THE SYNAPTIC ORGANIZATION OF THE BRAIN This page intentionally left blank THE SYNAPTIC ORGANIZATION OF THE BRAIN Fifth Edition Edited by Gordon M Shepherd OXFORD UNIVERSITY PRESS 2004 OXFORD UNIVERSITY PRESS Oxford New York Auckland Bangkok Buenos Aires Cape Town Chennai Dar es Salaam Delhi Hong Kong Istanbul Karachi Kolkata Kuala Lumpur Madrid Melbourne Mexico City Mumbai Nairobi Sao Paulo Shanghai Taipei Tokyo Toronto Copyright © 1974, 1979, 1990, 1998, 2004 by Oxford University Press, Inc Published by Oxford University Press, Inc 198 Madison Avenue, New York, New York, 10016 http://www.oup-usa.org Oxford is a registered trademark of Oxford University Press All rights 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 The synaptic organization of the brain / edited by Gordon M Shepherd.—5th ed p cm Includes bibliographical references and index ISBN 0-19-515955-1 (cloth)—ISBN 0-19-515956-X (pbk.) Brain Synapses Neural circuitry I Shepherd, Gordon M., 1933QP376.S9 2003 612.8'2—dc21 2003042914 246897531 Printed in the United States of America on acid-free paper PREFACE The most significant event since the publication of the previous edition has been the sequencing of the mouse and human genomes, opening up new horizons for all of biology For the brain, interpreting the functions of the genes depends on understanding how the proteins they produce function at different sites within a nerve cell, and how each nerve cell contributes to the circuits that carry out the fundamental operations of processing information in each brain region This is the subject matter of synaptic organization Taking advantage of the genomic and proteomic data are new methods, including new applications of patch clamp recordings, powerful new microscopic methods based on two-photon laser confocal microscopy, gene-targeting to enable specific genes and proteins to be labeled, knocked-in or knocked-out, and fluorescent methods that provide dramatic images of cells as they interact synaptically with their neighbors under a variety of different functional states Previously remote problems, such as the functions of dendrites and dendritic spines, are being attacked directly with the new methods In parallel with the experimental advances have come ever more powerful computational models that are building a deeper theoretical basis for brain function Just as more powerful accelerators give physicists the ability to probe more deeply into the atom and the fundamental forces that determine the nature of matter and energy, so the new methods are giving neuroscientists the ability to probe more deeply into the neuron and its synaptic circuits and the fundamental properties that determine how information is processed in the brain The results continue to constitute a quiet revolution in how we understand the neural basis of behavior, as potentially profound for brain science as the quantum theory has been for physics Each senior author is unique for his or her ability to bring together the molecular, anatomical, functional, and behavioral data in an authoritative integrated account I am profoundly grateful to them for taking on the task of revising and enlarging their accounts to cover the advances made in the past six years It is also a pleasure to welcome new co-authors and younger colleagues, not only to share the writing burdens but to show that a dedication to embracing all relevant disciplines in order to achieve an integrated understanding of brain organization has a thriving future As previously, this edition focuses on the brain regions best understood for their synaptic organization and functional correlates The chapters are organized for the most part in the same format, proceeding from neural elements and synaptic connections to a basic canonical circuit for that region This is followed by sections on synaptic physiology, neurotransmitters and neuromodulators, membrane properties, a special emphasis on dendritic properties that are crucial for action potential generation and for synaptic integration, and a final section on how the circuits mediate specific behaviors By working within the same organizational framework for each chapter, the authors are able to highlight principles that are common to all regions, as well as the adaptations unique to each It can now be seen that this same organizational structure constitutes in fact the first necessary step toward building a database of the information needed to identify those v vi Preface principles and adaptations Building databases is a new goal of the funding agencies at the National Institutes of Health, and of the multiagency Human Brain Project The study of synaptic organization may thus serve as leading model for the new field of neuroinformatics, which is dedicated to constructing databases and search tools that will enable experimentalists and theorists to construct a comprehensive multilevel, multidisciplinary database of the brain Among the unique aspects of this book is the combined reference list Most scientific writing these days involves strict limits on numbers of references cited in order to save space This means that in many cases authors are forced to cite review articles rather than the primary literature and to neglect the original literature In current vernacular, if it isn't in pubmed, forget it By contrast, this book continues to prize a scholarly depth behind our understanding There has been no limit placed on referencing the studies cited As a result, these accounts are among the most complete sources currently available for recognizing the main contributors to each field All of the references are gathered in a common list at the back of the book, its number now grown to over 3,000 I hope its utility will justify the editorial labor in composing it! Fiona Stevens at the Oxford University Press has been instrumental in stimulating the appearance of this new edition Leslie Anglin has expertly overseen the production I would like to dedicate this new edition to Wilfrid Rail, mentor, friend and collaborator for many years, who has inspired myself and the authors of this volume and countless colleagues around the globe by pioneering the theoretical foundations of the functions of dendrites and their synaptic organization Finally, as always, to Grethe: tak Hamden, Connecticut G.M.S ACKNOWLEDGMENTS Chapter Gordon M Shepherd is grateful to the National Institutes of Health for research support from the National Institute on Deafness and Other Communicative Disorders, to the Human Brain Project/Neuroinformatics Program with support from the National Institute on Deafness and Other Communication Disorders, National Institute of Mental Health, National Institute of Neurological Disorders and Stroke, National Institute on Aging, and National Science Foundation, and to a Multiple University Research Initiative (MURI) grant from the Department of Defense He thanks Wendolyn Hill and Gerry Domian for expert graphics, and Christof Koch for valuable