Advances in Understanding Mechanisms and Treatment of

Infantile Forms of Nystagmus

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Library of Congress Cataloging-in-Publication Data

Advances in understanding mechanisms and treatment of infantile forms of nystagmus / edited by R. John Leigh, Michael Devereaux.
p.; cm.
Result of a meeting held on May 3-4, 2007 at the Louis Stokes Cleveland Dept. of Veterans Affairs Medical Center.
Includes bibliographical references and index.
ISBN 978-0-19-534218-5
1. Nystagmus—Congresses. 2. Pediatric ophthalmology—Congresses. 3. Infants—Diseases—Congresses. 4. Vision in infants—Congresses. I.
Leigh, R. John. II. Devereaux, Michael.
[DNLM: 1. Nystagmus, Congenital—Congresses. 2. Eye Movements—physiology—Congresses. 3. Nystagmus, Congenital—therapy—
Congresses. 4. Strabismus—Congresses. WW 410 A244 2008]
RE748.A38 2008
618.92’0977—dc22 2007046222

987654321
Printed in the United States of America
on acid-free paper
 Foreword and Acknowledgments

Since the contributions of Hubel and Wiesel, substan- have been his contributions to developing treatments
tial advances have been made in understanding the of infantile forms of nystagmus, especially in suggest-
developmental biology of the visual system, leading ing and evaluating new surgical procedures. Beyond
to therapies for amblyopia. However, disorders of eye his scientific contributions, Dr. Dell’Osso brings a
movements that arise early in life remain a major chal- personal understanding to those individuals who are
lenge for ophthalmologists, pediatricians, and neuro- visually disabled by congenital forms of nystagmus;
logists. Recently, basic studies of infantile nystagmus this empathy is appreciated by the numerous patients
have provided new approaches, including psycho- that he has evaluated over four decades.
physical techniques, development of animal models, This volume is the result of a meeting held May 3–
genetic linkage studies, and trials of gene therapy. 4, 2007, under the auspices of Case Western Reserve
Over the past 40 years, Louis F. Dell’Osso has University, to celebrate Dr. Dell’Osso’s contributions
made major contributions to our understanding of nys- and the opening of the Daroff-Dell’Osso Laboratory
tagmus that begins in infancy. Starting with an engi- at the Louis Stokes Cleveland Department of Veterans
neering approach to the control of eye movements, he Affairs Medical Center. The meeting was made pos-
applied principles of linear control systems to a range sible through generous support from the Mt. Sinai
of ocular oscillations, including congenital nystagmus Health Care Foundation and the Garson Fund of Cleve-
(now termed infantile nystagmus syndrome) and latent land, Ohio. The goal of the meeting was to apply basic
nystagmus (now termed fusional maldevelopment nys- information about eye movements in order to better
tagmus syndrome). Dr. Dell’Osso’s first efforts defined understand the pathophysiology of infantile forms of
these ocular oscillations with reliable measurements and nystagmus and develop new therapies.
classified the forms of nystagmus on the basis of their The first section of this book, “Basic Concepts
waveforms. He then applied this knowledge to better of Stable Vision and Gaze,” comprises five chapters
understand how such nystagmus disturbs a clear view of that address psychophysical aspects of vision in nor-
the world and how reliable measurements of nystagmus mal subjects and individuals with nystagmus and the
can be used to predict each individual’s visual potential. relative contributions of afference (extraocular pro-
Throughout his career, Dr. Dell’Osso’s engineering prioception) versus efference (internal copies of the
background has led to development of mathematical ocular motor commands). The influence of extraocular
models to account for the underlying pathophysiol- proprioception on the control of gaze has been con-
ogy of disturbed gaze control. More recently, he has sidered minor compared with “efference copy” or
been involved with animal models of infantile nystag- “corollary discharge” of the ocular motor commands.
mus due to specific genetic disorders, which hold the However, anatomical studies by Jean Büttner-Ennever
promise of human gene therapy. Equally significant and colleagues have identified a possible mechanism

