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THE NEUROLOGYOF EYE MOVEMENTS

THIRD EDITION

CONTEMPORARY NEUROLOGY SERIES AVAILABLE:

19THE DIAGNOSIS OF STUPOR AND COMA, EDITION 3 Fred Plum, M.D., and Jerome B. Posner, M.D.

26PRINCIPLES OF BEHAVIORAL NEUROLOGY M-Marsel Mesulam, M.D., Editor

32CLINICAL NEUROPHYSIOLOGY OF THE VESTIBULAR SYSTEM, EDITION 2 Robert W. Baloh, M.D., and Vincente Honrubia, M.D.

36DISORDERS OF PERIPHERAL NERVES, EDITION 2

Herbert H. Schaumburg, M.D., Alan R. Berger, M.D., and P.K. Thomas, C.B.E., M.D., D.Sc., F.R.C.R, F.R.C.Path.

38PRINCIPLES OF GERIATRIC NEUROLOGY

Robert Katzman, M.D., and John W. Rowe, M.D., Editors

42MIGRAINE: MANIFESTATIONS, PATHOGENESIS, AND MANAGEMENT Robert A. Davidoff, M.D.

43NEUROLOGY OF CRITICAL ILLNESS Eelco F. M. Wijdicks, M.D., Ph.D., F.A.C.P.

44EVALUATION AND TREATMENT OF MYOPATHIES

Robert C. Griggs, M.D., Jerry R. Mendell, M.D., and Robert G. Miller, M.D.

45 NEUROLOGIC COMPLICATIONS OF CANCER

Jerome B. Posner, M.D.

46CLINICAL NEUROPHYSIOLOGY Jasper R. Daube, M.D., Editor

47NEUROLOGIC REHABILITATION Bruce H. Dobkin, M.D.

48PAIN MANAGEMENT: THEORY AND PRACTICE

Russell K. Portenoy, M.D., and Ronald M. Kanner, M.D., Editors

49AMYOTROPHIC LATERAL SCLEROSIS

Hiroshi Mitsumoto, M.D., D.Sc., David A. Chad, M.D., F.R.C.P., and Eric P. Pioro, M.D., D.Phil., F.R.C.P.

50MULTIPLE SCLEROSIS

Donald W. Paty, M.D., F.R.C.P.C., and George C. Ebers, M.D., F.R.C.P.C.

51NEUROLOGY AND THE LAW: PRIVATE LITIGATION AND PUBLIC POLICY H. Richard Beresford, M.D., J.D.

52SUBARACHNOID HEMORRHAGE: CAUSES AND CURES Bryce Weir, M.D.

53SLEEP MEDICINE Michael S. Aldrich, M.D.

54BRAIN TUMORS

Harry S. Greenberg, M.D., William F. Chandler, M.D., and Howard M. Sandier, M.D.

55THE NEUROLOGY OF EYE MOVEMENTS, EDITION 3 R.John Leigh, M.D., and David S. Zee, M.D.

(book and CD-ROM versions available)

THE NEUROLOGYOF EYE MOVEMENTS

THIRD EDITION

R. John Leigh

Professor, Departments of Neurology, Neurosciences,

Otolaryngology, and Biomedical Engineering

Case Western Reserve University

University Hospitals and Department of

Veterans Affairs Medical Center

Cleveland, Ohio

David S. Zee

Professor of Neurology, Ophthalmology,

Otolaryngology and Head and

Neck Surgery, and Neuroscience

Director, Ocular Motor-Visual Testing Lab

Johns Hopkins University

Baltimore, Maryland

New York Oxford

OXFORD UNIVERSITY PRESS

1999

Oxford University

Press

 

 

 

Oxford

New York

 

 

 

 

 

Athens

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Dar es Salaam

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and associated companies in

 

 

 

Berlin

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Copyright © 1999 by Oxford University Press Inc.

Published by Oxford University Press Inc.,

198 Madison Avenue, New York, New York 10016

Oxford is a registered trademark of Oxford UniversityPress.