contributions to an earlier version of this chapter Chapter David A McCormick's work has been supported by the National Institutes of Health and the Human Frontiers Science Program Chapter Robert E Burke's research support comes entirely from the Intramural Program of the National Institute of Neurological Disorders and Stroke (National Institutes of Health) He is grateful to his colleagues Michael O'Donovan, Jeffrey C Smith, and William Marks for much stimulating discussion Chapter Eric D Young is grateful to Phyllis Taylor for help in preparing the figures The work has been supported by the National Institute on Deafness and Other Communication Disorders (National Institutes of Health) Chapter Gordon M Shepherd, Charles A Greer, and Wei R Chen are grateful to the National Institutes of Health for research support from the National Institute on Deafness and Other Communicative Disorders Dr Shepherd is also grateful to the Human Brain Project/Neuroinformatics Program with support from the National Institute on Deafness and Other Communication Disorders, National Institute of Mental Health, National Institute of Neurological Disorders and Stroke, National Institute on Aging, and National Science Foundation, and to a Multiiple University Research Initiative (MURI) grant from the Department of Defense Dr Charles A Greer is also grateful for support from the Human Frontiers Program Dr Wei R Chen in addition thanks the Whitehall Foundation for research support Chapter We thank the following members of the Sterling laboratory, past and present, for their contributions to data and ideas summarized here: Barbara McGuire, Michael Freed, Ethan Cohen, Yoshihiko Tsukamoto, Rukmini Rao-Mirotznik, David Calkins, and Andrew Hsu We also thank the following collaborators: Robert Smith, Noga Vardi, Michael Freed, Gary Matthews, Henrique von Gersdorff, and Stanley J Schein The research was supported by grants from the National Eye Institute We are grateful to Gordon Shepherd for editorial suggestions and to Sharron Fina for preparing the manuscript and illustrations Chapter Eric Lange is grateful to the National Institute for Neurological Diseases and Stroke (NIH) and the National Science Foundation for research support Chapter We acknowledge support for our research from U.S Public Health Service grants from the National Institute for Eye Research Chapter This work was supported by the National Institute of Neurological Disorders and Stroke vii viii Acknowledgments Chapter 10 We thank Joshua Chover for contributing to the development of ideas This work was supported by a National Institutes of Health grant from the National Institute on Deafness and Other Communicative Disorders and a Howard Hughes predoctoral fellowship Chapter 11 Daniel Johnston and David G Amaral have been supported by grants from the National Institute of Neurological Disorders and Stroke and the National Institute of Mental Health during the preparation of this chapter Dr Johnston is also grateful to Diane Jensen for editorial assistance Chapter 12 The preparation of this chapter was supported by the Human Frontiers Science Program, the Koerber Foundation, and the European Union We thank John Anderson for neuron and dendritic reconstructions, and the Physiology Department of the University of Cape Town for educating the authors CONTENTS Online Resources, xi Contributors, xiii Introduction to Synaptic Circuits, Gordon M Shepherd Membrane Properties and Neurotransmitter Actions, 39 David A McCormick Spinal Cord: Ventral Horn, 79 Robert E Burke Cochlear Nucleus, 125 Eric D Young and Donata Oertel Olfactory Bulb, 165 Gordon M Shepherd, Wei R Chen, and Charles A Greer Retina, 217 Peter Sterling and Jonathan B Demb Cerebellum, 271 Rodolfo R Llinás, Kerry D Walton, and Eric } Lang Thalamus, 311 S Murray Sherman and R W Guillery Basal Ganglia, 361 Charles J Wilson 10 Olfactory Cortex, 415 Kevin R Neville and Lewis B Haberly 11 Hippocampus, 455 Daniel Johnston and David G Amaral 12 Neocortex, 499 Rodney Douglas, Henry Markram, and Kevan Martin References, 559 Index, 705 IX INDEX Accessory olfactory bulb (AOB), 184-185,215,216 Accommodation, 110 Acetylcholine (ACh), 21, 62, 64, 69, 202, 299, 343, 402 See also Cholinergic neurons in hippocampus, 480-481 in neocortex, 515, 528, 541-542 in olfactory cortex, 442-443 Action potential initiation, 45-47 sites within neuron for, 24, 203-204, 299-301, 489-493, 544 Action potential threshold, 46 Action potentials (APs), 45-47, 487, 489, 532 back-propagating, 25, 491-495 carried by auditory-nerve fibers, 128 spine, 23, 546-547 Activation and inactivation gates, 336-338 Active zone, Actor units, 412 Adenosine monophosphate See AMP Afferent depolarization, primary, 97, 98 Afferent drivers, 357-359 Afferent fibers, 166, 167, 364, 365, 372-373, 425, 432 Afferent input, 419, 433-435 Afferent system horizontal organization, 425 synaptic hierarchy in primary, 90, 91 Afferents, 168 See also Group la afferents brainstem, 323-324 cortical, 321-323, 366-367 corticothalamic driver, 355-356 driving, 321 flexor reflex, 81 monoaminergic, 298—299 in neocortex, 512-516 nigrostriatal, 367 primary, 81 thalamic, 314-315, 366-367, 512-514 Afterdepolarization (ADP), 527, 542 Afterhyperpolarization (AHP), 338, 476, 527-532 Afterhyperpolarizing current (IAHP) 23, 49, 51, 56,58,71,75-76, 111,338 Agranular cortex, 499 AII cells, 223-225, 249, 267-269 Allelic exclusion, 168 Alpha-motoneurons, 82-83, 88, 112 Alzheimer's disease, 497 Amacrine cells, 20-21, 33, 35, 217, 228-229, 231, 237, 252-253 starburst, 21, 249 AMP (adenosine monophosphate), 57 AMPA receptors, 139-141, 190-193, 197, 199-200, 296 GluR, 94, 139, 208 kainate and, 65, 66, 479, 535 NMDA and, 190, 208, 341, 441, 479, 480, 535 Amplification, 10 Anterior division of the VCN (AVCN), 127-129, 137 Anterior olfactory cortex (AOC), 416 Anterior olfactory nucleus (AON), 169 Anterior piriform cortex (APC), 418, 419, 425, 426, 433, 439-440, 449 Anterior thalamic nuclei, 312 Ascending branch (a.b.), 127 Aspiny neurons, 170 Associational connections, 420, 469 ATP (adenosine triphosphate), 48 Auditory-nerve fibers (ANFs), 125-126, 128, 132, 134, 140, 144, 149 action potentials carried by, 128 ANF type, 125-126, 136 in AVCN, 137 best frequency threshold, 162 bushy cells and, 130, 143, 148 cell types, convergence, and, 143 chopper neurons and, 153, 157, 158, 160 collaterals of, 129 defined, 126 glutamate and glutamine in terminals of, 139 innervation of cochlear nucleus cell by, 129 low spontaneous rate, 159 multipolar cells and, 130, 137, 151 octopus cells and, 130, 137, 139, 149 phase-locking in, 156, 157 primarylike neurons and, 155 primary like responses and, 146, 148 spontaneous firing rates, 158 Augmentation, 484 Autoinhibition, 72 Axo-axonic cells, 460, 465 See also Chandelier cells Axon, initial segment of, 90 Back propagation of action potentials, 25, 491-495 in network, 552 Baclofen, 538 705 706 Barbiturates, 538 Barlow, H B., 548-549 Basal forebrain, 324 Basal