthal and Optom. 1: 307-333, 2016.

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3. Kapoor N and Ciuffreda KJ, Vision disturbances following traumatic brain injury. Curr Treat Options Neurol. 4: 271-280, 2002.

4. Phan T and Cohen A, Neuro-optometric rehabilitation of visual and visual-vestibular symptoms following acquired brain injury. Vision Dev and Rehab. 3(2):110-20, 2017. 5. Ciuffreda KJ, Yadav NK, and Ludlam DP, Binasal occlusion (BNO), visual motion sensitivity (VMS), and the visually-evoked potential (VEP) in mild traumatic brain injury (mTBI/TBI). Brain Sci. 7, 98:1-14, 2017. 6. Website of the College of Optometrists in Vision Development. Available at: http://www.covd. org/?page=Braininjury, accessed May 16th 2018. 7. Master CL, Scheiman M, Gallaway M, et al., Vision diagnoses are common after concussion in adolescents. Clin Pediatr. 55 (3): 260-267, 2016. 8. Padula WV, Capo-Aponte JE, Padula WV, et al., The consequences of spatial visual processing dysfunction caused by traumatic brain injury (TBI). Brain Inj. 31(5): 589-600, 2017. 9. Ciuffreda KJ, Capo-Aponte JE, Peddle A, et al., Efferent-based oculomotor dysfunctions in chronic mild traumatic brain injury (mTBI): diagnostic and treatment aspects. Brain Injury Professional. 15 (3): 16-21, 2018. 10. Capo-Aponte JE, Urosevich TG, Temme LA, et al., Visual dysfunctions and symptoms during the subacute stage of blast-induced mild traumatic brain injury. Military Medicine. 177(7): 804-13, 2012.

Conclusion Concussion management is an ever-evolving area of treatment designed to better protect athletes from suffering the lingering 13. Chang TT, Ciuffreda KJ, and Kapoor permanent N, Critical flicker frequency and related symptoms in mild traumatic of a and potentially effects and symptoms brain injury. Brain Inj. 21(10): 1055-62, 2007. concussion and premature return to play. Remember, treating 14 Tannen B, Rogers J, Ciuffreda KJ, et al., Distance horizontal fusional facility (DFF): a proposed new concussions, particularly those that do diagnostic test for concussion patients. Vision Dev and Rehab. 2(3):170-75, 2016.not resolve quickly, 15. Ciuffreda Han Y, Kapoor N, et al., dynamic Oculomotor rehabilitation for reading brain injury. to stay is a KJ,complex and process. It inisacquired important NeuroRehabil. 21(1): 9-21, 2006. up to date on the literature, consensus statements, updated 16. Tannen B, Darner R, Ciuffreda KJ, et al., Vision and reading deficits in post-concussion patients: a organizational/institutional protocols and requirements, and retrospective analysis. Vision Dev and Rehab. 1(3):206-13, 2015. state laws. Maintain adequate and complete records. Educate 17. Kapoor N and Ciuffreda KJ, Assessment of neuro-optometric rehabilitation using the Developmental Eye Movement (DEM) test in adults with acquired brain injury. J Optom. 11(2):103-112, 2018. the athlete, the parents, if applicable, coaches, etc. to ensure 18. Marinides Z, Galetta KM, Andrews CN, et al., Vision testing is additive to the sideline assessment of everyone is doing their role to protect the athlete, is aware of sports-related concussion. Neurol Clin Pract. 5:25-34, 2015. the risks and dangers, and can assist in providing the best care 19. Taylor SE: Visagraph II Eye-Movement Recording System. Huntington, New York: Taylor Associates/ Communications, 2000.return to play of the concussed athlete. for theInc., safe 11. Truong JQ, Ciuffreda KJ, Han MH, et al., Photosensitivity in mild traumatic brain injury (mTBI): a retrospective analysis. Brain Inj. 28(10):1283-1287, 2014.

12. Ciuffreda KJ, Visual vertigo syndrome: clinical demonstration and diagnostic tool. Clin Eye and Vis Care. 11:41-42, 1999.

Neuro-Recovery

Specializing solely in post-acute neuro rehab since 1982

20. Tannen B and Ciuffreda KJ, A proposed addition to the standard protocol for the VisagraphTM eye movement recording system. J Behav Optom. 18: 143-147, 2007.

GALVESTON LUBBOCK

REFERENCES

21. Website of Brain Power Incorporated Available at: http://callbpi.com/golf/index.php?route=product/ product&product_id=707&search=autis accessed May 15, 2018.

Aubry M, Cantu R, Dvorak J, et al. Summary and agreement statement of the 1st

Call: 800.TLC.GROW

22. D’Angelo MInternational and Tannen B, The optometricon careConcussion of vision problems after concussion: a clinical guide. Symposium in Sport, Vienna 2011. Clin J Sport Med Optom Vis Perform. 3(6):298-306, 2015. 2002:12:6-11.

www.tlcrehab.org

2. P, College Aubryof M, Cantu R, Dvorak J, et al. Summary and Bellevue, agreement statement of the 1st 23. Quaid Optometrists in Vision Development, Annual Meeting, WA USA. Personal communication 2018. International Symposium on Concussion in Sport, Vienna 2011. Clin J Sport Med 2002:12:6-11. 24. Goodrich GL, Martinsen GL, Flyg HM, et al., Development of a mild traumatic brain injury-specific vision screening a Delphi study. J Rehabil Res Dev. 50(6): 2013. 3. protocol: McCrory P, Johnston K, Meeuwisse W, 757–68, et al. Summary and agreement statement of the 2

International Symposium on Concussion in Sport, Prague 2004. Br J Sports Med

25. Kleim JA and Jones TA, Principles of experience-dependent neural plasticity: implications for 2005;brain 39:196-204; McCrory P, Meeuwisse Johnston K, et al. Consensus statement rehabilitation after damage. J Speech Lang Hear Res. 51(1): Q, S225–S239, 2008.

on concussion in sport: the third international conference on concussion in sport held

26. Groffman S: injury and2008. visual information processing deficits. In: Vision Rehabilitation: inAcquired Zurich,brain November Phys Sportsmed 2009;37:141-59; McCrory P, Meeuwisse Multidisciplinary careAubry of the patient following brain injury. PS Suter LH Harvey (Eds.) CRC Press, th International WH, M, et al., Consensus statement on&concussion in sport: the 4Boca Raton, FL. Pages 407-420, 2011.

