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Exploring the Thalamus and Its Role in Cortical Function Exploring the Thalamus and Its Role in Cortical Function Exploring the Thalamus and Its Role in Cortical Function Exploring the Thalamus and Its Role in Cortical Function Second Edition S. Murray Sherman and R. W. Guillery The MIT Press Cambridge, Massachusetts London, England © 2006 Massachusetts Institute of Technology All Rights Reserved. No part of this book may be reproduced in any form by any electronic or mechanical means (including photocopying, recording, or infor- mation storage and retrieval) without permission in writing from the publisher. MIT Press books may be purchased at special quantity discounts for business or sales promotional use. For information, please email special_sales@mitpress. mit.edu or write to Special Sales Department, The MIT Press, 55 Hayward Street, Cambridge, MA 02142-1315. This book was set in 10/13 Sabon by SNP Best-set Typesetter Ltd., Hong Kong. Printed and bound in the United States of America. Library of Congress Cataloging-in-Publication Data Sherman, S. Murray. Exploring the thalamus and its role in cortical function / S. Murray Sherman and R. W. Guillery.—2nd cd. p.; cm. Rev. cd. of: Exploring the thalamus. © 2001 Includes bibliographical references and index. ISBN 0-262-19532-1 (alk. paper) 1. Thalamus. I. Guillery, R. W. II. Sherman, S. Murray. Exploring the thalamus. HI. Title. (DNLM: 1. Thalamus—physiology. 2. Cerebral Cortex—physiology. WL 312 S553c 2006) QP383.5.S53 2006 612.8'262—dc22 2005052120 10 987654321 Brief Contents Preface to the Second Edition xiii Preface to the First Edition xvii Abbreviations xxiii 1 Introduction 1 2 The Nerve Cells of the Thalamus 27 3 The Afferent Axons to the Thalamus: Their Structure and Connections 77 4 Intrinsic Cell Properties 137 5 Synaptic Properties 179 6 Function of Burst and Tonic Response Modes in the Thalamocortical Relay 221 7 Drivers and Modulators 253 8 Two Types of Thalamic Relay: First Order and Higher Order 289 9 Maps in the Brain 317 10 The Thalamus in Relation to Action and Perception 357 11 Overview 391 References 405 Index 463 Contents Preface to the Second Edition xiii Preface to the First Edition xvii Abbreviations xxiii 1 Introduction 1 l.A. Thalamic Functions: What Is the Thalamus and What Does It Do? 1 1.A.1. The Classical View of the Thalamus 1 1.A.2. Defining Thalamic Nuclei 5 1.A.3. Major Topics Addressed in This Book 5 1.B. Thalamic Nuclei and Their Connections: The Classical View 8 1.C. The Thalamus as a Part of the Diencephalon: The Dorsal Thalamus and the Ventral Thalamus 13 1.C.1. The Dorsal Thalamus 15 1.C2. The Ventral Thalamus 20 1.D. The Overall Plan of the Next Ten Chapters 22 2 The Nerve Cells of the Thalamus 27 2.A. On Classifying Relay Cells 28 2.A.1. Early Methods of Identifying and Classifying Thalamic Relay Cells 28 2.A.2. General Problems of Cell Classification 33 2.A.3. The Possible Functional Significance of Cell Classifications in the Thalamus 38 2.A.4. Classifications of Relay Cells Based on Dendritic Arbors and Perikaryal Sizes 41 2.A.5. Laminar Segregations of Distinct Classes of Geniculocortical Relay Cells 48 viii Contents 2.A.6. The Cortical Distribution of Synaptic Terminals from Relay Cell Axons 52 2.A.7. Perikaryal Size and Calcium-Binding Proteins 61 2.B. Intcrncurons 63 2.B.1. Interneuronal Cell Bodies and Dendrites 63 2.B.2. On Distinguishing Interneuronal Axons and Dendrites 66 2.B.3. The Axons of the Intcrncurons 68 2.B.4. Classifications of Interneurons 69 2.C. The Cells of the Thalamic Reticular Nucleus 71 2.D. Summary 75 2.E. Unresolved Questions 76 3 The Afferent Axons to the Thalamus: Their Structure and Connections 77 3.A. A General View of the Afferents 77 3.B. The Drivers 81 3.B.1. Identifying the Drivers and Their Functions 81 3.B.2. Identifying the Drivers on the Basis of Their Structure 85 3.B.3. The Origin of the Drivers and Their Heterogeneity 90 3.B.4. The Relationship of Two Driver Inputs to a Single Thalamic Nucleus: Docs the Thalamus Have an Intcgrarivc Function? 