ganglia, 361-363 anatomy, 361-363 basic circuit, 377-379 direct and indirect pathways, 363, 368, 381-382 mosaic organization of neostriatum, 379-381 dendritic membrane properties, 382-387 cholinergic interneurons, 387-390 GABA/parvalbumin fast spiking interneurons, 390 GABA/SOM/NO interneurons, 391 functional operations complex integrative tasks, 406-413 natural firing patterns, 403-406 neuronal elements, 364, 365 cell populations, 372-374 efferent axons, 371 inputs, 366-367 interneurons, 368, 370-371 principal neuron, 368, 369 synaptic actions of cortical and thalamic inputs, 391-394 input fibers, 391 intrinsic connections, 400-403 of substantia nigra inputs, 397-400 synaptic plasticity, 394-397 synaptic connections, 374 axon collateral, 376 cortical and thalamic, 375 interneuron, 376 output, 376-377 substantia nigra, 375 Basket cells, 277-280, 298, 428, 460, 508, 509, 520-521 Benzodiazepines, 538 Best frequency (BF), 125, 127, 145, 157-159, 162 Beta oscillation, 437 Beta-motoneurons, 83 Bicuculline, 189-190, 298, 538, 539 Binary signal, 221 Bipolar neurons, 217, 222, 429 ON vs OFF, 223-225, 240-241, 247, 251, 254, 257, 262, 263 Bistable membrane responses, 111 Bistratified cells, 460, 462 Bitufted cells, 429 Blobs, 523 Boutons, synaptic, 86-88, 90, 96 single, 113 Brain nitric oxide synthase (BNOS), 327 Index Brain-derived neurotrophic factor (BDNF), 535 Brainstem afferents, 323-324 Brainstem inputs, 343-344, 350 Branch point failure, 95 Bruce effect, 215 Brush cells, unipolar, 134 Buildup responses to sound, 151 Burst and tonic relay response modes anatomical relationship of modulator inputs to T channels, 348 control of response mode, 347-348 detectability, 347 linearity, 345-347 signal transmission during burst and tonic firing, 344-345 Burst mode of firing, 338, 339 Bursting, as "wake-up call," 347 Bushy cells, 128, 130, 138, 147, 154 auditory-nerve fibers and, 130, 143 EPSP in, 149 globular, 129, 131, 136, 137, 143, 144, 148, 155 phase-locking in, 155-157 primarylike responses from, 146-149 spherical, 129-131, 136, 137, 140, 143, 144, 146 CA3 neurons, 464, 467, 482, 483 See also under Hippocampus, synaptic connections Cable equation, 543 Cable model of dendrites, 90-93, 202-208, 384-386, 488-489, 542-543 Calbindin, 326 Calcium binding proteins, 326 Calcium (Ca2+), 483, 491 intracellular concentration of, 302 Calcium (Ca2+) conductances, 336-339, 528-530 in hippocampus, 489-495 low threshold, 336 in mitral cells, 189, 205 in neocortex, 528-530 in olfactory cortex, 444-445 in photoreceptors, 248 in Purkinje cells, 288 in thalamic cells, 336 Calcium (Ca2+) currents, 49, 53 See also Calcium (Ca2+) conductances decrease in, 72 high-threshold, 53-54 low-threshold, 54-55 Calcium (Ca2+)-activated K + currents, 56 Canonical circuits, regional, 34-38, 556-558 Canonical cortex circuit, 37-38, 556-558 Index Canonical neuron, concept of, 25-27 Cardinal neurons, 549 Cartwheel (Ca) cells, 131-133, 138, 145, 151-152 Cation conductance, hyperpolarization-activated, 340 Central pattern generator (CPG), 118-122 Centrifugal fibers, 201-202, 231 Centrifugal inputs, 169-170 Cerebellar cortex basic circuit organization, 284, 285 cerebellar cortex-deep nuclei circuit, 286-287 climbing fiber circuit, 286 mossy fiber circuit, 284-285 dendritic properties functional circuits, 304-309 microelectrode recordings, 299-301 optical recording, 302-304 granular layer See Granule cell layer intrinsic membrane properties, 287 cerebellar nuclear cells, 288-290 Purkinje cells, 287-288 molecular layer, 281-283, 294 neuronal elements, 273-274 cerebellar nuclei, 271, 278-279 geometric organization of, 273 input elements, 274-275 intrinsic elements, 277-278 output elements, 276-277 neurotransmitters, 297-299 synaptic actions, 290-292, 294-295 inhibitory synapses, 292-295 modulation of excitatory synapses, 295-296 synaptic connections, 279-284 cerebellar nuclei, 283-284 Cerebellar nuclear neurons intrinsic properties, 289-290 Purkinje cell action on, 294-295 response to white matter stimulation, 307 Cerebellar nuclei, 271 Cerebellum, 28, 271-272 Chandelier cells, 70, 429, 465, 511, 521 See also Axo-axonic cells Chattering cells, 530 Chestnut cells, 134 Choline acetyltransferase (ChAT), 299 Cholinergic fibers, 202 Cholinergic interneurons, 370, 376, 387-390, 401,402,404,411 Cholinergic neurons See also Acetylcholine pacemaking by, 387-389 Cholinergic responses, nicotinic, 64-65 Chopper neurons, 153, 154, 156 stimulus spectrum representation in, 157-160 707 Chopping, 146 Claustrum, 516 Climbing fiber circuit, 286 Climbing fibers (CF), 274, 275, 290-291, 304 Climbing fibers-Purkinje cell connection, 281 Cr -mediated IPSP, 430, 437 Cochlear nucleus, 125-126 basic circuit, 143-145 circuit functions, 155-163 membrane properties and integration of inputs, 146-152 models of somatic and dendritic properties, 153-155 neuronal elements and synaptic connections, 126-130 numbers of cell types and convergence, 143 synaptic connections, 134-136 Commissural connections, 420 Complex spikes, 290 Cone bipolar circuit, 264 Connectionist models of cortical function, 549 Connectivity, patterns of, Connexins, 519 Contextual modulation, 183 Contrast gain control, 351 Cortical canonical circuit, 37-38, 536-558 Corticogeniculate inputs, 342 Corticothalamic driver afferents, 355-356 Cruciform axodendritic, 366 Current source-density (CSD) analysis, 431, 436, 445, 447 Cyclic nucleotide-gated (CNG) channel, 201 Cytoarchitectonics, defined, 499 Deep pyramidal cells (DP), 417, 421 Delay non-match to sample (DNMS), 496 Delayed rectifier, 338 Dendrites, See also specific topics "filtering" by, 489 primary, 170, 203 secondary, 170, 203, 205 and synaptic action in spinal cord, 90-94 Dendritic branch units, 15, 19, 21 Dendritic branches, secondary, 202 Dendritic cells, granule cell, 178 Dendritic computation, 15-17 Dendritic integration and dendritic subunits, 15-19 Dendritic location, and somatic EPSPs, 90, 92 Dendritic processes, visualization of by current source-density (CSD) analysis, 431-432 Dendritic shaft, primary, 202 Dendritic spine units, 17-19 Index 708 Dendritic spines, 206-207, 421 See also under Neocortex fine structure, 17, 18 functions that have been ascribed to, 20 inhibition, 547 nonsaturating, 547 saturating, 546 Dendritic subunits, Dendritic tips, bipolar, 240 Dendritic trees, 7, 15 Dendrodendritic reciprocal excitatory-inhibitory synapses, 215 Dendrodendritic synaptic actions in olfactory bulb, 186-187 field potentials, 188-189 oscillatory activity, 187-188 presynaptic mechanisms, 192 recurrent excitation, 190, 192 tests of dendrodendritic interactions, 189-191 Dentate granule cells (DGC), 28, 464-466 Dentate gyrus (DG), 458, 463 interneurons in, 460, 461 synaptic connections extrinsic inputs, 466-467 outputs, 467-468 Dentate-CA3, 28 Depolarization, 45-46, 50, 69, 111, 112, 151 See also Ionic currents, types of gradient of, 203 primary afferent, 97-98 Depotentiation, 487 Derecruitment, 109-110 Descending branch (d.b.), 127 