Conference on Concussion in Sport held in Zurich, November 2012. Br J Sports Med 2013;47:250-258. 27. Chang A, Cohen A, and Kapoor N, Top-down visual framework for optometric vision therapy for those with traumatic brain injury. Vis Perform. 2013. 4. McCrory P, Optom Meeuwisse WH,1(2):82-93, Aubry M, et al. Consensus statement on concussion in the of 4thmemory: International Conference on Concussion in Sport heldW.W. in Zurich, 28. Kandel ER:sport: In search the emergence of a new science of mind. New York: Norton &November Company, 2006. 2012. Br J Sports Med 2013;47:250-258.\ 5. AH,Guskiewicz, K, Bruce, S, Cantu, R, etdysfunction: al., National Association Position 29. Cohen Vision rehabilitation for visual-vestibular the Athletic role of theTrainers’ neuro-optometrist. Management of Sport-Related Concussion. Journal of Athletic Training NeuroRehabil.Statement: 32:483-92, 2013. 2004;39(3)280-297. 6. Broglio, S, Cantu, R, Gioia, G et al., National Athletic Trainers’ Association Position Statement: Management of Sport Concussion. Journal of Athletic Training 2014:49(2):000-000. 7. Giza, C, Kutcher, J, Ashwal, S, et al. Summary of evidence-based guideline update: Evaluation and management of concussion in sports, American Academy of Neurology. 8. http://www.ncaa.org/sport-science-institute/concussion-diagnosis-and-managementBarrybest-practices Tannen, OD, is in an optometric private practice at EyeCare Professionals, PC in Hamilton, New Jersey, where his 9. http://www.ncaa.org/sport-science-institute/concussion-diagnosis-and-managementclinical and research emphases are visual deficits related to best-practices acquired brain injury. Dr. Tannen a 10. McCrory P, Meeuwisse WH, Aubry is M,the et al.program Consensussupervisor statement onfor concussion in sport: the practice-based, 4th International Conference in Sport held in Zurich, November private Residencyon in Concussion Vision Therapy and Neuro2012. BrRehabilitation J Sports Med 2013;47:250-258. Optometric at EyeCare Professionals. Dr. Tannen 11. McCrory Meeuwisse WH, AubryAward" M, et al. by Consensus statement on concussion in sport: received the P,"Ludlam Education the Neuro-Optometric the 4th International Conference on Concussion in Sport held in Zurich, November Rehabilitation Association in 2014 and the A.M. Skeffington 2012. Br J Sports Med 2013;47:250-258 award for C, excellence Optometric Writing from College ofguideline update: 12. Giza, Kutcher, J,inAshwal, S, et al. Summary of the evidence-based Optometrists Development (COVD) in 2016. HeAcademy is a of Neurology. Evaluation in andVision management of concussion in sports, American Fellow of COVD, the Immediate of evidence-based COVD, and anguideline update: 13. Giza, C, Kutcher, J, Ashwal, S, Past et al.President Summary of Evaluation and management of concussion in sports, AmericanCollege Academyof of Neurology. Associate Clinical Professor Emeritus of the SUNY/State 14. McCroryinP,New Meeuwisse M, lectures et al. Consensus statement on and concussion in sport: Optometry York.WH, Dr. Aubry Tannen internationally the 4th International Conference on Concussion in Sport held in Zurich, November has co-authored over 50 journal articles. 2012. Br J Sports Med 2013;47:250-258 at Table 1. 15. McCrory P, Meeuwisse WH, Aubry M, et al. Consensus statement on concussion in sport: Allenthe Cohen, OD, is a clinical professor of optometry 4th International Conference on Concussion in Sportand heldthe in Zurich, November 2012. Br Sports Med 2013;47:250-258 at Table 1; Giza,Residency C, Kutcher, J, Ashwal, S, et al. supervisor ofJthe Neuro-optometric Rehabilitation Summary evidence-based guideline update: and management at SUNY StateofCollege of Optometry, whereEvaluation he provides neuro- of concussion in sports, American Academy of Neurology.

Author Bios

optometric rehabilitation to visually-symptomatic patients with acquired brain injury (ABI). Dr. Cohen was previously in private practice for over 40 years where he specialized in neuro-optometric rehabilitation services for patients with visual ABOUT THE AUTHOR problemsR. as aPfeil, resultEsq. of ABI other neurologic Amanda is and an associate attorneydisorders. at Shapiro Winthers & In addition,P.C.in for over 25 years, he was theShe former the McGraw, Denver, Colorado. has Chief been ofpracticing law since Optometry Service the Northport Medical Center, where 2009 and has beenatawarded Super VA Lawyers Rising Star for the last three he treated numerous military service Dr.representing Cohen has individuals years in a row. Amanda focuses hermembers. practice on nationally have professional sustained life-altering as the result of published inwho numerous journals and injuries has contributed negligence others. A large majority of her practice has dealt with chapters onof vision and ABI. assisting injured individuals who have sustained traumatic brain injuries and spinal damage.