v
 vi FOREWORD AND ACKNOWLEDGMENTS

for proprioception located near the insertion of non- The third section, “New Therapies for Congeni-
twitch extraocular muscles in the eyeball. Recent stud- tal Nystagmus,” applies basic studies to develop a
ies by Michael E. Goldberg et al. have established that range of new therapies. Dr. Gottlob reports linkage
extraocular proprioception projects to the frontal eye to chromosome Xq26-q27 in patients with idiopathic
fields, where it may influence the programming and congenital nystagmus, leading to detection of a novel
consequences of gaze shifts. gene; she also reports that both memantine and gabap-
In Part 1, Dr. Steinbach, an abiding proponent of entin suppress some forms of infantile nystagmus and
extraocular proprioception, reports that in normal sub- support modest improvement of vision. Better identi-
jects the Jendrassik maneuver (voluntary, forceful con- fication of genotypes of infantile nystagmus may ulti-
traction of arm muscle groups) affects the registered mately enhance our ability to treat individual patients.
vergence eye position, possibly by changing activity Dr. Dell’Osso summarizes his singular contributions to
in the non-twitch muscle fibers–proprioceptive loop. several approaches to treating infantile forms of nystag-
Dr. Bedell summarizes a series of studies of the mech- mus—the importance of reliable measurements, the use
anisms for lack of oscillopsia in infantile nystagmus of these measurements to predict potential visual acuity,
syndrome and provides evidence for reduced percep- and evaluation of tenotomy and resuture surgical thera-
tual responses when the eyes are in motion. An acces- pies in clinical trials. Dr. Hertle provides the results of a
sible and useful review of current notions of spatial large study of such surgical treatment of those patients
and temporal visual functions and spatial constancy in with infantile forms of nystagmus that periodically
infantile nystagmus syndrome and latent nystagmus reverse direction. Dr. Tomsak provides a summary of
is provided by Dr. Abadi. Dr. Abel supplements this preliminary studies of tenotomy-and-resuture surgical
information by highlighting the effect of psychological therapies for acquired pendular and downbeat forms
factors on infantile nystagmus. Finally, Dr. Proudlock of nystagmus, with promising results in three patients.
presents evidence that perceptual fading in normal Finally, Dr. Kaminski and colleagues provide a molecu-
subjects is influenced by efference commands for eye lar biological approach to the treatment of a disorder
movements that commonly causes double vision—myasthenia
Part 2, “New Models and Techniques for Study- gravis—suggesting that complement inhibitor drugs
ing Gaze Stability,” opens with two chapters concern- may usher in a new therapeutic approach.
ing animal models of disorders causing nystagmus. Dr. Dell’Osso’s legacy in training scientists is
Developmental models for strabismus and amblyo- evident in the final section of this volume, “General
pia in primates also provide an opportunity to study Aspects of Normal and Abnormal Gaze Control,”
the nystagmus that often coexists with these condi- which is a compendium of shorter contributions from
tions. Dr. Das reports the effects of experimentally some of his former students. These chapters deal with a
induced strabismus on programming of voluntary sac- broad range of aspects of normal gaze control, infantile
cades, noting that reaction time (latency) depends on nystagmus, and acquired disorders of eye movements,
whether viewing is monocular or binocular. Cerebel- including new treatment measures. Further informa-
lar lesions in adults induce well-defined disturbances tion about the conference and some supplementary
of eye movements that resemble human disease syn- material are available at the Daroff-Dell’Osso Ocular
dromes. Dr. Walker extends this work by demonstrat- Motility Laboratory Web site (http://omlab.org).
ing that cerebellar nodulus lesions also impair the We thank the Mt. Sinai Health Care Foundation and
linear (translational) vestibulo-ocular reflex. The final the Garson Fund for providing financial support for this
two chapters in this section deal with new technolo- conference-symposium. Robert Garson was a longtime
gies. One approach to managing nystagmus has been member of the Board of Trustees at the Mt. Sinai Med-
to attempt to cancel the visual consequences of the ical Center and University Hospitals of Cleveland. The
ocular oscillations with optical devices. A high-tech fund was established by his family in his honor, and
version developed by Dr. Stahl incorporates mov- we thank the Garson family for their generous support.
ing prisms that are driven with signals derived from We are grateful to Ann Rutledge, who provided invalu-
recorded eye movements. Although this device is able administrative assistance during the conference
likely to improve vision in patients with acquired and the preparation of this volume. We would also
nystagmus, it may not help individuals with infan- like to take this opportunity to acknowledge support
tile nystagmus syndrome. Video displays, including of research at the Daroff-Dell’Osso Laboratory by the
miniaturized portable screens, are now an important U.S. Department of Veterans Affairs, the National Eye
part of our lives, especially the lives of our children, Institute, and the Evenor Armington Fund.
who are enchanted by video games. Dr. Tabuchi docu-
ments the potential effects of video displays on the R. John Leigh, MD
response to near viewing by children, of whom 20% Michael W. Devereaux, MD
show abnormal pupillary responses. July 2007
 Contents