All right reserved. No part of this publication may be reproduced, stored in a retrieval system, or transmitted, in any form or by any means, electronic, mechanical, photocopying, recording, or otherwise,

without the prior permission of Oxford University Press.

Library of Congress Cataloging-in-Publication Data Leigh, R.John.

The neurology of eye movements / R.John Leigh, David S. Zee. — 3rd ed.

p. cm. — (Contemporary neurology series ; 55) Includes bibliographical references and index.

ISBN 0-19-512972-5.— ISBN 0-19-512973-3 (book/CD package). — ISBN 0-19-512974-1 (CD ROM upgrade)

1.Eye—Movement disorders—Diagnosis. 2. Eye—Movements. 3. Diagnosis, Differential. I. Zee, David S. II. Title. III. Series.

[DNLM: 1. Eye Movements—physiology. 2. Ocular Motility Disorders. WlC'769Nv.55 1999] RE731.L44 1999 617.7'62—dc21 DNLM/DLC for Library of Congress 98-37880

The science of medicine is a rapidly changing field. As new research and clinical experience broaden our knowledge, changes in treatment and drug therapy do occur. The author and the publisher of this work have checked with sources believed to be reliable in their efforts to provide information that is accurate and complete, and in accordance with the standards accepted at the time of publication. However, in light of the possibilityof human error or changes in the practice of medicine, neither the author, nor the publisher, nor any other party who has been involved in the preparation or publication of this work warrants that the information contained herein is in every respect accurate or complete. Readers are encouraged to confirm the information contained herein with other reliable sources, and are strongly advised to check the product information sheet provided by the pharmaceutical company for each drug they plan to administer.

9 8 7 6 5 4 3 2 1

Printed in the United States of America on acid-free paper.

PREFACE TO

THE THIRD EDITION

As in the first two editions of The Neurology of Eye Movements, our main goal has been to synthesize information discovered through basic research into a form that is directly applicable to the interpretation of clinical disorders of eye movements.

A number of new concepts appear in this edition, such as three-dimensional aspects of eye rotations, identification of cortical "eye fields" in humans by functional imaging, and the development of treatments for nystagmus and other abnormal movements that impair vision. New findings have required us to revise or modify our hypothetical schemes for several classes of eye movements. In making these substantial revisions, we have abided with our effort to write for a broad audience that includes neurologists, ophthalmologists, otolaryngologists, optometrists, neurosurgeons, psychiatrists, and basic researchers working in various aspects of neuroscience for whom eye movements are pertinent. We have endeavored to provide up-to-date references but, since the current output of scientific papers is large, have had to leave out some fine citations that appeared in previous editions. The growth of the scientific and clinical literature shows no signs of slowing down. Thus, the reader will inevitably turn to bibliographic resources on the World Wide Web for the latest information. Nonetheless, we hope that the schemes we present here will provide a coherent way of interpreting basic and clinical research for some years.

New to this edition, we have provided the option of accessing supplementary material on a CD-ROM, in conjunction with the conventional clothbound book. Though the book can stand alone, the armchair reader can also choose to move to the computer to read and print the text, to view color figures and more than 60 videos referred to in the text, and to take advantage of the linking of physiology and anatomy with clinical ocular motor syndromes and their differential diagnosis.

The new CD-ROM component has many advantages. First, the reader can appreciate the dynamic characteristics of abnormal eye movements being discussed in the text, and relate these features to patients that they examine at the bedside. Second, when reading about a clinical disorder, access to pertinent basic information can be readily accessed (or vice versa) via hypertext links. This is facilitated by "displays," which summarize clinical syndromes and pertinent anatomy, and serve as bridges between related basic and clinical sections and videos. Case histories of illustrative patients, MR and CT scans, eye movement records, and videos are also linked in this way. One trade-off has been the need for us to make each heading and sub-heading specific, and the reader is asked to bear with what might seem unnecessary repetition of the topic titles within sections. Each video clip is quite short, to contain file size and facilitate real-time video images. The reader might find it useful to play the clips continuously while the legend is being read.