Direction(al) selectivity, 31-33 Distributed synapse, 290 D-multipolar cells, 129-131, 136, 143-145, 151, 159, 162 Dopamine, 515 Dopaminergic neurons, 253, 397-400, 411-413 reward-prediction-related responses of, 408-412 Dopaminergic synapses, 375, 399 Dorsal acoustic striae (DAS), 128, 133, 144 Dorsal cochlear nucleus (DCN), 127-129, 144, 145, 152 cell types, 131-134 feature detection, 160-163 response maps of type II and IV neurons in, 160-162 synapses, 140-143 Dorsal cortex, 28 Dorsal raph£ nucleus, 324, 363 Dorsal spinocerebellar tract neurons (DSCT), 107, 108 Dorsal thalamus See Thalamus Dorsal turtle cortex, 36, 37 Double bouquet neurons, 510, 521-522 Dreaming, 55 Duty-cycle units, 116 Dyad, 242 Electrical coupling, Electrotonic interactions, 113-114 Embryonic development of neocortex, 501-503 Endbulbs (EB), 136, 137 Endopiriform nucleus, 417 Entorhinal cortex, 466 Entorhinal-hippocampal system, compared with olfactory system, 454 Ephaptic interactions, 60-61, 87 Epileptiform activity, 483, 494 EPSP-IPSP sequence See Excitatory-inhibition (EPSP-IPSP) sequence Eulaminate cortex, 501 Exchange of small molecules, Excitatory amino acid (EAA) responses, 65-67, 94 Excitatory postsynaptic potentials (EPSPs), 3-4, 11, 12,22,25,75-76 in basal ganglia, 391-394, 396, 397 in bushy cells, 149 in cerebellum, 290-295, 297, 307 in cochlear nucleus, 137, 139, 149, 153 composite, 90, 91 in glomerular synaptic actions, 192-193, 208 group la, 96-97, 113 in hippocampus, 475-477, 480, 482, 484, 489, 493-495 in mitral cells, 192-193 in neocortex, 536, 543 in octopus cells, 149 in olfactory cortex, 430, 433, 435-437, 445-447 integration of, 447 passive return current and electrotonic spread of, 445-447 polysynaptic, 114 single-bouton, 90, 91, 113 single-fiber, 90, 91 somatic, 97 effect of dendritic location on, 90, 92 local vs., 94 in spinal cord, 90-92, 94-98, 106, 107, 113, 114, 119-120,206 in thalamus, 341, 344, 353 Excitatory synaptic currents (EPSCs), 142 Excitatory-inhibition (EPSP-IPSP) sequence, 213, 307, 308, 475-477 Excitatory-inhibitory interactions, types of, 11 Index Extensor digitorum longus (EDL), 118, 120-122 External plexiform layer (EPL), 170, 173, 177-179, 205-206 development and plasticity, 179 Exteroceptors, 81 Eye movements, "pursuit" foveal architecture implies, 237-238 Fan-in, 11 Fan-out, Fast spiking cells, 530-531 Fast spiking interneurons, 390 Fastigial nucleus, 278 Feedback (FB) excitation, 29-30 Feedback (FB) inhibition, 14, 427 Feedback neural networks, 553, 555 Feedback pathways, 516 Feedforward (FF) excitation, 28-29 Feedforward (FF) inhibition, 12-14, 427 Feedforward networks, 451, 453, 552, 553, 555 Feedforward pathways, 516, 522 Fiber systems, association horizontal organization, 425-426 Fiber volley, 475 Flexion reflex, 100 Flexor, 106 Flexor digitorum longus (FDL), 117, 118, 120-122 Flexor hallucis longus (FHL), 117, 120 Flexor reflex afferents (FRAs), 81 Foveola, 233, 237-238 Fusiform cells See Pyramidal (Py) cells GABA (gamma-aminobutyric acid), 21 in amacrine cells, 252-253 in basal ganglia, 371, 400 in cerebellum, 297-298 in cochlear nucleus, 134, 143 in granule cells, 200 in hippocampus, 472, 481 inhibitory actions, 245 K + conductance and, 69 molecular mechanisms of ionotropic amino acids and, 61 in neocortex, 515, 537-541 in olfactory bulb, 200, 208, 215 in olfactory cortex, 442 in outer plexiform layer of retina, 241 primary afferent depolarization and, 97-98 in retina, 241, 245, 251-253 in spinal cord, 97-98, 103 in thalamus, 331, 343 709 GABAA and GABAB receptors, 97-98, 197, 199-200, 341, 342, 430-431, 481, 538-539 GABAergic activity, 304-306 inhibitory responses, 74 GABAergic cells, 199, 278-279, 330, 401, 428, 429, 465, 472, 503, 524, 556-557 GABAergic inhibition, axo-axonic, 429, 521 GABAergic input, 324, 330, 331 GABA-mediated IPSPs, 67, 68, 440 GABA/parvalbumin-containing interneurons, 370-371,396,400,401,411 GABA/SOM/NO interneurons, 391, 401, 402, 411 Gamma oscillation, 435-437 Gamma-motoneurons, 82-83 static vs dynamic, 83 Ganglion cell receptive field, 254-257 Ganglion cells, retinal, 217, 225-227, 236, 243-245, 252 alpha and beta, 226 forms and function, 225-226 Gap junctions, 59, 241-242, 286, 518-519 Gating by different mechanisms, in thalamus, 344 Gating actions of neurotransmitters, 72, 73 Gemmules, 173 Genes, level of, Giant (Gi) cells, 128, 129, 132, 133, 144 gK See Potassium (K + ) conductance Glia, 180-181, 238 See also Miiller cells Glial cells, 231 Global integration, 27 Global modulation, 27 Globular bushy cells (GBCs), 129, 131, 136, 137, 143, 144, 148, 155 Globus pallidus (GP), 363, 371, 372, 376 external segment (GPe), 363, 372, 376-377, 381 internal segment (GPi), 363, 372, 377 Glomerular complex, modified, 184 Glomerular dendritic tuft, 202 Glomerular layer (GL) cells, 172, 194-196 dopaminergic cells, 196, 198 excitatory properties, 194, 195 GABAergic, 199 synaptic relations between, 198 Glomerular layer (GL) of olfactory bulb development and plasticity, 176-177 interglomerular connections, 176 interglomerular microcircuits, 182 intraglomerular connections, 175-176 intraglomerular microcircuits, 182 Glomerular modules form odor image, 210-211 710 Glomerular synapses, 142 Glomerular synaptic actions, EPSPs in, 192-193, 208 Glomerular tuft, 202-203 synchronization by, 208-209 Glomeruli, 168, 169, 214, 279 defined, 183 necklace, 184 olfactory, 168-169, 183 synaptic triadic arrangements, 319 Glutamate (GLU), 61, 66, 190, 192-193, 208-209, 215 in cerebellum, 297 in cochlear nucleus, 139-141 in hippocampus, 478, 479 mGluR6 receptor, 251 in neocortex, 541 in olfactory bulb, 190-194, 196-199 in olfactory cortex, 441-442 in thalamus, 341-342 in ventral horn, 94-95 Glutamate receptors (GluRs), 94, 95, 139-141, 208, 251, 535-536 metabotropic, 251, 342 Glutamic acid decarboxylase (GAD), 252, 298, 402 Glycine, as neurotransmitter, 67, 69 in cochlear nucleus, 143 in olfactory bulb, 200 in ventral horn, 100 Goldman-Hodgkin-Katz (GHK), 44 Golgi cell dendrite (Gcd), 281, 283 Golgi cells (GCs), 134, 277, 281-284 G-proteins, 481 Graded actions, 11 Graded signal, 221 Grandmother cell scheme, 549 Granule (Gr) cells (GCs), 28 in cerebellum, 277 in cochlear nucleus, 131-134, 142, 144, 145, 163 deep (Gn), 173 dendrodendritic microcircuit between mitral and, 189 in hippocampus, 467 intermediate (GO, 173 in olfactory bulb, 177, 186-188, 200, 205-207 superficial (Gm), 173 synchronization by, 208 Granule cell dendritic spines (Grs), 178 Granule cell layer in cerebellar cortex, 274, 279, 280, 293-294 in olfactory bulb, 170, 173-174 Group la afferents, 88, 90-94 anatomy, 88-90 Index disynaptic la reciprocal system, 99-100 modulation of transmitter release at la synapses, 96 neurotransmitter receptors, 94-95 physiology, 90 quantization of synaptic action, 95 Group la excitatory transmission See also Excitatory postsynaptic potentials mechanisms of, 94 Group la inhibition, synaptic organization of, 106, 107 Group la reciprocal inhibition, disynaptic, 105-106 Hebb's