Contributors ix 7. Effects of Cerebellar Lesions in Monkeys

on Gaze Stability 55
Part I Basic Concepts of Stable Vision MARK F. WALKER, JING TIAN, XIAOYAN SHAN,
and Gaze RAFAEL J. TAMARGO, HOWARD YING, AND
DAVID S. ZEE
1. Afferent and Efferent Contributions to
Knowledge of Eye Position 3 8. Development of Visual Stabilization
EWA NIECHWIEJ-SZWEDO AND MARTIN J. Devices with Applications for Acquired and
STEINBACH Infantile Nystagmus 61
JOHN S. STAHL, IGOR S. KOFMAN, AND ZACHARY
2. Perceptual Influences of the Extraretinal C. THUMSER
Signals for Normal Eye Movements and
Infantile Nystagmus 11 9. Pupil Abnormalities of the Near Response
HAROLD E. BEDELL, JIANLIANG TONG, SAUMIL S. in Children with Visual Display Terminal
PATEL, AND JANIS M. WHITE Syndrome 70
AKIO TABUCHI, ATSUSHI FUJIWARA, AND
3. Perception with Unstable Fixation 23 MAHMOODI KHADIJA
RICHARD V. ABADI

4. Internal and External Influences on Part III New Therapies for Congenital
Foveation and Perception in Infantile Nystagmus
Nystagmus Syndrome 33
LARRY A. ABEL AND LINDA MALESIC 10. Genetics and Pharmacological Treatment
of Nystagmus: A Review of the Literature
5. Perceptual Fading during Voluntary and and Recent Findings 79
Involuntary Eye Movements 42 IRENE GOTTLOB
FRANK A. PROUDLOCK, ASTRID Y. JORGENSEN,
AND IRENE GOTTLOB 11. New Treatments for Infantile and Other
Forms of Nystagmus 87
LOUIS F. DELL’OSSO
Part II New Models and Techniques for
Studying Gaze Stability 12. Clinical and Electrophysiological Effects
of Extraocular Muscle Surgery on
6. Alternating Saccades in a Primate Model of Fifty-three Patients with Infantile
Strabismus 47 Periodic Alternating Nystagmus 99
VALLABH E. DAS RICHARD W. HERTLE, LEAH REZNICK,
DONGSHENG YANG, AND KIMBERLY ZOWORTY

