The Vestibular System A Sixth Sense

by Goldberg, Jay M.; Wilson, Victor J.; Cullen, Kathleen E.; Angelaki, Dora E.; Broussard, Dianne M.; Buttner-Ennever, Jean; Fukushima, Kikuro; Minor, Lloyd B.

• ISBN13: 9780195167085
• ISBN10: 0195167082
• Edition: 1st
• Format: Hardcover
• Copyright: 2012-01-23
• Publisher: Oxford University Press

Summary

The Vestibular System: A Sixth Sense is an integrative look at the vestibular system and the neurobiology of balance. Written by eight leading experts and headed by Jay M. Goldberg, this book builds upon the classic by Victor Wilson and Geoffrey Melville Jones published over 25 years ago and takes a fresh new look at the vestibular system and the revolutionary advances that have been made in the field. A core reference work for sensory neurobiologists, and also neurologists and other clinicians interested in postural control, motion sickness and nausea, and eye movements, this book is destined to become a classic in its own right.

Author Biography

Jay M. Goldberg, The Department of Neurobiology, Pharmacology and Physiology, University of Chicago, Chicago, IL.

Victor J. Wilson, Laboratory of Neurophysiology, Rockefeller University, New York, NY.

Kathleen E. Cullen, Laboratory of Neurophysiology, McGill University, Montreal, Quebec, Canada.

Dora E. Angelaki, Department of Anatomy and Neurobiology, Division of Biology and Biomedical Sciences
School of Medicine, Washington University in St. Louis, St. Louis, MO.

Dianne M. Broussard, Division of Cellular and Molecular Biology, Toronto Western Hospital, Toronto, Ontario
Canada

Jean A. Büttner-Ennever, Institute of Anatomy III, Ludwig-Maximilians University of Munich, Munich, Germany.

Kikuro Fukushima, Department of Physiology, Hokkaido University School of Medicine, Kitaku, Sapporo, Japan.

Lloyd B. Minor, Department of Otolaryngology, Head and Neck Surgery, Department of Neuroscience, The Johns Hopkins University School of Medicine, Baltimore, MD.

