Table Of ContentTHE VESTIBULAR SYSTEM
Credit: (c) Gerard Lacz/Peter Arnold, Inc.
THE VESTIBULAR SYSTEM
A Sixth Sense
Jay M. Goldberg, PhD Victor J. Wilson, PhD Kathleen E. Cullen, PhD
Department of Neurobiology, Laboratory of Neurophysiology Department of Physiology
Pharmacology and Physiology The Rockefeller University McGill University
University of Chicago New York, New York Montreal, Quebec, Canada
Chicago, Illinois
Dora E. Angelaki, PhD Dianne M. Broussard, PhD
Department of Anatomy and Neurobiology Division of Cellular and Molecular Biology
Washington University School of Medicine Toronto Western Hospital
St. Louis, Missouri Toronto, Ontario, Canada
Jean A. Büttner-Ennever, PhD Kikuro Fukushima, PhD, MD
Institute of Anatomy I Department of Physiology
Ludwig-Maximilians University of Munich Hokkaido University School of Medicine
Munich, Germany Kitaku, Sapporo, Japan
Lloyd B. Minor, MD
Departments of Otolaryngology–Head & Neck Surgery,
Neuroscience and Biomedical Engineering
Johns Hopkins University
Baltimore, Maryland
1
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Library of Congress Cataloging-in-Publication Data
The vestibular system : a sixth sense / Jay M. Goldberg ... [et al.].
p. ; cm.
Includes bibliographical references and index.
ISBN 978-0-19-516708-5 (hardcover)
1. Vestibular apparatus. 2. Equilibrium. I. Goldberg, Jay M.
[DNLM: 1. Vestibule, Labyrinth—physiology. 2. Refl ex, Vestibulo-Ocular.
3. Vestibular Diseases—physiopathology. 4. Vestibular Nuclei—physiology. WV 255]
QP471.V4566 2011
612.8’58—dc22 2010040865
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Printed in China
on acid-free paper
To the memory of
Volker Henn, Wolfgang Precht, and David Tomlinson,
valued colleagues who died at the height of their powers
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Preface
In the late 1970s, Victor Wilson and Geoffrey today, most of us are unaware of the operation
Melvill Jones co-authored a book, M ammalian of the vestibular system until it malfunctions.
Vestibular Physiology, which became a staple in Another impediment was the location of the
laboratories devoted to vestibular research. The peripheral vestibular apparatus in the inner
book was particularly useful as an introduction ear, which led to the presumption that it was
for graduate students and postdoctoral fellows involved in hearing. It was only in the middle
considering working in the fi eld. Over the inter- of the 19th century that the vestibular organs
vening decades, so much progress was made that were recognized as providing the basis for a
it became clear that a new book was needed and separate sensory modality. Since then, empha-
that no one or two individuals could hope to sis has been on the contribution of vestibular
cover the entire fi eld adequately. For that reason, information to refl exes involved in the stabili-
a team was assembled. zation of gaze and posture. Important as are
The customary practice for a multi-authored these functions, the vestibular system has a
book is to assign one or more chapters to an indi- more general role in multisensory processing
vidual and assemble the various chapters into a involved in motor control and in the percep-
single volume. We decided on a somewhat more tion of our place in and motion through our
ambitious goal. While individuals wrote the fi rst environment.