The TLC Continuum •

Intensive inpatient and outpatient/day program for brain & spinal cord injuries

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Long-term supported living and respite care

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BRAIN INJURY professional 27

Evaluation and Management of Visual Processing, Visual Attention, and Visual Field Deficits in Individuals with Brain Injuries Derek Tong, OD • Marcel Ponton, PhD Wei-Ching Lee, MD • Tonya Umbel, OD • DeAnn Fitzgerald, OD

Introduction Sequelae of brain injuries, including traumatic brain injury (TBI), often include deficits in visual processing, visual attention, and visual field integrity. Visual processing, also known as visual information processing, or visual perception, is the active process of locating, extracting, and interpreting visual information from the environment.1 Visual attention involves searching, shifting, remaining focused on one task, and/or being aware of the surroundings while focusing on a task.2 Visual field, or peripheral vision, is the extent of physical space visible to each eye. This inter-professional article provides an evidence-based overview regarding these three aspects, as well as relevant symptoms assessment, evaluation techniques, and generalized intervention options.

Background Research involving veterans with TBI has advanced the understanding of visual processing deficits such as reduced visual memory, visual processing speed, visuo-spatial attention, and visual sustained attention.3 In addition, neurocognitive research on children with TBI revealed reduced intelligence quotient scores, visual identification, and visual integration. Testing results for these children manifested as reduced efficiency of visual processing and were hypothesized as contributing factors to their poorer cognitive performance.4 Further investigation showed that children with TBI had reduced visual-auditory integration, which suggested reduced efficiency of multisensory integration.5 Regarding visual attention, studies on visual processing of facial expressions utilizing computerized objective techniques noted reduced ability for children with TBI to process facial expressions visually.6 Using functional magnetic resonance imaging (fMRI), reduced visual facial expression processing in adults with TBI was evident and accompanied by reduced white matter integrity in the inferior longitudinal fasciculus and inferior-fronto-occipital fasciculus, as well as reduced gray

FIGURE 1: Example of homonymous hemianopia

FIGURE 2: Example of unilateral spatial inattention (USI)

28 BRAIN INJURY professional

Evaluation Techniques

matter volume in the lingual gyrus and para-hippocampal gyrus.7 Adults with TBI from motor vehicle accidents manifested reduced activation in cortical emotion-processing circuits including the left medial orbitofrontal gyrus, the left and right lateral orbitofrontal gyrus, and the left superior parietal gyrus.8

Screening by Rehabilitation Physician

Regarding visual field integrity, a study on visually-symptomatic persons with acquired brain injury (ABI) reported visual field deficits in 66.67% of those with stroke and 38.75% of those with TBI.9 Homonymous hemianopsia, illustrated in FIGURE 1, was evident in 31.67% of those with stroke and 8.75% of those with TBI. Further, unilateral spatial inattention (USI), which is also known as visual spatial neglect (see FIGURE 2), was reported in 8.1% of those with TBI10 and 72.6% of those hospitalized with acute stroke.11

Symptoms Assessment A retrospective study regarding a sample of visually-symptomatic persons with ABI reported that the most common vision symptoms in those with TBI included eyestrain when reading, light sensitivity, headaches when reading, and blurry near vision. Whereas, the most common vision symptoms amongst those with stroke were blurred near vision, eyestrain when reading, loss of place when reading, and blurred distance vision.12 Common vision symptoms can be ascertained by using a thorough case history and administering a symptom survey, of which there are many. A recent validated vision symptom survey related to ABI is the Brain Injury Vision Symptom Survey (BIVSS), which quantifies the severity of their vision symptoms.13 This one-page, self-administered questionnaire consists of 28 questions encompassing 8 areas of quality of life (QOL): eyesight clarity, visual comfort, double vision, light sensitivity, dry eyes, depth perception, peripheral vision, and reading. Each question is quantified by a 0 to 4 scale: (0 = never, 4 = always). The BIVSS may be downloaded free online http://links.lww. com/OPX/A248 as a vision symptoms screening tool by brain injury professionals.

The presence of signs or symptoms of visual field defects, visual spatial neglect, saccadic dysfunction, binocular vision dysfunction and/or visual processing dysfunction serves as a rationale for referring for neuro-optometric rehabilitation (NOR) evaluation. The rehabilitation physician determines the impact of the vision deficits on the individual's activities of daily living (ADLs). In collaboration with neuro-optometry, strategies and interventions to optimize vision function for ADLs and improve the patientâ&#x20AC;&#x2122;s QOL are implemented. Evaluation of Visual Field Integrity Visual field integrity can be evaluated by confrontation or automation in individuals whose cognitive abilities are reasonably intact.1 Confrontation visual field testing can detect most large visual field defects including homonymous hemianopsia 76-90% of the time.14 15 Detecting subtle visual field defects or quantifying defects evident with confrontation testing requires automated visual field testing, which can be performed by most eye care providers. TABLE 1 summarizes an advanced, four-step confrontation visual field technique 16 often used by neuro-optometry to assess large visual field defects, rule out the Riddoch phenomenon or blindsight, screen for visual field defects that could interfere with ADLs, and identify USI. In addition to confrontation visual field testing, the draw-a-clock test and/or the Behavioral Inattention Test are often performed when either USI or visual neglect is suspected. 17 Comprehensive Evaluation of Visual Processing and Visual Attention Visual processing evaluation may involve visual discrimination, visual memory, visual spatial relations, visual-spatial closure, visual processing speed, visual attention, and visual spatial awareness.

Table 1: Advanced Four-Step Confrontation Visual Field Technique

Steps STEP 1: Static visual field

Procedure 1. 2. 3. 4. 5. 6.

STEP 2: Kinetic visual field

1. 2. 3. 4.