Table of Contents

Introduction
The Vestibular System in Everyday Life	p. 3
Overview of the Vestibular System	p. 3
Visual Acuity and the Vestibulo-Ocular Reflex	p. 4
Air-Righting Reflex in the Cat	p. 7
Post-Rotational Reactions	p. 8
Positional Alcohol Nystagmus	p. 10
Motion Sickness	p. 12
Vection Illusions	p. 13
The Subjective Visual Vertical	p. 13
Adaptive Plasticity	p. 15
Path Finding and Spatial Orientation	p. 16
Postural Control	p. 17
Summary	p. 17
Selected Readings	p. I8
Peripheral Vestibular System
Structure of the Vestibular Labyrinth	p. 23
Gross and Microscopic Anatomy	p. 23
Fine Structure of the Sensory Regions	p. 25
Hair Cells	p. 28
Supporting Cells	p. 33
Transitional Regions	p. 33
Regional Variations in Cellular Architecture and Afferent Innervation	p. 33
Crista Ampullaris	p. 35
Utricular Macula	p. 35
Saccular Macula	p. 37
Efferent Innervation	p. 38
Summary	p. 40
Selected Readings	p. 42
Hair Cell Transduction	p. 45
Mechanoelectric Transduction	p. 46
Basolateral Currents	p. 49
Neurotransmitter Release and Presynaptic Calcium Channels	p. 50
Calcium Channels	p. 51
Neurotransmitter Release	p. 51
Postsynaptic Mechanisms	p. 55
Synaptic Transmission Involving Type I Hair Cells	p. 56
Spike Encoding	p. 59
Efferent Neurotransmission	p. 60
Summary	p. 63
Selected Readings	p. 63
Physiology of the Vestibular Organs	p. 70
General Features of the Vestibular Organs	p. 70
Vestibular Organs Are Inertial Sensors	p. 70
Resting Discharge	p. 71
Discharge Regularity	p. 72
Information Transmission	p. 76
Semicircular Canals	p. 76
Directional Properties	p. 78
Macromechanics and the Torsion-Pendulum Model	p. 78
Interspecies Variations and Canal Dimensions	p. 84
Afferent Response Dynamics	p. 85
Variations in Gain and Phase	p. 90
Afferent Morphology and Physiology	p. 92
Dynamic Range of Afferent Discharge	p. 93
Otolidi Organs	p. 94
Directional Properties	p. 94
Macromechanics and the Otoconial Membrane	p. 100
Afferent Response Dynamics	p. 104
Dynamic Range of Afferent Discharge	p. 105
Variations in Gain and Phase	p. 107
Afferent Morphology and Physiology	p. 107
Summary	p. 109
Selected Readings	p. 109
The Efferent Vestibular System	p. 116
Comparative Anatomy of Central Efferent Pathways	p. 116
Responses of Afferents to Electrical Activation of the EVS	p. 118
Mammals	p. 118
Non-Mammals	p. 121
Responses of Efferents to Natural Stimulation	p. 125
Efferent-Mediated Responses of Afferents	p. 126
Possible Functions of Efferents in Mammals	p. 129
Summary	p. 130
Selected Readings	p. 131
Central Vestibular System
Neuroanatomy of Central Vestibular Pathways	p. 137
Introduction	p. 137
The Vestibular Nuclei: Subdivisions and Anatomical Organization	p. 137
Medial Vestibular Nucleus	p. 138
Lateral Vestibular Nucleus	p. 141
Superior Vestibular Nucleus	p. 142
Descending Vestibular Nucleus	p. 142
y Group	p. 142
Interstitial Nucleus of the Vestibular Nerve	p. 142
Associated Cell Groups	p. 143
Projection and Intrinsic Neurons	p. 144
Connections with the Ipsilateral Vestibular Nerve	p. 145
Commissural Pathways	p. 148
Vestibulo-Ocular and Optokinetic Systems	p. 148
Semicircular Canal Projections to Oculomotor Neurons	p. 148
Otolith Projections to Oculomotor Neurons	p. 150
Nucleus Propositus Hypoglossi	p. 152
Interstitial Nucleus of Cajal	p. 153
Reticular Formation	p. 154
Optokinetic Padiways	p. 154
Vestibulospinal Systems	p. 156
Medial Vestibulospinal Tract	p. 156
Lateral Vestibulospinal Tract	p. 157
Vestibulo-Ocular Cervical Padiways	p. 158
Odier Vestibulospinal Tracts	p. 161
Reticulospinal Tracts	p. 161
Spinal Projections to the Vestibular Nuclei	p. 162
Vestibulocerebellar Relations	p. 163
Functional Organization	p. 164
Basic Circuitry	p. 166
Vestibular Projections to the Cerebellum	p. 167
Prepositus Nucleus	p. 168
Projections from the Deep Cerebellar Nuclei to the Vestibular Nuclei	p. 169
Projections from the Cerebellar Cortex to the Vestibular Nuclei	p. 169
Cerebellar Cortical Modules	p. 170
Lateral Reticular Nucleus	p. 173
Vestibulo-Paramedian Tract Projections	p. 174
Vestibulo-Autonomic Connections	p. 174
Vestibular Connections with the Neocortex	p. 175
Pathways Involving the Hippocampal Formation	p. 177
Summary	p. 178
Selected Readings	p. 180
List of Abbreviations	p. 181
Synaptic Mechanisms in the Vestibular Nuclei	p. 191
Historical Perspective	p. 191
Basic Circuitry of the Vestibular Nuclei	p. 192
Ipsilateral Vestibular Nerve Inputs	p. 192
Commissural Connections	p. 195
Neurotransmitters in the Vestibular Nuclei	p. 198
Transmission between the Vestibular Nerve and Secondary Neurons	p. 200