postulate for learning, 493-494 High-threshold currents, 50 High-voltage activated currents (HVA), 53-54 Hilar pathways, 482 Hippocampal cortex, 28 Hippocampal formation, 415, 455, 456 basic circuits, 462-463 cytoarchitectonic divisions, 457-458 Hippocampus, 60, 455-457 dendritic properties, 488 active, 489-493 dendritic integration of synaptic and action potentials, 493-495 passive, 489 diseases, 497-498 learning and memory, 494, 496-497 neuronal elements interneurons, 460-462 principal neurons, 458-460 three-dimensional position and layers of rat, 457-458 neurotransmitter receptors excitatory neurotransmitters, 478-481 inhibitory neurotransmitters, 481-482 specific pathways, 482-484 physiological and pharmacological properties basic response, 474 extracellular responses, 475-476 inhibitory synapses, 478 intracellular responses, 476-477 physiology and biophysics of synaptic actions, 477-478 synaptic connections of CA1, 473-474 of CA2, 472-473 of CA3, 469-472 of dentate gyrus, 464-468 of subiculum, 474 synaptic plasticity, 484 depression, 485, 487-488 111 Index facilitation, 484 long-term plasticities, 485 long-term potentiation, 485-487 post-tetanic potentiation, 484-485 short-term plasticities, 484 Homocysteate, 297 Homotypical cortex, 501 Hopfield network, 451, 553-554 Horizontal cell spines, 240 Horizontal cells, 217, 227-228, 241, 429 Horizontal limb of the diagonal ban (HDB), 169 Horizontal plane, sound localization in, 155-157 Hubel-Wiesel models of visual cortex circuits, 522 Hyperpolarization, 43, 70, 151 See also Ionic currents, types of currents activated by, 57 Hyperpolarization-activated conductance, 340 Hyperpolarizing inhibition, 11 /A (neurotransmitter), decrease in, 72 /AHP (neurotransmitter), decrease in, 70-71 /H (hyperpolarization-activated), 149, 388 7M (neurotransmitter), decrease in, 71-72 Inactivation (kinetics), 45-46, 50 removal of, 50 Induction phase, 485 Inferior colliculus (1C), 128, 129, 133 Information processing, specific, 17-19 Inhibitory operations, 12-14, 30-34 See also specific operations Inhibitory postsynaptic potentials (IPSPs), 69 See also Excitatory-inhibition (EPSPIPSP) sequence in basal ganglia, 400-401 in cerebellum, 290, 292, 307, 308 defined, disynaptic, 99 in neocortex, 537 in olfactory bulb, 213 in olfactory cortex, 430 reciprocal la, 99 recurrent, 102-103 slow vs fast, 69, 342 in spinal cord, 99 in thalamus, 342 Initial segment-soma dendritic (IS-SD) break, 287 Inner hair cells (IHCs), 125-126, 128 Input convergence, 103 Input fibers, Input processing, 35 Intermediate acoustic striae (IAS), 128, 144 Internal plexiform layer (IPL), 170-171 Interneurons, 422 See also Local/intrinsic neurons in basal ganglia, 368, 370-371, 376, 387-391, 401-403 excitatory, 460 in olfactory bulb, 166, 167 recurrent inhibition through Renshaw, 102-104 segmental/local, 84 spontaneous firing patterns of hippocampal, 478 Interplexiform cells, 229 Intralaminar nuclei, 314 Intrinsic associational connections, 426 Intrinsic operations, 35 Invagination, 240 Ionic channels, 47 Ionic currents, types of, 48-58 Ionic pumps, 47-48 lonotropic amino acid synapses, molecular mechanisms of, 61-62 lonotropic receptors, 62, 340-342, 481 Ions distribution across neuronal membranes, 39, 40 equilibrium potentials, 39-42 permeability, 43, 45 IPIC, 111, 114 Ipsilateral associational-commissural projection, 465 Irregularity, 146 Islets, 173 Isofrequency sheets, 132-133 Juxtaglomerular (JG) cells, 172 Kainate receptors, 65, 66, 479, 535 Kinesin, 240 Koniocortex, 499 Large multipolar (ML) cells, 417 See also Multipolar (M) cells Last-order interneurons, 120 Lateral geniculate nucleus (LGN), 312, 326, 327, 351 interneurons, 325, 333, 335 main connections, 320 relay cells, 325, 333 See also Thalamic relay neurons burst and tonic firing for, 338, 339, 346 synaptic inputs onto X and Y cells, 328 Lateral habenular nucleus, 363 Lateral inhibition, 13, 14, 429 mediates odor contrast enhancement, 214-215 712 Lateral nucleus of trapezoid body (LnTB), 128, 129 Lateral olfactory tract (LOT), 170, 171, 416, 418, 419, 433, 436, 439, 447 Lateral superior olivary (LSO), 128, 129, 155 Laterodorsal nucleus, 312 Light intensity range, 220-221 Limulus eye, 33 Lobe output cells, 213 Local activity-dependent changes, 26 Local circuit interactions, 31-33 Local decision point, 26 Local/intrinsic circuits, 7, 27 excitatory operations, 27-30 inhibitory operations, 30-34 Local/intrinsic neurons, See also Interneurons Locomotion fictive, 105, 116-118 spatial facilitation of cutaneous reflexes during, 118-122 motor neuron activity patterns in, 116-118 Locomotor drive potentials (LDPs), 119-121 Locomotor inhibition, 118 Locus coeruleus (LC), 169, 323 Longitudinal axodendritic pattern, 371 Long-lasting (L) current, 50 Long-term depression (LTD) in basal ganglia, 394-396, 411 in cerebellum, 295, 296 in cochlear nucleus, 141, 142 in hippocampus, 485—488 in neocortex, 533-535 in olfactory cortex, 440 synaptic plasticity and, 394-396, 411 Long-term potentiation (LTP), 67, 410-411 associative, 439-440 associative learning and, 19 in basal ganglia, 394-396, 411 in cochlear nucleus, 141, 142 in hippocampus, 485-487, 494 in neocortex, 533-535, 546 NMDA-dependent homosynaptic, 437-439 regulation of, 440-441 synaptic plasticity and, 394-396, 486 Lorente de No, 522 Low-threshold currents, 50, 148 Low-threshold spikes (LTSs), 290, 336, 396, 530 Magnesium ions (Mg2+), 65, 66 Magnification factor of projection, 512 Martinotti cell, 510-511 Matrix, 379, 380 Medial gastrocnemius (MG) motor units, 84 Medial geniculate nucleus, 312 Index Medial lemniscus, 321 Medial nucleus of trapezoid body (MnTB), 128, 129 Medial plantar (MPL) nerve, 118-122 Medial superior olivary (MSO), 128,129,155-157 Mediodorsal nucleus, 312 Membrane conductance, increasing, 41, 43 Membrane depolarization See Depolarization Membrane potential, resting, 43-45, 50 Membrane properties See also Resistance intrinsic, 31, 58 Membranes and ionic currents, 39-43 Memory storage in accessory olfactory bulb, 216 Metabotropic glutamate receptors, 342 Metabotropic receptors, 62, 251, 340-342, 344, 481 Microcircuits, synaptic, 7-14 cortical, 557 simplest types of, Middle temporal visual area (MT), 501 Midget bipolar terminal (MB), 243 Midget ganglion cell (MG), 243 Midget (M) cells, 226, 234, 254 Mitral cell dendritic tree, 202-205 Mitral cell membrane properties, synchronization by, 209 Mitral cells, 21, 24, 25, 189 in olfactory bulb, 170-171, 184, 185-187, 192-194, 199, 213, 214 synaptic activation by olfactory nerve volleys, 192, 193 Modified glomerular complex (MGC), 184 Modulation, 70 Modulatory gating, 27 Molecular layer, 274 Molecular receptive range (MRR), concept of, 211-212,215 Monoaminergic afferents, 298-299 Monoaminergic inhibition, 294 Monoamines, 514 in olfactory cortex, 443 Mossy fiber activation of Purkinje cells, 292, 293 Mossy fiber axonal plexus, 464 Mossy fiber circuit, 284-285 Mossy fiber rosettes, 274 Mossy fiber-parallel fiber pathway, 274-275, 