draft of each chapter, it was reviewed by other As in most fi elds of neurobiology, functional
team members with the aim of achieving a coher- insights have been buttressed by neuroanatomi-
ent treatment of the subject matter. The aim was cal studies both peripherally and centrally, as
to create an advanced textbook that could be well as by cellular studies of synaptic transmis-
used by incoming students, by experienced sci- sion, spike encoding, and neural plasticity. One
entists interested in parts of the fi eld outside of of our goals has been to present a balanced
their areas of expertise, and by colleagues in description, ranging from cellular studies to
closely related fi elds who wanted a more detailed higher brain function. At the same time, consid-
treatment than is offered by general neurobiol- eration of molecular/developmental mechanisms
ogy textbooks. has been limited to their role in synaptic plastic-
The title of the book includes the phrase ity and hair-cell regeneration. These mecha-
A Sixth Sense. This is an obvious reference to nisms, as well as the psychophysics of vestibular
the fact that neither the vestibular system nor sensation, are topics deserving a fuller treat-
other proprioceptive senses were recognized ment. Some readers will be interested only in
with the fi ve senses (vision, hearing, touch, smell, selected topics. Each chapter, while containing
and taste) by Aristotle as important avenues of cross-references to other chapters, can be under-
information. Perhaps this is not surprising: even stood on its own.
viii PREFACE
Jacob de Groot and Jerome Carriot helped was provided by the Brain Research Foundation
in the preparation of the manuscript. Corinne of Chicago, the William Dawson Scholar Program
Kennedy and Justin Stephens did the artwork. of McGill University, and a fund of the Depart-
The patience, advice, and help of our editors, ment of Otolaryngology, Johns Hopkins Medical
Craig Panner, David D’Addona, and Kathryn School.
Winder, are appreciated. Financial under writing
Contents
Part I. Introduction 3. HAIR CELL TRANSDUCTION 45
3.1 Mechanoelectric Transduction 46
3.2 Basolateral Currents 49
1. THE VESTIBULAR SYSTEM IN
3.3 Neurotransmitter Release and
EVERYDAY LIFE 3 Presynaptic Calcium Channels 50
1.1 Overview of the Vestibular System 3
Calcium Channels 51
1.2 Visual Acuity and the Vestibulo-Ocular
Neurotransmitter Release 51
Refl ex 4 3.4 Postsynaptic Mechanisms 55
1.3 Air-Righting Refl ex in the Cat 7 3.5 Synaptic Transmission Involving Type
1.4 Post-Rotational Reactions 8 I Hair Cells 56
1.5 Positional Alcohol Nystagmus 10 3.6 Spike Encoding 59
1.6 Motion Sickness 12 3.7 Efferent Neurotransmission 60
1.7 Vection Illusions 13 3.8 Summary 63
1.8 The Subjective Visual Vertical 13 3.9 Selected Readings 63
1.9 Adaptive Plasticity 15
1.10 Path Finding and Spatial Orientation 16
1.11 Postural Control 17 4. PHYSIOLOGY OF THE
1.12 Summary 17 VESTIBULAR ORGANS 70
1.13 Selected Readings 18 4.1 General Features of the Vestibular
Organs 70
Vestibular Organs Are Inertial Sensors 70
Part II. Peripheral Vestibular Resting Discharge 71
System Discharge Regularity 72
Information Transmission 76
4.2 Semicircular Canals 76
2. STRUCTURE OF THE VESTIBULAR
Directional Properties 78
LABYRINTH 23 Macromechanics and the
2.1 Gross and Microscopic Anatomy 23 Torsion-Pendulum Model 78
2.2 Fine Structure of the Sensory Interspecies Variations and Canal
Regions 25 Dimensions 84
Hair Cells 28 Afferent Response Dynamics 85
Supporting Cells 33 Variations in Gain and Phase 90
Transitional Regions 33 Afferent Morphology and Physiology 92
2.3 Regional Variations in Cellular Dynamic Range of Afferent Discharge 93
Architecture and Afferent 4.3 Otolith Organs 94
Innervation 33 Directional Properties 94
Crista Ampullaris 35 Macromechanics and the Otoconial
Utricular Macula 35 Membrane 100
Saccular Macula 37 Afferent Response Dynamics 104
2.4 Efferent Innervation 38 Dynamic Range of Afferent Discharge 105
2.5 Summary 40 Variations in Gain and Phase 107
2.6 Selected Readings 42 Afferent Morphology and Physiology 107
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