91 3.C. The Modulators 92 3.C.1. Corticothalamic Axons from Layer 6 Cells 92 3.C.2. Afferents from the Thalamic Reticular Nucleus to First and Higher Order Nuclei 101 3.C.3. Connections from Interneurons to Relay Cells 105 3.C.4. Other GABA-Immunorcactivc Afferents 107 3.C.5. Cholinergic Afferents from the Brainstem 108 3.C.6. Other Afferents to Thalamic Nuclei 110 3.D. The Arrangement of Synaptic Connections in the Thalamus 111 3.D.1. The Four Terminal Types 111 3.D.2. The Glomeruli and Triads 118 3.E. Afferents to the Thalamic Reticular Nucleus 122 3.F. Afferents to Interneurons 125 3.G. Some Problems of Synaptic Connectivity Patterns 126 3.H. Quantitative and More Detailed Relationships 129 3.1. Summary 133 3.J. Unresolved Questions 134 ix Contents 4 Intrinsic Cell Properties 137 4.A. Cable Properties 137 4.A.1. Cable Properties of Relay Cells 140 4.A.2. Cable Properties of Interneurons and Reticular Cells 143 4.A.3. Implications of Cable Properties for the Function of Relay Cells and Interneurons 144 4.D. Membrane Conductances 147 4.B.1. Voltage Independent Membrane Conductances in Relay Cells 148 4.B.2. Voltage Dependent Membrane Conductances in Relay Cells 149 4.B.3. Intcrncurons 173 4.B.4. Cells of the Thalamic Rcticular Nucleus 174 4.C. Summary and Conclusions 177 4.D. Unresolved Questions 178 5 Synaptic Properties 179 5.A. Properties Common to Synapses Throughout the Brain 179 5.A.1. Ionotropic and Metabotropic Receptors 180 5.A.2. Functional Differences Between Ionotropic and Metabotropic Receptors 182 5.A.3. Short-Term Synaptic Plasticity: Paired-Pulse Effects 186 5.B. Synaptic Inputs to Relay Cells 190 5.B.1. Driving Inputs to Relay Cells 190 5.B.2. Inputs to Relay Cells from Interneurons and Cells of the Thalamic Rcticular Nucleus 196 5.B.3. Inputs from Cortical Layer 6 Axons to Relay Cells 200 5.B.4. Brainstem Modulatory Inputs to Relay Cells 202 5.B.5. Other Synaptic Properties 205 5.C. Inputs to Interneurons and Reticular Cells 208 5.C.1. Glutamatergic Inputs 208 5.C.2. Cholinergic Inputs 213 5.C.3. GABAcrgic Inputs 215 5.C.4. Noradrenergic Inputs 216 5.C.5. Scrotonergic Inputs 216 5.C.6. Histaminergic Inputs 217 5.D. Summary 217 5.E. Unresolved Questions 218 x Contents 6 Function of Burst and Tonic Response Modes in the Thalamocortical Relay 221 6.A. Rhythmic Bursting 221 6.B. Effect of Response Mode on Thalamocortical Transmission 223 6.B.1. Visual Responses of Gesticulate Relay Cells 223 6.B.2. Responses of Relay Cells of Other Thalamic Nuclei 233 6.C. Effect of Response Mode on Transmission from Relay Cells to Cortical Cells 234 6.C.1. Paired-Pulse Effects in Thalamocortical Synapses 234 6.C.2. Relationship of Response Mode to Paired-Pulse Effects 235 6.D. Control of Response Mode 239 6.D.1. Brainstem Control 242 6.D.2. Cortical Control 245 6.E. Summary 247 6.F. Unresolved Questions 250 7 Drivers and Modulators 253 7.A. Drivers and Modulators in the Lateral Geniculate Nucleus 253 7.A.1. Influence on Receptive Field Properties (Criterion 1) 258 7.A.2. Postsynapric Receptors (Criterion 2) 259 7.A.3. Postsynapric Potential Amplitude (Criteria 3-5) 260 7.A.4. Convergence onto Postsynapric Target (Criterion 6) 261 7.A.5. Axon Diameter (Criterion 7) 262 7.A.6. Transmitters (Criterion 8) 262 7.A.7. Paired-Pulse Effects and Probability of Transmitter Release (Criterion 9) 262 7.A.8. Terminal Arbor Morphology (Criterion 10) 263 7.A.9. Innervation of the Thalamic Reticular Nucleus (Criterion 11) 263 7.A.10. Extrathalamic Targets (Criterion 12) 264 7.A.11. Cross-Correlograms Resulting from Input (Criterion 13) 264 7.B. Other Plausible Examples of Drivers Beyond First Order Thalamic Relay Cells 269 7.B.1. Thalamic Reticular Cells 270 7.B.2. Layer 5 Input as a Driver to Higher Order Thalamic Relays 271 7.B.3. Lateral Geniculate Input to Cortex as a Driver 271 7.B.4. Driver/Modulator Distinction for Branching Axons 273 xi Contents 7.C. Tonic and Burst Modes in Thalamic Relay Cells 274 7.D. The Sleeping Thalamus 274 7.D.1. Slow-Wave Sleep 275 7.D.2. REM Sleep 277 7.E. Can GABAergic Inputs to Thalamus Be Drivers? 277 7.E.1. Extradicnccphalic GABAergic Inputs 277 7.E.2. Interneurons 280 7.F. Implications of Driver Concept for Cortical Processing 281 7.G. Drivers and Labeled Lines 283 7.H. Modulators and Ionotropic Receptors 284 7.I. Summary 285 7.J. Unresolved Questions 286 8 Two Types of Thalamic Relay: First Order and Higher Order 289 8.A. Basic Categorization of Relays 289 8.B. Evidence in Favor of Two Distinct Types of Thalamic Relay 294 8.B.1. Structure and Laminar Origin of the Corticothalamic Axons 296 8.B.2. Functional Evidence for Two Distinct Types of Corticothalamic Afferent 298 8.C. Some Differences between First and Higher Order Thalamic Relays 300 8.D. Defining the Functional Nature of Driver Afferent? in First and Higher Order Nuclei 302 8.D.1. Defining the Functional Role of Higher Order Relays 303 8.E. Unresolved Questions 316 9 Maps in the Brain 317 9.A. Introduction 317 9.B. The Nature of Thalamic and Cortical Maps 318 9.C. Early Arguments for Maps 320 9.D.
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