STEP 3: Static and kinetic visual fields with varied attention allocation STEP 4: Dual presentation

Purpose

Outcome

Patch one eye. Instruct patient to fixate central target at all times. Instruct patient to close both eyes Position your hand for finger counting test Have patient open eyes and fixate on central target and respond. Test all 4 quadrants one eye at a time.

Eliminates movement cues, otherwise, results can be inaccurate due to stimulation of the V5 processes in the visual cortex which may cause false negative due to blindsight or Riddoch phenomenon

Assesses the basic static visual field (V1 processes)

Patch one eye. Instruct patient to fixate central target at all times. Then position your hand for count finger test and ask patient to respond. Test all 4 quadrants one eye at a time.

Allows for movement cues to identify differences between kinetic versus static visual field testing

Differentiates V1 from V5 data (detect blindsight)

Determines if attention allocation to motor task such as standing and walking will cause visual field reduction.

Screens for visual field deficits that affect activities of daily living and therapy.

Determines if patient can detect targets presented on both sides at the same time.

Differentiates visual extinction from other defects (e.g., USI and HH)

Repeat static and kinetic visual fields while patient is standing and then walking. Examiner will need to walk backward keeping equidistant from patient at all times. Show two finger targets simultaneously in each horizontal hemisphere performing binocularly for static visual field as well as kinetic visual field

TABLE 1: Advanced Four-Step Confrontation Visual Field Technique

BRAIN INJURY professional 29

Table 2: Commonly Used Neuropsychological Tests for Visual Processing

Visual Discrimination • Neuropsychological Assessment Battery (NAB): Visual Discrimination Subtest • Benton Visual Form Discrimination Visual-Constructive/Visual Motor skills • Rey-Osterreith Complex Figure Test and Recognition Trial • Wechsler Adult Intelligence Scale, 4th edition (WAIS-IV): Block Design • Beery-Buktenica Visual Motor Integration, 6th edition. (Beery VMI) • Test of Visual-Motor Skills (TVMS-3) Visual Reasoning • Raven’s Progressive Matrices • Wechsler Scale: Matrix Reasoning • Motor Free Visual Perception Test (MVPT-4) • Test of Non-Verbal Intelligence (TONI-4)

Batteries of Visual Functioning • Tests of Visual Perceptive Skills, 4th edition (TVPS-4) • Developmental Test of Visual Perception, 3rd edition (DTVP-3) • Full Range Test of Visual Motor Integration (FRTVMI) • Preschool Visual Motor Integration Assessment (PVMIA) Selective Attention • Ruff 2 & 7 Selection Attention Test • Stroop Color and Word Test • Delis-Kaplan Executive Function System (D-KEFS): ColorWord Interference Test Visual Attention/Vigilance • Trails Making Test (TMT) • Color Trails Test (CTT) • Delis-Kaplan Executive Function System (D-KEFS): Trails Making Test

TABLE 2: Commonly Used Neuropsychological Tests for Visual Processing Commonly used tests by neuropsychologists for assessing higherlevel visual processing are summarized in TABLE 2. Findings indicating symptoms caused by visual deficits serve as a rationale to refer to neuro-optometry. Computerized Evaluation in the Rehabilitation Setting ImPACT® (Immediate Post-Concussion Assessment and Cognitive Testing) is a computer-based, neurocognitive assessment tool for concussion taking less than 30 minutes to administer. 18 ImPACT® has baseline and post-injury testing, which may be used along with other clinical measures to determine an individual’s ability to safely return to school, work or play. The assessment begins with a survey of 22 concussion-related symptoms, rated using a 0 to 6 severity scale. Table 3: ImPACT Test Components Test Components

Processing Skills Measured

Word discrimination

Visual attention, verbal memory

Design memory

Visual attention, visual memory

X’s and O’s

Visual processing speed, visual memory

Symbol matching

Visual processing speed, visual memory

Color match

Reaction time with impulse control & response inhibition

Three letters

Visual processing speed, verbal memory

TABLE 3: ImPACT Test Components Neurocognitive and visual processing skills assessed are summarized in TABLE 3. Upon completion, a detailed report summarizes performance in five areas: verbal memory, visual memory, visual processing speed, reaction time, and impulse control. The sensitivity and specificity of ImPACT® to detect concussion in athletes were 81.9% and 89.4% (original version) 19 and 91.4% and 69.1% (online version) respectively. 20

30 BRAIN INJURY professional

ImPACT® is a useful component in assessing the neurocognitive sequelae of concussion, providing post-injury data to monitor rehabilitation progress and decide when to return to activity (i.e., school, work, or play). Evaluation of Visual Spatial Awareness A unique type of visual spatial disorder, abnormal egocentric localization, or visual midline shift syndrome (VMSS) was reported in 40-93% of those with ABI 21 22 23 , with a recent study showing objective assessment of VMSS utilizing a computerized walkway mat.24 Proper identification of VMSS facilitates determination of the appropriate rehabilitative management, which involves lenses/ prisms described below in conjunction with searching and scanning techniques while sitting, standing, and eventually walking.

