The Neurology of Eye Movements

657 Pages·1999·51.06 MB·English

by  R. John Leigh

THE NEUROLOGY OF
EYE MOVEMENTS
THIRD EDITION
CONTEMPORARY NEUROLOGY SERIES AVAILABLE:
19 THE DIAGNOSIS OF STUPOR AND COMA, EDITION 3
Fred Plum, M.D., and Jerome B. Posner, M.D.
26 PRINCIPLES OF BEHAVIORAL NEUROLOGY
M-Marsel Mesulam, M.D., Editor
32 CLINICAL NEUROPHYSIOLOGY OF THE VESTIBULAR SYSTEM, EDITION 2
Robert W. Baloh, M.D., and Vincente Honrubia, M.D.
36 DISORDERS 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.
38 PRINCIPLES OF GERIATRIC NEUROLOGY
Robert Katzman, M.D., and John W. Rowe, M.D., Editors
42 MIGRAINE: MANIFESTATIONS, PATHOGENESIS, AND MANAGEMENT
Robert A. Davidoff, M.D.
43 NEUROLOGY OF CRITICAL ILLNESS
Eelco F. M. Wijdicks, M.D., Ph.D., F.A.C.P.
44 EVALUATION 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.
46 CLINICAL NEUROPHYSIOLOGY
Jasper R. Daube, M.D., Editor
47 NEUROLOGIC REHABILITATION
Bruce H. Dobkin, M.D.
48 PAIN MANAGEMENT: THEORY AND PRACTICE
Russell K. Portenoy, M.D., and Ronald M. Kanner, M.D., Editors
49 AMYOTROPHIC 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.
50 MULTIPLE SCLEROSIS
Donald W. Paty, M.D., F.R.C.P.C., and George C. Ebers, M.D., F.R.C.P.C.
51 NEUROLOGY AND THE LAW: PRIVATE LITIGATION AND PUBLIC POLICY
H. Richard Beresford, M.D., J.D.
52 SUBARACHNOID HEMORRHAGE: CAUSES AND CURES
Bryce Weir, M.D.
53 SLEEP MEDICINE
Michael S. Aldrich, M.D.
54 BRAIN TUMORS
Harry S. Greenberg, M.D., William F. Chandler, M.D., and Howard M. Sandier, M.D.
55 THE NEUROLOGY OF EYE MOVEMENTS, EDITION 3
R.John Leigh, M.D., and David S. Zee, M.D.
(book and CD-ROM versions available)
THE NEUROLOGY OF
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
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Copyright © 1999 by Oxford University Press Inc.
Published by Oxford University Press Inc.,
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Oxford is a registered trademark of Oxford University Press.
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,
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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
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Printed in the United States of America
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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 func-
tional imaging, and the development of treatments for nystagmus and other ab-
normal 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 ap-
peared in previous editions. The growth of the scientific and clinical literature
shows no signs of slowing down. Thus, the reader will inevitably turn to biblio-
graphic resources on the World Wide Web for the latest information. Nonethe-
less, 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 supplemen-
tary 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 differ-
ential diagnosis.
The new CD-ROM component has many advantages. First, the reader can
appreciate the dynamic characteristics of abnormal eye movements being dis-
cussed 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 ba-
sic 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 con-
tributed 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, fig-
ures, 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 editor-
ial 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 Com-
municative 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. SYNTHESIS OF 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