304, 309 Mossy fibers (MF) in cerebellum, 275, 299 in hippocampus, 458-459, 467-468, 482-483 Motoneurons (MNs), 81-84 Motor coordination, 272 Movement control, 359 Muller cells, 231 spatial density, 238 Index Multipolar (M) cells, 129-131, 154, 417, 428, 429 See also T-multipolar cells auditory-nerve fibers and, 130, 151 Muscarine-sensitive K + currents, 57 Muscarinic receptors, 480-481 Muscle unit, 83 Myeloarchitectonics, 499 Myotatic unit, 89 NADPH-diaphorase, 371 Neocortex, 28, 36, 37, 499-501 amino acid neurotransmitters, 540-542 basic circuit, 522-523 cortical output, 523-525 corticocortical connections, 516 dendrites, 542-544 active properties, 544-545 dendritic spines, 545 biochemical compartments, 547-548 electrical models, 545-547 embryonic development, 501-503 functional operations neural networks compared with cortical circuits, 552-554 new designs for visual circuits, 550-551 parallel processing in neural networks, 551-552 single neurons vs neural networks, 549-550 static and dynamic connectivity, 555-558 neuronal elements, 503-512 afferents, 512-516 considerations of cortical wiring, 516-517 smooth neurons, 507-512, 520-522 spiny neurons, 503-507, 519-520 synaptic actions, 525 electrical properties of IPSP, 539-540 excitatory synapses, 535-536 inhibitory synapses, 537-539 neuronal excitability, 525-532 synaptic dynamics, 532-535 synaptic connections, 518-522 types, 517-519 Neostriatum, 362 See also Basal ganglia afferent fibers and neuron types, 364, 365, 372-373 mosaic organization, 379-381 Nernst equation, 41-42 Nerve impulse See Action potential Nervous system, organization of, 2-3 Neural images, multiple, 217 Neural network models, 451-453, 549, 555-556 See also under Neocortex, functional operations Neuromodulation vs neurotransmission, 62-63 713 Neuromuscular junction (NMJ), 10, 83 Neuron, concept of canonical, 25-27 as integrative unit, 22-27 Neuron doctrine, 548 Neuronal communication, types of, 58-63 Neuronal computation, biophysics of, 22 Neuronal elements, triad of, 2-3 Neuronal operations and underlying biophysical mechanisms, 22, 23 Neurone doctrine, 237 Neuronism, 237 Neuropeptides, 200-201, 443, 542 Neurotransmitter responses in CNS, common, 62-63 Neurotransmitters See also specific neurotransmitters ionic actions, 63-74 Nicotinic cholinergic responses, 64-65 Nicotinic receptors, 402 Nigrostriatal afferents, 367 Nitric oxide (NO), 5, 201, 402 Nitric oxide synthase (NOS), 5, 201 NMDA (W-methyl-D-aspartate) dendrodendritic interactions and, 190 excitatory amino acid responses and, 65-67 NMDA component of EPSP, 341, 394, 441, 480 NMDA (ion) channels, 394, 440 NMDA receptors See also Glutamate in basal ganglia, 394 GluR, 95 in hippocampus, 479, 487-488 in neocortex, 533 in olfactory bulb, 190, 208, 209 in olfactory cortex, 441 in retina, 250 in spinal cord, 95 in thalamus, 341 NMDA-dependent homosynaptic LTP, 437-439 Noradrenaline (NA), 344, 514-515 Noradrenaline (NA)-containing fibers, 201 Norepinephrine, 514-515, 542 and excitability of pyramidal neurons, 70-71 Nucleus of lateral lemniscus (nLL), 128, 129 Octopus cells (O), 129-131, 136-139, 144, 145 auditory-nerve fibers and, 130, 137, 139, 149 onset units from, 149-151 Odor See also Olfactory bulb; Olfactory cortex fast and slow oscillatory rhythms evoked by, 433-435 Odor contrast enhancement, lateral inhibition mediates, 214-215 714 Odor discrimination, functional mechanisms in, 212-214 Odor image, glomerular modules form, 210-211 Odor maps on olfactory bulb, methods for demonstrating, 210 Odor memory, modulation of recurrent inhibition mediates, 215-216 "Odor opponent" interactions, 215 Odor stimulation, responses to, 447-451 Odor-induced slow-temporal patterning of afferent input, 433-435 Olfactory bulb, 14, 34-35, 165 activity patterns elicited by, 210, 211 basic circuit, 181 centrifugal modulation, 185-186 input processing, 181, 182 output control, 181, 183 parallel pathways, 183-185 dendritic properties, 202-209 synchronization depends on, 208-209 functional circuits, 210-216 neuronal elements, 166-167 cell populations, 174 inputs, 168-170 intrinsic neurons, 172-174 oscillatory activity in neurons, 208-209 principal neurons, 170-172 neurotransmitters and neuromodulators, 196-202 gaseous messengers, 201 return projections from olfactory cortex to, 420 synaptic actions, 186 dendrodendritic, 186-192 glomerular, 192-196 synaptic connections, 174 external plexiform layer, 177-179 glia, 180-181 glomerular layer, 175-177 granule cell layer, 179-180 Olfactory cortex, 28, 169, 415-416 See also Piriform cortex defined, 415 excitatory circuitry horizontal organization of afferent system, 425 horizontal organization of association fiber systems, 425-426 laminar organization, 423-424 functional operations, 447-453 comparisons with other cortical systems, 453-454 inhibitory circuitry, 426-429 membrane and dendritic properties electrotonic structure, 443-444 integrative processes, 445-447 Index voltage-dependent processes, 444-445 neuronal elements, 417-420 afferent input, 419 cytoarchitecture, 416-417 neuromodulatory inputs, 419-420 nonpyramidal neurons, 422 numbers of pyramidal cells, 422 outputs, 420-421 principal neuron, 421 neurotransmitters, 441-443 primary, 454 synaptic actions, 433-437 afferent stimulation evokes series of postsynaptic currents, 433 dendritic processes, 431-432 synaptic potentials and currents, 430-431 synaptic connections, 422-423 Olfactory cortical areas, connections between, 415-416, 420 Olfactory discrimination and memory, role of olfactory cortex in, 451-453 Olfactory pathway, 166 main, 183 Olfactory receptor neurons (ORNs), 450 Olfactory sensory neurons, 196 Olfactory system, patterns of connectivity in, 450 Olivocerebellar circuit, 307-309 Onset units, 149 Optic nerve, 321 Optic stalk, 217 Optic tract, nucleus of, 324 Organelles, Output control, 35 Output convergence, 103 P cells See Midget (M) cells Pacemaker activity, 53 Paired-pulse facilitation (PPF), 483 Parabigeminal nucleus, 324 Parabrachial inputs, 343 Parabrachial region, 323 Parabrachial triad, 319-320 Parallel fibers (p.f.), 144, 275, 280-283 Paraolivary nucleus (PON), 128, 129 Paravermis, 278 Parvalbumin, 326 Patches, striatal, 379 Pathways, interregional, Pauser responses to sound, 151 Paw shake reflex, 115 Pedunculopontine tegmental nucleus, 323 Peptides See Neuropeptides Perceptrons See Feedforward networks Perforant pathway, 482 Index Periglomerular (PG) cells, 172, 199, 207-208 Periolivary nuclei (PON), 129 Permeability, ionic, 43, 45 Persistent current See Long-lasting (L) current Phaclofen, 539 Phase-locking in bushy cells, 155-157 defined, 156 Photon noise, 258, 266 Photoreceptors, 217-220 intensity range, 220-221 isolated rod, 220 spectral sensitivity, 221-222 Pinso terminale, 281 Piriform cortex, 415 anterior, 418, 419, 425, 426, 433, 439-440, 449 current-voltage relationship for deep pyramidal cell in, 444 inhibitory circuitry, 427-428 patterns of afferent fiber distribution to, 425 subdivisions of, 417-419 