Treatment Interventions Based on the individual’s rehabilitation goals and results of the neuro-optometric rehabilitation evaluation, the treatment options may include: 1. Compensatory lenses (i.e., spectacles or contact lenses) for nearsightedness, farsightedness, and/or astigmatism to optimize the clarity of eyesight. 2. Therapeutic lenses/prisms that are incorporated 1 into the individuals’ glasses prescription to minimize eyestrain, enhance visual spatial abilities, and improve visual field awareness. Examples include yoked prisms, field-expanding lenses, and spotting prisms.1,21,22,24 3. Tinted lenses to relieve light sensitivity for either outdoor and/or indoor and anti-reflective coating to minimize glare when driving at night or using a computer screen. 1,25 ,27 4. Neuro-optometric rehabilitation therapy (NORT) to rehabilitate any visual processing or visual attention deficits that interfere with ADLs. Details about NORT are described in Ciuffreda et al. 26 and Tannen and Cohen. 27

Summary Incorporating expertise from neuro-optometry, neuropsychology, and physical medicine and rehabilitation, this article provides an overview of the current symptom assessment, evaluation techniques, and intervention options of visual processing, visual attention, and visual field integrity that can improve treatment outcomes and opportunities for individuals with brain injuries. References 1 Suter PS and Harvey LH, editors: Vision Rehabilitation: Multidisciplinary Care of the Patient Following Brain Injury. New York, NY: Taylor and Francis Group,2011. 2 Steinman S and Steinman B: Visual attention: basic and clinical aspects. In: Intention, Attention, Inattention and Neglect. S Super, editor: Optometric Extension Program Foundation, Santa Ana, CA: Pages 47-79,2011. 3 Adams E: Visual problems in traumatic brain injury: a systematic review of sequelae and interventions for the veteran population. Briefing to the Consensus Validation Panel. Department of Veterans Affairs. VHA Office of Patient Care—Technology Assessment Program. May 2009.

11 Stone SP, Halligan PW, Greenwood RJ, The incidence of neglect phenomena and related disorders in patients with an acute right or left hemisphere stroke. Age and Ageing. 22(1):46-52,1993. 12 Craig SB, Kapoor N, Ciuffreda KJ, et al., Profile of selected aspects of visually-symptomatic individuals with acquired brain injury: a retrospective study. J Behav Optom. 19(1):7-10,2008. 13 Laukkanen H, Scheiman M, Hayes JR, Brain Injury Vision Symptom Survey (BIVSS) Questionnaire. Optom Vis Sci. 94(1):43-50,2017. 14 Shahinfar S, Johnson LN, Madsen RW, Confrontation visual field loss as a function of decibel sensitivity loss on automated static perimetry: implications on the accuracy of confrontation visual field testing. Ophthalmology. 103(6):872-877,1995. 15 Johnson LN, Baloh FG, The accuracy of confrontation visual field test in comparison with automated perimetry. J National Medical Assoc. 83(10):895-8,1991. 16 Umbel TMS, Baxstrom C, Multi-sensory factors when examining visual fields in unilateral spatial inattention and its effects on treatment. Optom Vis Perf. 3(6):317-323,2015. 17 Suchoff IB, Ciuffreda K, A primer for the optometric management of unilateral spatial inattention. Optometry. 75(5):305-19,2004. 18 Lovell M: The ImPACT neuropsychological test battery. In: Sports Neuropsychology: Assessment and Management of Traumatic Brain Injury. Echemendia RJ (Ed) New York, NY: Guildford Press. Pages 193215,2006. 19 Schatz P, Pardini J, Lovell M, et al., Sensitivity and specificity of the ImPACT test battery for concussion in athletes. Arch Clin Neuropsychol. 21(1):91-9,2006. 20 Schatz P and Sandel N, Sensitivity and specificity of the online version of ImPACT in high school and collegiate athletes. Am J Sports Med. 41(2):321-326,2013.

4 Konigs M, Weeda W, Van Heurn L, et al., Impaired visual integration in children with traumatic brain injury: an observational study. Plos One. 10(12):1-15,2015.

21 Bansal S, Han E, Ciuffreda K, Use of yoked prisms in patients with acquired brain injury: a retrospective analysis. Brain Injury. 28:1441-6,2014.

5 Konigs M, Weeda W, Van Heurn L, et al., Pediatric traumatic brain injury affects multisensory integration. Neuropsychology. 31(2):137-48,2017.

22 Padula W, Nelson C, Padula W, et al., Modifying postural adaptation following a CVA through prismatic shift of visuo-spatial egocenter. Brain Injury. 23:566-576,2009.

6 D’Hondt F, Lassonde M, Thebault-Dagher F, et al., Electrophysiological correlates of emotional face processing after mild traumatic brain injury in preschool children. Cognitive, Affective & Behavioral Neuroscience. 17(1):124-42,2017.

23 Tong D, Cao J, Beaudry A, et al., High prevalence of visual midline shift syndrome in TBI. Vision Dev & Rehab. 2(3):176-84,2016.

7 Genova, H, Rajagopalan V, Chiaravalloti N, et al., Facial affect recognition linked to damage in specific white matter tracts in traumatic brain injury. Social Neuroscience. 10(1):27-34,2015. 8 Wang X, Hong X, Cotton A, et al., Early changes in cortical emotion processing circuits after mild traumatic brain injury from motor vehicle collision. Journal of Neurotrauma. 34(2):273-80,2017.

24 Padula WV, Subramanian P, Spurling A, et al., Risk of fall (RoF) intervention by affecting visual egocenter through gait analysis and yoked prisms. NeuroRehabil. 37:305-14,2015. 25 Suchoff IB, Ciuffreda KJ, and Kapoor N, editors: Visual and Vestibular Consequences of Acquired Brain Injury. Santa Ana, CA: Optometric Extension Program Foundation,2001.

9 Suchoff I, Kapoor N, Ciuffreda K, et al., The frequency of occurrence, types and characteristics of visual field defect in acquired brain injury: a retrospective analysis. Optometry. 79:259-65,2008.

26 Ciuffreda KJ, Capo-Aponte J, Peddle A, et al., Efferent-based oculomotor dysfunctions in chronic mild traumatic brain injury (mTBI): diagnostic and treatment aspects. Brain Injury Professional. 15 (3): 16-21, 2018.