Transmission within the Vestibular Nuclei	p. 201
Output Pathways of the Vestibular Nuclei	p. 201
Properties of Individual Neurons	p. 201
Resting Discharge	p. 201
In vitro Electrophysiology	p. 202
Central Projections of Regular and Irregular Afferents	p. 206
Intracellular Labeling of Vestibular-Nerve Fibers	p. 206
Electrophysiological Studies	p. 207
Functional Ablation of Irregular Afferents	p. 209
Convergence from Separate Vestibular Organs	p. 210
Canal-Canal Convergence	p. 211
Otolith-Otolith Convergence	p. 213
Spatio-Temporal Convergence	p. 214
Canal-Otolith Convergence	p. 217
Convergence from Somatosensory Receptors	p. 218
Input from Neck Afferents	p. 219
Input from Limb Afferents	p. 219
Neck-Vestibular Convergence in the Vestibular Nuclei	p. 220
Summary	p. 221
Selected Readings	p. 221
Vestibulo-Ocular and Vestibulospinal Mechanisms
An Oculomotor Tutorial	p. 231
Overview and Classification of Eye Movement Types	p. 231
Ocular Structure and Functional Implications	p. 232
The Extraocular Eye Muscles	p. 232
Mechanics of the Oculomotor Plant	p. 234
Oculomotor Motoneuron Discharge	p. 235
Plant Mechanics and Premotor Control	p. 237
Gaze Redirection	p. 240
Saccades	p. 240
Smooth Pursuit	p. 242
Vergence	p. 242
Gaze Stabilization	p. 243
Vestibulo-Ocular Reflexes	p. 243
Optokinetic System	p. 245
Interactions between Eye and Head Movements	p. 245
Summary	p. 246
Selected Readings	p. 246
Vestibulo-Ocular Reflexes	p. 249
Semicircular-Canal-Related Angular VOR	p. 249
General Properties of the Canal-Related AVOR	p. 249
AVOR during High-Frequency Rotations	p. 252
AVOR at Low Frequencies: Velocity Storage	p. 252
AVOR-Visual Interactions: The Optokinetic System	p. 255
AVOR in Three Dimensions	p. 256
Otolith-Ocular Reflexes	p. 259
Tilt VOR	p. 259
Otolith Influences on the AVOR during Off-Vertical Axis Rotations	p. 260
Otolith Influences on the AVOR during Canal-Otolith Conflict	p. 264
Translational VOR (TVOR)	p. 264
Optic Flow during Translation	p. 266
TVOR Properties	p. 268
Visual Mechanisms for Short Latency Visual Compensation during Translation	p. 271
Distinguishing Tilts from Translations	p. 271
Differences between the AVOR and the TVOR	p. 272
Comparative Adaptations	p. 273
Summary	p. 274
Selected Readings	p. 274
The Vestibulospinal System and Postural Control	p. 280
Reflexes Versus Multisensory Strategies	p. 280
Multisensory Strategies	p. 281
Vestibular Reflexes: General Considerations	p. 284
Vestibulocollic Reflexes (VCR)	p. 287
The Angular VCR	p. 287
The Linear VCR Evoked by Translation and Tilts	p. 293
The Cervicocollic Reflex	p. 294
Control Systems Analysis of the Head-Neck Plant	p. 295
Head Plant	p. 297
Vestibulocollic Reflex	p. 298
Cervicocollic Reflex	p. 302
Reflex Interactions	p. 302
Use of Control Systems Models	p. 303
Vestibulospinal and Neck Reflexes Acting on the Limbs	p. 303
Spatial and Temporal Properties of the Reflexes	p. 303
Afferent Origin of the Reflexes	p. 305
Neural Substrate of the Reflexes	p. 306
Vestibulospinal Actions on Hindlimb Motoneurons	p. 306
Vestibulospinal Actions on Forelimb Motoneurons	p. 307
Actions on Fusimotor Neurons	p. 310
Tonic Neck Reflexes	p. 311
Summary	p. 311
Selected Readings	p. 312
Signal Processing in Alert Animals
Signal Processing in Vestibular Nuclei (Vn) of Alert Animals During Natural Behaviors	p. 321
Introduction	p. 321
Classes of Neurons in Head-Restrained, Alert Monkeys	p. 322
Position-Vestibular-Pause (PVP) Neurons	p. 323
Vestibular Only (VO) and Vestibular-Pause Cells	p. 325
Eye-Head (EH) Neurons	p. 327
Burst-Tonic (BT) Neurons	p. 330
Dynamics of Neuronal Responses	p. 332
Frequency Response during Sinusoidal Rotations	p. 332
Response Linearity	p. 332
Velocity Storage	p. 332
Response to Linear Translations in Alert Head-Restrained Monkeys	p. 335
Distinguishing Translation from Tilt	p. 336
Interactions with the Oculomotor Pathways that Control Pursuit Eye Movements	p. 338
Integration of Inputs from Vestibular and Optokinetic Pathways	p. 339
VN Modulation during the OKR	p. 339
Optokinetic Pathways to the VN	p. 343
Integration of Vestibular and Proprioceptive Inputs	p. 344
Differential Processing of Active Versus Passive Head Movements	p. 346
Neuronal Responses during Active Versus Passive Head Movement	p. 347
Mechanisms for the Differential Processing of Active Versus Passive Head Movement	p. 347
Vestibular Processing Depends on Current Gaze Strategy	p. 351
Vestibular Processing during Voluntary Gaze Shifts	p. 352
Vestibular Processing during Visual Tracking; VOR Cancellation and Eye-Head Pursuit	p. 354