vii
 viii CONTENTS

13. Eye Muscle Surgery for Acquired Forms 21. Posterior Internuclear Ophthalmoplegia
of Nystagmus 112 of Lutz Revisited: Report of a Case
ROBERT L. TOMSAK, LOUIS F. DELL’OSSO, Associated with a Midbrain Lesion 156
JONATHAN B. JACOBS, ZHONG I. WANG, AND BERND F. REMLER AND R. JOHN LEIGH
R. JOHN LEIGH
22. Divergence Insufficiency Associated with
14. The Complement Hypothesis to Explain Hereditary Spinocerebellar Ataxia 162
Preferential Involvement of Extraocular DAVID G. MORRISON, SEAN P. DONAHUE, AND
Muscle in Myasthenia Gravis 117 PATRICK J. M. LAVIN
HENRY J. KAMINSKI, YUEFANG ZHOU, JINDRICH
SOLTYS, AND LINDA L. KUSNER 23. Neuromuscular Junction Dysfunction in
Miller Fisher Syndrome 167
JANET C. RUCKER
Part IV General Aspects of Normal and
Abnormal Gaze Control 24. Involuntary Version-Vergence Nystagmus
Induced by Ground-Plane Optic Flow:
15. Studies of the Ability to Hold the Eye in Analysis of Dynamic Characteristics of
Eccentric Gaze: Measurements in Normal Nystagmus Quick Phases 170
Subjects with the Head Erect 129 DONGSHENG YANG, MINGXIA ZHU, AND
JEFFREY T. SOMERS, MILLARD F. RESCHKE, ALAN H. RICHARD W. HERTLE
FEIVESON, R. JOHN LEIGH, SCOTT J. WOOD,
WILLIAM H. PALOSKI AND LUDMILA KORNILOVA 25. The Neuro-ophthalmologic Complications
of Chiropractic Manipulation 175
16. Effect of Eye Exercise on Clinical MICHAEL W. DEVEREAUX
Outcome of Noncompressive Ocular
Motor Nerve Palsy 136 26. Vergence Hysteresis in Infantile
ANUCHIT POONYATHALANG, PISIT PREECHAWAT, Nystagmus 180
AND VITOO JANVIMALUANG ALESSANDRO SERRA, LOUIS F. DELL’OSSO, AND
ZHONG I. WANG
17. Expanding the Original Behavioral
Infantile Nystagmus Syndrome Model 27. Using Wavelet Analysis to Evaluate
to Jerk Waveforms and Gaze-angle Effects of Eye and Head Movements on
Variations 139 Ocular Oscillations 184
ZHONG I. WANG, LOUIS F. DELL’OSSO, AND KE LIAO, SIMON HONG, DAVID S. ZEE, LANCE M.
JONATHAN B. JACOBS OPTICAN, AND R. JOHN LEIGH

18. Extension of the eXpanded Nystagmus 28. Multifocal Electroretinographic Study

Acuity Function to Vertical and of Patients with Oculocutaneous Albinism
Multiplanar Data 143 and Infantile Nystagmus Syndrome 189
JONATHAN B. JACOBS AND LOUIS F. DELL’OSSO ELISA BALA, JONATHAN B. JACOBS, AND NEAL S.
PEACHEY
19. Inertial and Noninertial Contributions to the
Perception of Translation and Path 147 Index 193
SCOTT H. SEIDMAN

20. The Effect of the Duncker Visual Illusion

on Occluded Smooth-arm Tracking 152
ARI Z. ZIVOTOFSKY, ADI BERCOVICH, JASON
FRIEDMAN, EVA KELMAN, ELINOR SHINHERTZ,
AND TAMAR FLASH
 Contributors

Richard V. Abadi, PhD Louis F. Dell’Osso, PhD

Faculty of Life Sciences Daroff-Dell’Osso Ocular Motility Laboratory
University of Manchester Louis Stokes Cleveland Veterans Affairs Medical
Manchester, United Kingdom Center
Cleveland, Ohio
Larry A. Abel, PhD
Department of Optometry and Vision Sciences Michael W. Devereaux, MD
University of Melbourne Neurological Institute
Melbourne, Victoria, Australia University Hospitals Case Medical Center
Cleveland, Ohio
Elisa Bala, MD
Research Service Sean P. Donahue, MD, PhD
Cleveland Veterans Affairs Medical Center Vanderbilt Eye Institute
Cleveland, Ohio Vanderbilt University Medical Center/School
Nashville, Tennessee
Harold E. Bedell, PhD
College of Optometry and Center for Alan H. Feiveson, PhD
Neuro-Engineering and Cognitive Science Neurosciences Laboratories, Johnson Space Center
University of Houston National Aeronautics and Space Administration
Houston, Texas Houston, Texas