10 Alvarez T, Kim E., Vicci V, et al., Concurrent vision dysfunctions in convergence insufficiency with traumatic brain injury. Optom Vis Sci. 89(12):1740-51,2012.

27 Tannen B and Cohen A, Neuro-optometric rehabilitation for the sensory-triggered anomalies associated with mild traumatic brain injury. Brain Injury Professional. 15 (3): 22-27, 2018.

Author Bios Derek Tong OD, FAAO, FCOVD, FNORA, has been practicing optometry for 20 years with a strong focus on Neuro-Optometric Rehabilitation and Vision Therapy. He is founder, clinic director and post-doctorate supervisor of the Center for Vision Development Optometry Inc. in in Pasadena, California and Adjunct Clinical Assistant Professor of the Southern California College of Optometry at Marshall B. Ketchum University. Marcel Ponton PhD, is a clinical neuropsychologist with 30 years of experience in head injury assessment and treatment. He is also an Associate Clinical Professor in the Department of Psychiatry at UCLA, and a Fellow of the National Academy of Neuropsychology. He is Clinical Director of Persona Neurobehavior Group and practices in Pasadena, CA. Wei-Ching Lee MD, is a UCLA-trained Physiatrist and Independent Medical Examiner in Arcadia, California. She is a Board-certified Diplomate of American Board of Physical Medicine & Rehabilitation and serves as California Medical Association delegate of Los Angeles County. Tonya Umbel OD, FNORA is Fellowship-trained in Neuro-Optometric Rehabilitation and completed a Post-doctorate in Vision Therapy & Rehabilitation. She is a travelling optometrist who provides vision care in nursing homes throughout West Virginia. DeAnn Fitzgerald OD, is the founder and clinic director of Dr. D.M. Fitzgerald and Associates in Cedar Rapids, Iowa. She is also the Vice President of the Neuro-Optometric Rehabilitation Association (NORA), an international, non-profit, optometric organization based in the US that embraces a multi-disciplinary approach to maximize treatment outcome of individuals who suffer TBI, stroke and other physical disabilities. Please visit www.noravisionrehab.com for further information.

BRAIN INJURY professional 31

BIP

expert interview

with Dr. Kenneth J. Ciuffreda Kenneth J. Ciuffreda, OD, PhD is a Distinguished Teaching Professor at the SUNY/State College of Optometry in New York City and a world-renowned vision scientist. Dr. Ciuffreda is best known for his expertise in understanding the mechanisms of accommodation and eye movements in those with and without acquired brain injury (ABI). Having received many awards and honors throughout his illustrious career, he is the appropriate expert to be interviewed for this special issue on neuro-optometry.

Kenneth J. Ciuffreda, OD, PhD Q. During your early years of research, who were your mentors? Are there skills that they instilled in you that you retain and now instill in your graduate students? A. During my early years, and beyond, I was so fortunate to have a constellation of mentors who influenced and impacted on my research and the multitude of directions it has taken over the past nearly fifty years. First, there were several who directly influenced my research direction and thinking. Primary was my Ph.D. advisor, Larry Stark, a neurologist and bioengineer at Berkeley. Others included Meredith Morgan, Jay Enoch, Gerald Westheimer, Glenn Fry, Robert Kenyon, and Terry Bahill. More generally with respect to optometric and clinical thinking, these included Norman Haffner, Gordon Heath, Henry Peters, Diana Ludlam, Neera Kapoor, Monroe Hirsch, and of course Irwin Suchoff who was primary in introducing me to the wonderful world of acquired brain injury (ABI) and the important role of the neurooptometrist in treating these patients. There were a multitude of attributes and skills that these mentors instilled in me, and then me to my graduate students and visiting professors. These included: hard work, critical and clear thinking, scholarliness, research ethics, seriousness, and clear writing. Q. Please tell our readers more about who or what piqued your interest to transition from studying efferent (motor) vision in those without brain injury to those with ABI.

Q. Since 2013 or so, you have been increasing your investigational focus into afferent vision in ABI, especially mild traumatic brain injury (mTBI)/concussion, more specifically light sensitivity and visual motion sensitivity. Please share with our readers what prompted this shift in your research.

A. Well, to some extent, I have always been involved and interested in neurological conditions given the fact that Larry Stark was a neurologist. In fact, we started the first neuro-optometry clinic at Berkeley in 1975. One of the first published papers from that clinic was a series of case reports, one or more dealing with cerebrovascular accident and the adverse impact of the residual hemianopia on the reading process. However, the real turning point occurred about twenty-five years ago. I was absorbed in the study of vergence eye movements and its neurological control in normal individuals, working with my colleagues George Hung and John Semmlow at the Rutgers University bioengineering department. One day, however, Irwin Suchoff, who had started the brain injury clinic at SUNY College of Optometry, called me down to the clinic to see two of his patients. They were so fascinating, that I shifted much of my research interest to patients with ABI and the adverse effects on the oculomotor system, including vergence and reading aspects. And, I have remained in the field over these past two decades or so. No regrets!