V

VI Preface

As is previous editions, we are indebted to many inidividuals who have contributed their expertise and time to improve our book, any short-comings being our own. The following individuals read substantial portions of the manuscript: Lea Averbuch-Heller, Kanokwan Boonyapisit, Stephan Brandt, Vallabh Das, Henry Kaminski, Phillip Kramer, Lloyd Minor, Lance Optican, Vivek Patel, Grace Peng, Klaus Rottach, Mark Shelhamer, Heimo Steffen, John Stahl, Ronald Tusa, and Mark Walker. Individuals who have provided reviews, figures, videos, or other contributions include Jean Biittner-Ennever, Patrick Chinnery, Mark Cohen, Robert Daroff, Louis Dell'Osso, Joseph Demer, Susan Herdman, Manabu Honda, Anja Horn, Henry Kaminski, Gregory Kosmorsky, Richard Leigh, Hans Liiders, Vendetta Matthews, Lloyd Minor, Joel Miller, Neil Miller, Adonis Moschovakis, Gary Paige, Robert Ruff, Scott Seidman, Robert Spencer, Ki Bum Sung, David Waitzman, Shirley Wray, Stacy Yaniglos, and Arthur Zinn. We are grateful to Bernice Wissler and Nancy Wolitzer for editorial assistance, and to Kyle Bates and Kirk Pedrick for help in making the videos. We thank Lauren Enck and her staff at Oxford University Press, Al Cecchini and his colleagues at Libera, and Sid Gilman for his crucial role in facilitating the publication of this edition. We are grateful for the continued support of our work by the National Eye Institute, the National Institute of Deafness and Communicative Disorders, the National Space Biomedical Research Institute (NASA), the Department of Veterans Affairs Medical Research Service, and the Evenor Armington Fund. Finally, we thank Daniele Nuti for making it possible for us to make a start on our writing in the inspiring atmosphere of the Certosa of the University of Siena, Italy.

January 1999

R.J.L.

 

D.S.Z.

CONTENTS

PART I THE PROPERTIES AND NEURAL SUBSTRATE OF

EYE MOVEMENTS

 

1. A SURVEY OF EYE MOVEMENTS:

3

CHARACTERISTICS AND TELEOLOGY

 

Why Study Eye Movements?

3

Visual Requirements of Eye Movements

5

Functional Classes of Eye Movements

5

Orbital Mechanics: Phasic and Tonic Innervation

6

Vestibular and Optokinetic Systems

8

Saccadic System

10

Smooth Pursuit and Visual Fixation

10

Combined Movements of the Eyes and Head

11

Vergence Eye Movements

12

Three-Dimensional Aspects of Eye Movements

12

Adaptive Control of Eye Movements

13

Voluntary Control of Eye Movements

13

Eye Movements and Spatial Localization

14

The Scientific Method Applied to the Study of

15

Eye Movements

 

Summary

15

2. THE VESTIBULAR-OPTOKINETIC SYSTEM

19

Function of the Vestibular-Optokinetic System

21

Anatomy and Physiology of the Peripheral Vestibular System

24

Brain Stem Elaboration of the Vestibulo-ocular Reflex

29

Neural Substrate for Optokinetic Responses

36

Quantitative Aspects of the Vestibular-Optokinetic System

37

Adaptive Properties of the Vestibulo-ocular Reflex

48

Vestibulocerebellar Influences on the Vestibulo-ocular Reflex

53

Vestibular Sensation

56

Clinical Examination of Vestibular and Optokinetic Function

57

Laboratory Evaluation of Vestibular and Optokinetic Function

63

Pathophysiology of Disorders of the Vestibular System

67

Summary

72

3. THE SACCADIC SYSTEM

90

The Purpose of Saccades

90

Behavior of the Saccadic System

91

Vii

Viii Contents

 