Vestibular Processing during Near Versus Far Viewing	p. 355
Summary	p. 355
Selected Readings	p. 357
The Cerebellum and the Vestibular System	p. 364
Overview of Signal Processing in the Cerebellum	p. 364
The Basic Cerebellar Circuit	p. 364
Vestibular Inputs Are Specific to Localized Regions of the Cerebellum	p. 365
Nodulus and Ventral Uvula	p. 365
Mossy Fiber Inputs	p. 365
Climbing Fiber Inputs	p. 367
Efferent Connections	p. 367
Neuronal Responses	p. 369
Lesions and Function	p. 372
Flocculus and Ventral Paraflocculus	p. 374
Mossy Fiber Inputs	p. 377
Climbing Fiber Inputs	p. 377
Efferent Projections of the Flocculus	p. 377
Differences between the Flocculus and Ventral Paraflocculus	p. 378
Neuronal Responses	p. 379
Complex Spikes	p. 380
Simple Spikes	p. 383
Changes in Neuronal Responses following VOR Learning	p. 386
Lesions and Function	p. 386
Lesions Studies Emphasize the Role of the Flocculus in VOR Adaptation and Motor Learning	p. 388
The Vermis of the Anterior and Posterior Lobes	p. 389
The Deep Cerebellar Nuclei	p. 391
Fastigial Nucleus	p. 392
Rostral Fastigial Nucleus	p. 392
Caudal Fastigial Nucleus	p. 393
The Interposed Nuclei	p. 397
Dentate Nuclei	p. 397
Summary	p. 397
Selected Readings	p. 398
Functional Considerations
Learning and Compensation in the Vestibular System	p. 409
Motor Learning in the Vestibulo-Ocular Reflex	p. 409
The Adaptive Capabilities of the VOR	p. 410
Signal Flow in the VOR Network	p. 411
Rules for the VOR and Motor Learning	p. 413
Possible Sites of Motor Learning: Cerebellum Versus; Brain Stem	p. 413
Evidence for Sites of Learning and Memory	p. 414
Possible Cellular Mechanisms of Synaptic Plasticity	p. 418
Consolidation of VOR Motor Memory	p. 424
Generalization: Can Learning Be Applied to New Situations?	p. 425
Compensation for Vestibular Damage	p. 427
Uninilateral Labyrinthectomy	p. 427
Activity in the Vestibular Nuclei following Labyrinthectomy	p. 429
Cellular Mechanisms of Compensation in the Vestibular Nuclei	p. 431
The Role of the Cerebellum in Compensation	p. 434
Summary	p. 435
Selected Readings	p. 435
Cortical Representations of Vestibular Information	p. 443
Introduction	p. 443
Historical Perspective	p. 443
Multiple Representations of Vestibular Signals in the Cerebral Cortex	p. 444
Visuomotor Areas in Frontal Cortex	p. 446
Extrastriate Visual Cortex	p. 449
Ventral Intraparietal Area	p. 453
Parieto-Insular Vestibular Cortex, Area 2v and Area 3a	p. 454
Ascending Vestibular Pathways through the Thalamus	p. 455
Descending Cortical Information Affecting Vestibular Responsiveness in the Vestibular Nuclei	p. 455
Vestibular Influences in the Head-Direction Circuit of the Limbic System	p. 457
Summary	p. 460
Selected Readings	p. 460
Reference Frames for the Coding of Vestibular Signals	p. 467
Definitions of Coordinate Systems and Reference Frames	p. 468
Head- Versus Body-Centered Reference Frames: Vestibular-Neck Proprioceptive Interactions	p. 468
Head- Versus Eye-Centered Reference Frames for Self-Motion Perception: Vestibular-Visual Interactions in Extrastriate Visual Cortex	p. 472
Head- Versus World-Centered Reference Frames: Canal-Otolith Convergence for Inertial Motion Detection	p. 476
Computational Solution for the Two Ambiguities of Peripheral Vestibular Sensors	p. 478
The Rotation Problem: Allocentric Coding of Angular Velocity	p. 478
The Linear Acceleration Problem: Evidence for Segregation of Tilt and Translation	p. 480
Tilt-Translation Exceptions	p. 481
Neural Representations of Inertial Motion	p. 483
Implications for Canal-Canal and Otolith-Canal Convergence	p. 485
Multisensory Influences	p. 487
Summary	p. 487
Selected Readings	p. 487
Clinical Disorders
Clinical Manifestations of Peripheral Vestibular Dysfunction	p. 495
Prevalence and Impact of Vestibular Disorders	p. 496
Diagnosis of Vestibular Disorders	p. 497
Planes of Individual Canals and Direction of Eye Movements	p. 504
Benign Paroxysmal Positional Vertigo	p. 504
Positional Alcohol Nystagmus	p. 504
Superior Semicircular Canal Dehiscence Syndrome	p. 507
Recovery of the Horizontal VOR after Unilateral Labyrinthectomy	p. 508
Multisensory Control of Posture	p. 509
Disorders of Otolith Function	p. 511
Clinical Tests of Vestibular Function	p. 512
Caloric Test	p. 512
Rotational Chair Tests	p. 514
Quantitative Evaluation of the VOR Evoked by Rapid Head Movements	p. 514
Vestibular-Evoked Myogenic Potentials	p. 516
Future Directions	p. 517
Hair-Cell Regeneration	p. 517
Vestibular Prosthesis	p. 518
Summary	p. 519
Selected Readings	p. 519
Index	p. 525
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