A. Well, there are several reasons. First, it is an interesting area that I had rarely explored. My problem is that I am interested in everything in ABI, and in the world, so why not? Second, the decision was driven by practical aspects: my new graduate students were interested in afferent aspects of visual processing in ABI. Third, I had earlier begun a series of experiments dealing with the visualevoked potential (VEP) in mTBI, and a natural extension was the use of binasal occluders (BNO) to reduce visual motion sensitivity using objective assessment of cortical responsivity with and without the BNO, which had a significant positive effect. Fourth, my last Ph.D. student was interested in photosensitivity in these patients. This led to a series of pupil experiments in this population, which revealed a range of subtle abnormalities that cannot be detected with the naked eye in the clinic. We also determined that several of these dynamic, objectively-based, pupillary parameters can likely serve as biomarkers for the presence of mTBI/concussion. These pupillary experiments were conducted in adults, and we are now extending these studies to children having acute-phase sports-related

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concussion, with doctors at Children’s Hospital of Philadelphia, including Dr. Tina Master. Thus, there were many reasons for the transition to afferent aspects, and again I have no regrets. So exciting! Q. Please tell the readers what you feel are the next stages for investigating sensorimotor vision dysfunction in those with mTBI/ concussion. A. There are at least three new frontiers to conquer. The first is the determination of objectively-based, vision biomarkers which will assist in the diagnosis. We have already begun this research in the laboratory: some likely parameters included peak vergence velocity, peak accommodative velocity, and peak pupillary dilation velocity, and more. This area will advance as the technology and software become more sophisticated while remaining user-friendly for the doctor and therapist. The second is incorporating brain imaging techniques, such as diffusion tensor imaging, to assist in the initial diagnosis at baseline as well as assess the effects of a vision intervention, such as neuro-optometric rehabilitation, on brain centers with initially reduced responsivity. This is currently being studied at some optometric research centers. Lastly, and related to the above, is a more widespread investigation for the most optimal, efficacious, and long-lasting neuro-optometric rehabilitation using a range of clinical techniques and metrics. These would include objective assessment of the system under study, such as measuring static and dynamic aspects of accommodation before and after some vision intervention. It would likely involve a randomized clinical trial (RCT), perhaps studying therapeutic dose effects, the interactive effects of different therapies, or novel treatments such as acupuncture and oculomotor-based feedback therapy. One could also incorporate several mathematical approaches, such as power spectrum analysis, ROC (receiving operator characteristic) analysis, and the root-mean square (rms) technique, all of which we have used, as well as others. Thus, the future appears to be bright for our patients with ABI. I thank the Brain Injury Professional, and Dr. Kapoor, for allowing me to express my thoughts in this interview to your readers.

Neera Kapoor, OD, MS

About the Interviewer Dr. Neera Kapoor graduated with a Masters of Vision Sciences, Doctor of Optometry, and Residency in Vision Therapy and Rehabilitation, all at SUNYCollege of Optometry in the mid-1990s. She served as Chief of Vision Rehabilitation Services from June 2010 through early July 2015 and remained at SUNY College of Optometry through early 2016.

BIO: In early 2016, she transitioned from SUNY-College of Optometry to • Dr. Neera Kapoor graduated a Masters NYU-School of Medicine, where she is Clinicalwith Associate Professorof Vision Sciences, Doctor of Optometry, and of Rehabilitation Medicine and provides clinical careRehabilitation, as a neuroResidency in Vision Therapy and all at SUNY-College of Optometry in the optometrist at NYU-Langone Health's RUSK Institute of Rehabilitation mid-1990s. Medicine. • She served as Chief of Vision Rehabilitation Services from June 2010 through early July Dr. Kapoor co-authored overat 30SUNY peer-reviewed articles, 2015hasand remained College of10Optometry through early 2016. textbook chapters, and 25 poster presentations, and has presented • 110 In lectures early 2016, transitioned from SUNY-College of Optometry to NYU-School of over regionally,she nationally, and internationally, regarding visionMedicine, and acquired brain injury.she is Clinical Associate Professor of Rehabilitation Medicine and where provides clinical care as a neuro-optometrist at NYU-Langone Health's RUSK Institute of Rehabilitation Medicine. • Dr. Kapoor has co-authored over 30 peer-reviewed articles, 10 textbook chapters, andINJURY 25 BRAIN professional 33 poster presentations, and has presented over 110 lectures regionally, nationally, and

events 2018 September â&#x20AC;&#x201C; October 20: Conference EBIS, September 20, Brussels, Belgium. For more information, visit ebissociety.org. 26 - 28: Third International Conference on Paediatric Acquired Brain Injury, September 26 -28, Belfast, Northern Ireland. For more information, visit interrnationalbrain.org. 30 - 3: ACRM 95th Annual Conference, September 30 - October 3, Dallas, Texas. For more information, visit acrm.org. November 15-16: Toronto ABI Network Conference, November 15 - 16, Toronto, Ontario, Canada. For more information, visit abinetwork.ca/abi-conference-2018. 15 â&#x20AC;&#x201C; 17: ASHA Convention, November 15-17, Boston, MA, USA. For more information, visit convention.asha.org.

2019 March 13 - 16: IBIA 13th World Congress on Brain Injury, March 13-16, Toronto, Ontario. For more information, visit ibia2019.org. 13 -16: North American Brain Injury Society 32rd Annual Conference on Legal Issues in Brain Injury, March 13 -16, Toronto, Ontario, Canada. For more information, visit nabis. org. April 4 - 7: AOTA Annual Conference & Expo, April 4-17, New Orleans, LA, USA. For more information, visit aota.org. June 9-13: 13th International Society of Physical and Rehabilitation Medicine World Congress, June 9 - 13, Kobe, Japan. For more information, visit isprm2019.com.