synaptic events evoked by afferent-fiber stimulation in, 432 synaptic plasticity and its regulation in, 437-441 temporal patterns of activity in, 433-437 Place cells, 496 Plasticity, homeostatic, 535 Plateau potentials, 51-52, 111, 112 Population excitatory postsynaptic potential (pEPSP), 475-476 Posterior division of the VCN (PVCN), 127-130 Posterior piriform cortex (PPC), 418, 419, 424-426, 432, 433, 439-440 "dispersive propagation" of afferent-evoked response in, 433, 434 Postsynaptic inhibition, microcircuits that mediate different types of, 13 Postsynaptic potentials (PSPs), 11, 122 See also Excitatory postsynaptic potentials; Inhibitory postsynaptic potentials fast, 64-69 latencies of mono- and disynaptic, 99 separation of, 12 slow, 69-74 Postsynaptic process, 3, Post-tetanic depression (PTD), 96 Post-tetanic potentiation (PTP), 96, 484-485 Potassium (K + ) channels, 336-338 Potassium (K+) conductance (gK), 338, 340 in cochlear nucleus cells, 148 in hippocampus, 489-495 increase in, 69-70 low-threshold, 148 715 in motor neurons, 93 in neocortex, 526-528 in neostriatal neurons, 382-387 in olfactory bulb cells, 195, 203-205 in olfactory cortex, 444-445 in thalamic cells, 336 Potassium (K + ) currents, 49, 55, 526-528 See also Ionic currents decrease in, 70-72 delayed rectifier, 56 transient, 56-57 Potassium (K + ) ions, 40 Potassium (K+)-mediated IPSP, 430 Potentiation, 67 Prediction units, 412 Predictive coding, 261 Prepiriform cortex See Piriform cortex Prepotential, 147 Presynaptic control, 9, 14 Presynaptic inhibition, 9, 12 Presynaptic process, 3, Primary afferent depolarization (PAD), 97, 98 Primary afferents, 81 Primarylike neurons, 153-156 Primarylike responses, 146 from bushy cells, 146-149 Primary like-with-notch (pri-N) responses, 148 Principal neurons See Relay neurons Projection neurons, 3, 369 See also Thalamic relay neurons Proprioceptors, 81 Propriospinal neurons, 84-85 Protein molecular components of cells, Pspike, 475 Pulvinar region, 314, 355 Purkinje cell connectivity, plasticity of, 283 Purkinje cell dendrite (Pcd), 280, 281 Purkinje cell layer of cerebellum, 279-281 Purkinje cells (PC), 28, 244 in cerebellar cortex, 287-288 in cerebellum, 216-211 See also Cerebellum climbing fiber activation, 290-291 Pyramidal cell layer of hippocampus, 458-460 Pyramidal (Py) cells (PC) in cochlear nucleus, 129, 131-133, 138, 144, 151-152 cortical, 24-30, 421 activation of excitatory inputs to, 74, 75 norepinephrine and excitability of, 70-71 synaptic potentials generated in, 68 deep, 417, 421 in hippocampus, 458 in neocortex, 504-506 in olfactory cortex, 421 Pyriform cortex See Piriform cortex 716 Quantal actions, 11 Quantum, 477 Raphe nucleus (Ra), 169 Rapidly inactivating current, 50 Rate coding, 110 Rebound response, 290, 307 Receptor molecules, 62 Reciprocal synapses, 14, 242 Recruitment, 109 Recurrent collaterals, 170 Recurrent excitation, 29, 104, 190, 192, 556-558 Recurrent inhibition, 13, 14 disynaptic, 102-104 Recurrent networks, 451-453, 554 Recurrent pathways, 483-484, 522 Re-excitation, 29 See also Recurrent excitation Reflex, stretch synaptic organization in, 101 Reflex interneurons See Spinal interneurons, dynamic control of Reflex pathways, 100-101 Reflex responses, automatic vs voluntary motor acts, 100-101 Reflex systems, disynaptic, 106-108 Reflexes, multisynaptic, 101-108 Regio inferior, 459 Regie superior, 459 Regional circuits, basic See Canonical circuits Reinforcement learning, 409-412 Relay neurons, See also Thalamic relay neurons Release failure, 95 Release probabilities, 10 Remote inhibition, 97 Renshaw cells, 102-104 Renshaw inhibition, 14 Renshaw interneurons, recurrent inhibition through, 102-104 Repetitive discharge of neocortical cells, 530-532 Repolarization, 45 Resistance/resistivity, 91-93, 110 Respiratory modulation, 433-435 Retention of sign, 10 Reticularism, 237 Retina, 34-35, 217-219, 269 dendritic and axonal properties amacrine cells, 252-253 bipolar to ganglion and amacrine cells, 252 horizontal to photoreceptor and bipolar cells, 251-252 individual retinal neurons are electronically compact, 250 Index neurotransmitters and postsynaptic receptors, 250 patterns of functional polarization, 248-250 photoreceptors to horizontal and bipolar cells, 250-251 development, 244-246 efficiency, 253-254 functional circuits, 253-254 for daylight, twilight, and starlight, 264-269 for ganglion cell receptive field, 254-257 how retinal circuits serve vision efficient coding strategies, 260-265 natural scenes contain fine detail at low contrast, 257-260 transmitting low-contrast neural image, 260 neuronal elements cell populations, 231-238 input elements, 218-222 intrinsic elements for forward transmission, 222-225 intrinsic elements for lateral transmission, 227-231 output elements, 225-227 synaptic connections inner plexiform layer, 242-244 outer plexiform layer (OPL), 238-242 Retinal triad, 320 Retinogeniculate inputs, 341-342 Retrograde messengers, Retrograde signaling, 73-74 Retzius-Cajal neuron, 510 Rhodopsin (Rh), 248, 253, 268 Rhythmic bursting, 344-345 Rhythmic generation, 31, 32 Ribbon synapse, 238-241 Rod bipolar circuit, 264 Saclophen, 539 Safety factors for synaptic transmission, 10 Scaling principle, 203 Schaffer collateral projection, 463 Schaffer collaterals, 469, 484 Scratch reflex, 100, 101 Semilunar cells (S), 417, 421, 424 Septotemporal axis (S-T), 456, 457 Serotonin (5-HT), 111,515 Serotonin-containing fibers, 201-202 "Sharp wave" activity, 483 Short-axon (SA) cells, 172 deep, 174 Shunting inhibition, 70, 430 Signal-to-noise enhancement, Signal-to-noise (S/N) ratio, 260-263 Silent synapses, 10 Index Silent/shunting inhibition, 11 Simple spikes, 292 Single-fiber group la ESPSs (sfEPSPs), 95 Size principle, 110, 113, 184 Sleep, transition to, 55 Sodium (Na + ) conductances, 336 Sodium (Na+) currents, 49-53, 525-526 See also Sodium (Na+) conductances in hippocampus, 489-495 in mitral cells, 203-205 in neocortex, 525-526 in neostriatal neurons, 382-384 in olfactory cortex, 444-445 in photoreceptors, 248 in Purkinje cells, 287 in thalamic cells, 336 Solitary cells of Meynert, 505 Soluble guanylate cyclase (sGC), 201 Somas, See also different cells Somatostatin (SOM)/nitric oxide synthetase (NOS)-containing interneurons, 370, 371, 402 Sound, buildup and pauser responses to, 151 Sound localization in horizontal plane, 155-157 Spatial contrast, 32-34 Spatial facilitation, 105, 106 Spatial summation, 11 nonlinear, 264 Specific local information processing, 26 Spherical bushy cells (SBC), 129-131, 136, 137, 140, 143, 144, 146 Spike See Action potential Spike frequency adaptation, 56, 70, 527 Spike-timing dependent (synaptic) plasticity (STOP), 440, 486, 487, 533 Spillover effect, 190 Spinal circuits, synaptic organization of, 100-108 Spinal cord, 79, 122-123 in action, 109-116 anatomy, 80 excitatory systems, 98-99 See also Group la afferents motor unit recruitment alternative recruitment patterns, 114-116 functional consequences, 116 