Adi Bercovich Tamar Flash, PhD

Gonda Multidisciplinary Brain Research Center Department of Computer Science and Applied
Bar Ilan University Mathematics
Ramat Gan, Israel Weizmann Institute of Science
Rehovot, Israel
Vallabh E. Das, PhD
Yerkes National Primate Research Center Jason Friedman
Emory University Department of Computer Science and Applied
Atlanta, Georgia Mathematics
Weizmann Institute of Science
Rehovot, Israel
ix
 x CONTRIBUTORS

Atsushi Fujiwara, CO Ludmila Kornilova, MD, PhD

Department of Sensory Science Institute of Biomedical Problems
Kawasaki University of Medical Welfare Moscow, Russia
Kurashiki, Okayama, Japan
Linda L. Kusner, PhD
Irene Gottlob, MD Department of Neurology and Psychiatry
Ophthalmology Group Saint Louis University
University of Leicester St. Louis, Missouri
Leicester, United Kingdom
Patrick J. M. Lavin, MD
Richard W. Hertle, MD Department of Neurology
Division of Ophthalmology Vanderbilt University Medical Center
Children’s Hospital of Pittsburgh Nashville, Tennessee
Pittsburgh, Pennsylvania
R. John Leigh, MD
Simon Hong, PhD Departments of Neurology, Biomedical Engineering,
Laboratory of Sensorimotor Research and Neurosciences
National Eye Institute, NIH, DHHS Case Medical Center
Bethesda, Maryland Cleveland, Ohio

Jonathan B. Jacobs, PhD Ke Liao, MS

Department of Neurology Department of Biomedical Engineering
Case Medical Center Case Western Reserve University
Cleveland, Ohio Cleveland, Ohio

Vitoo Janvimaluang, MD Linda Malesic, PhD

Department of Ophthalmology Department of Clinical Vision Sciences
Ramathibodi Hospital La Trobe University
Mahidol University Melbourne, Victoria, Australia
Bangkok, Thailand
David G. Morrison, MD
Astrid Y. Jorgensen, BSc Vanderbilt Eye Institute
University of Leicester Vanderbilt University Medical Center/School
Leicester, United Kingdom Nashville, Tennessee

Henry J. Kaminski, MD Ewa Niechwiej-Szwedo, BSc, MSc

Department of Neurology and Psychiatry Vision Science Research
Saint Louis University University of Toronto and Toronto Western Hospital
St. Louis, Missouri Toronto, Ontario, Canada

Eva Kelman Lance M. Optican, PhD

Gonda Multidisciplinary Brain Research Center Laboratory of Sensorimotor Research
Bar Ilan University National Eye Institute, NIH, DHHS
Ramat Gan, Israel Bethesda, Maryland

Mahmoodi Khadija, OD William H. Paloski, PhD

Department of Sensory Science Neurosciences Laboratories, Johnson Space Center
Kawasaki University of Medical Welfare National Aeronautics and Space Administration
Kurashiki, Okayama, Japan Houston, Texas

Igor S. Kofman, BSEE Saumil S. Patel, PhD

Louis Stokes Cleveland Veterans Affairs Medical Departments of Neurobiology and Anatomy
Center University of Texas Medical School
Cleveland, Ohio Houston, Texas
 CONTRIBUTORS xi

Neal S. Peachey, PhD Elinor Shinhertz

Research Service Gonda Multidisciplinary Brain Research Center
Cleveland Veterans Affairs Medical Center Bar Ilan University
Cleveland, Ohio Ramat Gan, Israel