Neurophysiology of Saccadic Eye Movements

102

Saccades and Movements of the Eyelids

126

Examination of Saccades

128

Pathophysiology of Saccadic Abnormalities

130

Summary

134

4. SMOOTH PURSUIT AND VISUAL FIXATION

151

The Purpose of Smooth Pursuit

151

Visual Fixation

152

Stimulus for Smooth Pursuit

156

Quantitative Aspects of Smooth Pursuit

159

Neural Substrate for Smooth Pursuit

164

Models of Smooth Pursuit

174

Clinical Examination of Fixation and Smooth Pursuit

177

Laboratory Evaluation of Fixation and Smooth Pursuit

179

Abnormalities of Visual Fixation and Smooth Pursuit

180

Summary

186

5. GAZE HOLDING AND THE NEURAL INTEGRATOR

198

Neural Coding of the Ocular Motor Signal

199

Quantitative Aspects of Neural Integration

201

Neural Substrate for Gaze Holding

203

Clinical Evaluation of Gaze Holding

208

Abnormalities of the Neural Integrator

209

Summary

211

6. SYNTHESISOF THE COMMAND FOR CONJUGATE

215

EYE MOVEMENTS

 

Brain Stem Connections for Horizontal Conjugate

215

Movements

 

Brain Stem Connections for Vertical and Torsional

221

Movements

 

Cerebellar Influences on Gaze

228

The Cerebral Hemispheres and Voluntary Control of

233

Eye Movements

 

Summary

250

7. EYE-HEAD MOVEMENTS

263

Stabilization of the Head

263

Voluntary Control of Eye-Head Movements

265

Examination of Eye-Head Movements

273

Laboratory Evaluation of Eye-Head Movements

273

Disorders of Eye-Head Movement

274

Summary

278

 

Contents

iX

8. VERGENCE EYE MOVEMENTS

286

Stimuli to Vergence Movements

 

287

Fusion or Disparity-Induced Vergence

 

287

Blur-Induced Vergence

 

290

The Near Triad

 

290

Interactions between Accommodation and Vergence

 

291

Dynamic Properties of Vergence Eye Movements

 

292

Neural Substrate of Vergence Movements

 

295

Conceptual Models of Supranuclear Control of Vergence

 

300

Adaptive Mechanisms to Maintain Ocular Alignment

 

302

Examination of Vergence Movements

 

306

Abnormalities of Vergence

 

307

Summary

 

310

PART II: THE DIAGNOSIS OF DISORDERS OF EYE MOVEMENTS

9. DIAGNOSIS OF PERIPHERAL OCULAR MOTOR

321

PALSIES AND STRABISMUS

 

Anatomy of the Orbital Fascia and the Extraocular Muscles

323

Structure and Function of Extraocular Muscle

327

Anatomy of Ocular Motor Nerves and Their Nuclei

331

Physiologic Basis for Conjugate Movements:

336

Yoke Muscle Pairs

 

Clinical Testing in Diplopia

337

Pathophysiology of Some Commonly Encountered Signs

344

in Strabismus

 

Clinical Features and Diagnosis of Concomitant Strabismus

348

Clinical Features of Ocular Nerve Palsies

350

Disorders of the Neuromuscular Junction

373

Chronic Progressive External Ophthalmoplegia and

379

Restrictive Ophthalmopathies

 

10. DIAGNOSIS OF CENTRAL DISORDERS OF

405

OCULAR MOTILITY

 

Diagnosis of Nystagmus and Saccadic Intrusions

407

Treatments for Nystagmus and Saccadic Intrusionsists

456

Skew Deviation and the Ocular Tilt Reaction (OTR)

463

Disease of the Vestibular Periphery

465

Oscillopsia

479

Ocular Motor Syndromes Caused by Lesions in

482

the Medulla

 

Ocular Motor Syndromes Caused by Disease of

487

the Cerebellum