intrinsic motoneuron properties related to, 110-111 synaptic organization underlying, 112-113, 115 motor units, 83-84 properties, 84, 85 recruitment, 109-110 types of, 83-84 111 neuronal elements, 79-86 postsynaptic excitation, 88-96 postsynaptic inhibition, 99-100 presynaptic inhibition, 86, 96-98 synaptic action in, 86-88 synaptic organization of ascending tracts, 108-109 "relay" vs integrative" functions, 108 synthesis, 109 Spinal interneurons, 84-86, 101-102 See also Renshaw interneurons dynamic control of, 116-122 Spindles, 348, 349 Spine action potentials, 546-547 Spines See also Dendritic spines horizontal cell, 240 Spiny branchlets, 281 Spiny neurons, 170 See also Pyramidal (Py) cells in basal ganglia, 369 See also Basal ganglia conditions for induction of LTD and LTP into, 394-395 dendritic membrane properties and, 382-387 intrinsic connections and, 400-401 synaptic types of neostriatal, 374-377 "sparsely," 504 Spiny stellate (St) cells, 506-507 Spontaneous rate fibers, high vs low, 158-159 Starburst amacrine cell, 21, 249 State dependence, 106-108, 118 Stellate (St) cells (SC), 28, 132, 134, 277-278, 298 spiny, 506-507 Stretch reflex inhibition, 118 Striatal interneurons, cortical and thalamic inputs to, 396-397 Striate cortex, 225 Striatum See Neostriatum Striosomes, 379, 380 Stumbling corrective reaction, 122 Subiculum, 474 Substantia nigra, 371, 375, 397-400 pars reticulata (SNr), 363 Substantia nigra pars compacta (SNc), 363 Subthalamic nucleus, 363 Superficial peroneal (SP) nerve, 118-122 Superficial pyramidal cells (SP), 417, 421 Superior colliculus, 324, 363 "Surround" mechanism reduces redundancy, 261-262 Sustained current See Long-lasting (L) current Synapse(s), 61-63 as basic unit of neural circuit organization, 3-6 718 Synapse(s) (continued) defined, as integrative micro-unit, mechanisms involved in signaling at, 3-5 as multifunctional multitemporal unit, 3-5 types of, 5-6 types and 2, 5-6 Synaptic and intrinsic currents, 74-77 Synaptic circuits See also Canonical circuits; Local/intrinsic circuits development of, levels of organization of, 6-8 Synaptic cleft, 61 Synaptic convergence, 9, 11-12, 14 Synaptic density, 113 Synaptic divergence, 9, 14 Synaptic efficacy, factors that control, 113-115 Synaptic integration, 488 Synaptic organization, 1-3 See also specific topics as multidisciplinary and multilevel subject, Synaptic scaling/normalization, 489 Synaptic strength See Synaptic efficacy Synaptic summation, as fundamentally nonlinear, 11 Synaptic system, 113 Synaptic terminal, types of, 316-318 Synaptic transmission in reverse See Retrograde signaling Synchronization, 8, 10 T channels, 336-338 anatomical relationship of modulator inputs to, 348 Temporal contrast, 32, 34 Temporal differentiation, 13 Temporal summation, 11 Terminal tuft (T), 19 Tetanic depression, 96 Tetrodotoxin (TTX), 287-288, 290, 301, 383, 495 Thalamic afferents, 366-367, 512-514 Thalamic neurons, 74-75 Thalamic nuclear groups, major, 312-314 Thalamic nucleus, major types of afferent to, 314-315 Thalamic relay neurons, 314, 324-326, 329-334 classes of, 325-326 firing mode, 58, 72-73 inputs to, 328-329 noradrenaline's effects on, 344 Thalamic relay(s) first and higher order, 312, 353-356 gating and other transformations in, 344, 348-350 Index brainstem inputs, 350 burst and tonic relay response modes, 344-348 cortical inputs from layer 6, 350-351 Thalamic reticular nucleus, 331, 332 cells of, 328 inputs from, 323, 348-350 Thalamocortical cells (TC), 28 Thalamocortical relationships, 355-356 Thalamus, 311-312, 359, 363 basic neuronal circuit, 329 component populations, 329-330 intrinsic circuitry, 330-332 dendritic cable properties, 332-334 drivers and modulators, 314, 351-353 general organization, 312-315 maps, 315-316 parallel processing, 315 how it relates to motor outputs, 357 motor links of first order afferent drivers, 357-358 motor links of higher order afferent drivers, 358-359 relationships of sensory perception to mechanisms of motor control, 359 interneurons, 326-327, 334, 342 inputs to, 329 membrane properties, 334-340 of monkey, 312-313 neuronal elements, 316, 324-327 electron microscopic appearance of, 316-320 inputs, 320-324 synaptic connections, 328-329 synaptic transmission brainstem inputs, 343-344 GABAergic inputs, 342-343 glutamatergic inputs, 341-342 ionotropic and metabotropic receptors, 340-341 Theta, 485 Theta burst pairing, 485-486 Theta burst stimulation, 485 Thorny excrescence, 467-468 Tibialis anterior (TA), 117 T-multipolar cells, 129, 130, 136, 138, 143-147, 159 chopper responses from, 146 Tonic mode of firing, 338, 339 See also Burst and tonic relay response modes Tonotopic map, 125 Tract cells, 85 Transient current, 50 Transmitter substance, Transverse axis (TRANS), 456, 457 Index Trapezoid body (TB), 128-130, 144 Trigger features, 550 Trisynaptic circuit, 463 Tuberculoventral cells See Vertical (tuberculoventral) cells Tuberomammilary nucleus of hypothalamus, 324 Tufted cell membrane properties, synchronization by, 209 Tufted cells, 171-172, 184, 194, 199 external (Te), 171 internal (TO, 171 middle (Tm), 171 "Twitching spine" hypothesis, 546 Two-port, nonreciprocal, Tyrosine hydroxylase (TH), 375 Varicosity/bouton, Ventral anterior thalamic nuclei, 312 Ventral cochlear nucleus (VCN), 144, 145 anterior division, 127-129, 137 cell types in, 129-131 posterior division, 127-130 synapses in, 136-140 Ventral horn, synaptic types in, 86, 87 Ventral horn interneurons, 86 Ventral lateral thalamic nuclei, 312 Ventral nucleus of lateral lemniscus (VnLL), 129 719 Ventral posterior thalamic nuclei, 312 Ventral spinocerebellar tract neurons (VSCT), 107-109 Ventral thalamus, 311 Ventricular cells, symmetrical and asymmetrical modes of division, 501-503 Ventricular zone (VZ), 501-503 Vermis, 278 Vertical (tuberculoventral) cells (V), 132, 133, 138 Vesicles, synaptic, 3-6, 61, 240, 268 Visual cortex, basic circuit for, 524-525 Visual system, compared with olfactory system, 454 Visual transduction, 246-248 Voltage clamp, 45 Voltage-dependent channels, 336-338 Voltage-dependent processes, 444-445 Voltage-gated Ca2+ channels (VGCCs), 192, 493 Voltage-gated currents, 45, 47, 51 high-voltage activated currents, 53-54 Voltage-gated Na+ channels, 489-491 Voltage-sensitive ion channels, 47 Voltage-sensitive membrane currents, 45, 149 Vomeronasal organ (VNO), 185 Waking, transition to, 55 Waveform of stimulus, 157 .. .THE SYNAPTIC ORGANIZATION OF THE BRAIN This page intentionally left blank THE SYNAPTIC ORGANIZATION OF THE BRAIN Fifth Edition Edited by Gordon M Shepherd OXFORD UNIVERSITY... photocopying, recording, or otherwise, without the prior permission of Oxford University Press Library of Congress Cataloging-in-Publication Data The synaptic organization of the brain / edited by Gordon... that there is a lack of basic principles for understanding the vast amount of information about the brain that is accumulating One The Synaptic Organization of the Brain of the main aims of this