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ophthalmic terms accommodation: the ability to change focus and maintain a clear image of an object (when looking from far to near and vice versa), using the eyeâ&#x20AC;&#x2122;s crystalline lens-based mechanism. accommodative amplitude: the closest point of clear vision, typically performed monocularly. astigmatism: unequal refractive error in orthogonal meridians of the eye; when rays of light from infinity come to a focus at different distances relative to the retina, with accommodation minimally stimulated. binocular: viewing with two eyes at the same time. convergence insufficiency: the vision diagnosis presenting with exophoria greater at near than far, with a receded near point of convergence and reduced relative fusional convergence at near. diopter: unit of lens power esophoria: the lines of sight intersect in front of the plane of regard when fusion is disrupted. esotropia: the lines of sight intersect in front of the plane of regard when fusion is not disrupted (i.e., under normal binocular viewing conditions). exophoria: the lines of sight intersect beyond the plane of regard when fusion is disrupted. exotropia: the lines of sight intersect beyond the plane of regard when fusion is not disrupted (i.e., under normal binocular viewing conditions). fixation: ocular alignment with the image of the fixated target falling on the fovea; may be performed one eye at a time (i.e., monocularly) or with both eyes at the same time (i.e., binocularly). fusion: single, cortically-integrated vision under binocular viewing conditions. hemianopsia: hemi-field visual field defect, which may be unilateral or bilateral (i.e., homonymous or bitemporal). heterophoria: the position of the eyes when fusion is disrupted. heterotropia (i.e., strabismus): the position of the eyes when fusion is not disrupted (i.e., under normal binocular viewing conditions). hyperopia: far-sightedness; when rays of light from infinity come to a focus behind the eye, with accommodation minimally stimulated. monocular: viewing with one eye at a time. myopia: near-sightedness; when rays of light from infinity come to a focus in front of the eye, with accommodation minimally stimulated. near point of convergence: the closest point of binocular, fused, single vision. nystagmus: rapid involuntary oscillation or movement of the eyes, the presence or absence of which may be diagnostic of neurological and vision disorders. orthophoria: the lines of sight intersect precisely at the plane of regard when fusion is disrupted. prism diopter: unit of prism power presbyopia: normal age-related, physiological loss of accommodation. pursuit: slow, continuous, and conjugate eye movement used when the eyes follow an object as it is moved slowly and smoothly. relative accommodative range: the range over which the accommodative system can be stimulated by the addition of plus (i.e., negative relative accommodation) and minus (i.e., positive relative accommodation) lenses binocularly and still maintain clear, single vision at near (40 cm). relative fusional range: the range over which the vergence system can be stimulated by the addition of prisms binocularly and still maintain single, binocular vision at both distance (6 m) and near (40 cm). Three parameters are recorded: the first is the amount of prism at which the patient reports blurred vision; the second is the amount of prism at which the patient reports diplopia; and, the third is the amount of prism at which the patient regains fusion. saccade: rapid, step-like conjugate eye movement that redirects the line of sight from one position to another. stereopsis: relative depth perception strabismus (i.e., heterotropia): the position of the eyes when fusion is not disrupted (i.e., under normal binocular viewing conditions). vergence: the disjunctive movement of the eyes to track targets moving in depth. versional eye movements: the conjunctive movement (including fixation, pursuit, and saccade) of the eyes to follow targets moving laterally, vertically, or obliquely in one plane, with no change in depth.

SAVE THE DATE/CALL FOR ABSTRACTS! THE I N T E R N A T I O N A L B R A I N INJURY ASSOCIATION PRESENTS THE

13 TH WORLD CONGRESS ON BRAIN INJURY MARCH 13-16, 2019 SHERATON CENTRE HOTEL TORONTO, ONTARIO CANADA

WWW.IBIA2019.ORG

ABSTRACTS DUE: NOVEMBER 19, 2018 WWW.IBIA2019.ORG

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PHOTO BY HERMAN PRIVETTE

Madison Schwartz, Stanford Law, Randall H. Scarlett, Randall A. Scarlett, Ronnie Pang, Olga Rios, Mary Anne Scarlett, and Brendan D. Nay.

SCARLETT LAW GROUP Scarlett Law Group is a premier California personal injury law firm that in two decades has become one of the state’s go-to practices for large-scale personal injury and wrongful death cases, particularly those involving traumatic brain injuries. With his experienced team of attorneys and support staff, founder Randall Scarlett has built a highly selective plaintiffs’ firm that is dedicated to improving the quality of life of its injured clients. “I live to assist people who have sustained traumatic brain injury or other catastrophic harms,” Scarlett says. “There is simply no greater calling than being able to work in a field where you can help people obtain the treatment they so desperately need.” To that end, Scarlett and his firm strive to achieve maximum recovery for their clients, while also providing them with the best medical experts available. “As a firm, we ensure that our clients receive both

the litigation support they need and the cutting-edge medical treatments that can help them regain independence,” Scarlett notes. Scarlett’s record-setting verdicts for clients with traumatic brain injuries include $10.6 million for a 31-year-old man, $49 million for a 23-year-old man, $26 million for a 7-year-old, and $22.8 million for a 52-year-old woman. In addition, his firm regularly obtains eight-figure verdicts for clients who have endured spinal cord injuries, automobile accidents, big rig trucking accidents, birth injuries, and wrongful death. Most recently, Scarlett secured an $18.6 million consolidated case jury verdict in February 2014 on behalf of the family of a woman who died as a result of the negligence of a trucking company and the dangerous condition of a roadway in Monterey, Calif. The jury awarded $9.4 million to Scarlett’s clients, which ranks as

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one of the highest wrongful death verdicts rendered in recent years in the Monterey County Superior Court. “Having successfully tried and resolved cases for decades, we’re prepared and willing to take cases to trial when offers of settlement are inadequate, and I think that’s ultimately what sets us apart from many other personal injury law firms,” observes Scarlett, who is a Diplomate of the American Board of Professional Liability Attorneys. In 2015, Mr. Scarlett obtained a $13 million jury verdict for the family of a one year old baby who suffered permanent injuries when a North Carolina Hospital failed to diagnose and properly treat bacterial meningitis that left the child with severe neurological damage. Then, just a month later, Scarlett secured an $11 million settlement for a 28-year-old Iraq War veteran who was struck by a vehicle in a crosswalk, rendering her brain damaged.