Anuchit Poonyathalang, MD Jindrich Soltys, PhD

Department of Ophthalmology Department of Neurology and Psychiatry
Ramathibodi Hospital Saint Louis University
Mahidol University St. Louis, Missouri
Bangkok, Thailand
Jeffrey T. Somers, MS
Pisit Preechawat, MD Wyle Laboratories
Department of Ophthalmology Houston, Texas
Ramathibodi Hospital
Mahidol University John S. Stahl, MD, PhD
Bangkok, Thailand Department of Neurology
Case Western Reserve University
Frank A. Proudlock, PhD Cleveland, Ohio
University of Leicester
Leicester, United Kingdom Martin J. Steinbach, PhD
Vision Science Research
Bernd F. Remler, MD Toronto Western Hospital
Departments of Neurology and Ophthalmology Toronto, Ontario, Canada
MCW Clinics at Froedtert
Milwaukee, Wisconsin Akio Tabuchi, MD
Department of Sensory Science
Millard F. Reschke, PhD Kawasaki University of Medical Welfare
Neurosciences Laboratories, Johnson Space Center Kurashiki, Okayama, Japan
National Aeronautics and Space Administration
Houston, Texas Rafael J. Tamargo, MD, FACS
Departments of Neurosurgery and
Leah Reznick, MD Otolaryngology—Head and Neck Surgery
Division of Ophthalmology Johns Hopkins University School of Medicine
Children’s Hospital of Pittsburgh Baltimore, Maryland
Pittsburgh, Pennsylvania
Zachary C. Thumser, MBME
Janet C. Rucker, MD Louis Stokes Cleveland Veterans Affairs Medical
Department of Neurological Sciences Center
Rush University Cleveland, Ohio
Chicago, Illinois
Jing Tian, PhD
Scott H. Seidman, PhD Department of Neurology
University of Rochester Medical Center Johns Hopkins University School of Medicine
Rochester, New York Baltimore, Maryland

Alessandro Serra, MD Robert L. Tomsak, MD, PhD

Daroff-Dell’Osso Ocular Motility Laboratory Departments of Neurology and Ophthalmology
Louis Stokes Cleveland Veterans Affairs Medical Case Medical Center
Center Cleveland, Ohio
Cleveland, Ohio
Jianliang Tong, PhD
Xiaoyan Shan, MD, PhD College of Optometry
Department of Neurology University of Houston
Johns Hopkins University School of Medicine Houston, Texas
Baltimore, Maryland
 xii CONTRIBUTORS

Mark F. Walker, MD David S. Zee, MD

Departments of Neurology and Ophthalmology Departments of Neurology, Ophthalmology,
Johns Hopkins University School of Medicine Otolaryngology–Head and Neck Surgery, and
Baltimore, Maryland Neuroscience
Johns Hopkins University School of Medicine
Zhong I. Wang, MS Baltimore, Maryland
Department of Biomedical Engineering
Case Medical Center Yuefang Zhou, PhD
Cleveland, Ohio Department of Neurology and Psychiatry
Saint Louis University
Janis M. White, OD, PhD St. Louis, Missouri
Veterans Affairs New Jersey Health Care System
East Orange, New Jersey Mingxia Zhu, PhD
Laboratory of Visual and Ocular Motor Physiology
Scott J. Wood, PhD Children’s Hospital of Pittsburgh
Universities Space Research Association Pittsburgh, Pennsylvania
Houston Texas
Ari Z. Zivotofsky, PhD
Dongsheng Yang, PhD Gonda Multidisciplinary Brain Research Center
Division of Ophthalmology Bar Ilan University
Children’s Hospital of Pittsburgh Ramat Gan, Israel
Pittsburgh, Pennsylvania
Kimberly Zoworty
Howard Ying, MD, PhD Division of Ophthalmology
Department of Ophthalmology Children’s Hospital of Pittsburgh
Johns Hopkins University School of Medicine Pittsburgh, Pennsylvania
Baltimore, Maryland Advances in Understanding Mechanisms and
Treatment of Infantile Forms of Nystagmus
ADVANCES IN UNDERSTANDING
MECHANISMS AND TREATMENT OF
INFANTILE FORMS OF NYSTAGMUS
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 I
BASIC CONCEPTS OF
STABLE VISION AND GAZE
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