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Neurotransmitter Actions in the Vertebrate Nervous System PDF

524 Pages·1985·12.14 MB·English
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Neurotransmitter Actions in the Vertebrate Nervous System Neurotransmitter Actions in the Vertebrate Nervous System Edited by Michael A. Rogawski and Jeffery L. Barker National Institute of Neurological and Communicative Disorders and Stroke National Institutes of Health Bethesda, Maryland PLENUM PRESS • NEW YORK AND LONDON Library of Congress Cataloging in Publication Data Main entry under title: Neurotransmitter actions in the vertebrate nervous system. Includes bibliographies and index. 1. Neurotransmitters. 2. Nervous system-Vertebrates. I. Rogawski, Michael A. II. Barker, Jeffery L. [DNLM: 1. Neuroregulators-physiology. QV 126 N4938j QP364.7.N465 1985 596'.0188 85-16784 ISBN-IS: 978-1-4684-4963-1 e-ISBN-13: 978-1-4684-4961-7 DOl: 10.1007/978-1-4684-4961-7 Cover: Upper traG.es show continuous recording of elementary Cl- ion-channel cur- rents activated by the transmitter GABA in a patch of membrane excised from the cell body of a cultured mouse spinal cord neuron and held at -60 mV. Lower trace reflects a synaptically activated Cl- current recorded at -60 mV in another cultured mouse spinal cord neuron that is most likely mediated by GABA. The time scales of the il- lustrated pharmacological and physiological activities are similar. The elementary ion-channel events are about one picoampere (pA) in amplitude, while the synaptic current peak is about 400 pA. Thus, the peak of the synaptic current is comprised of some 400 ion channels and the time course of decay reflects the histogram of ion channel durations with most channels staying open briefly and fewer and fewer re- maining open for longer and longer periods. This broad spectrum of channel dura- tions can easily be seen in the patch-clamp recording. (G. A. Redmann, H. Lecar, R. N. McBurney, and J. L. Barker, unpublished observations. See Chapter 3 for further details.) ©1985 Plenum Press, New York Softcover reprint of the hardcover 1st edition 1985 A Division of Plenum Publishing Corporation 233 Spring Street, New York, N.Y. 10013 All rights reserved No part of this book may be reproduced, stored in a retrieval system, or transmitted, in any form or by any means, electronic, mechanical, photocopying, microfilming, recording, or otherwise, without written permission from the Publisher Contributors B. E. ALGER • Department of Physiology, University of Maryland School of Medicine, Baltimore, Maryland 21201 JEFFERY 1. BARKER. Laboratory of Neurophysiology, National Institute of Neurological and Communicative Disorders and Stroke, National In- stitutes of Health, Bethesda, Maryland 20892 BENJAMIN S. BUNNEY • Departments of Psychiatry and Pharmacology, Yale University School of Medicine, New Haven, Connecticut 06510 ROBERT A. DAVIDOFF • Department of Neurology, University of Miami School of Medicine, and Neurology Service, Veteran's Administration Medical Center, Miami, Florida 33101 JOHN R. DELFS. The William P. Arnold Pain Treatment and Research Center, New England Deaconess Hospital, and Departments of Neurol- ogy, Harvard Medical School, Beth Israel Hospital, and Children's Hos- pital, Boston, Massachusetts 02115 MARC A. DICHTER. Departments of Neurology, Harvard Medical School and Beth Israel Hospital, and Department of Neuroscience, Children's Hospital, Boston, Massachusetts 02115 RAYMOND DINGLEDINE • Department of Pharmacology, University of North Carolina, Chapel Hill, North Carolina 27514 J. J. DREIFUSS • Department of Physiology, University Medical Center, Ge- neva, Switzerland NAE J. DUN. Department of Pharmacology, Loyola University, Stritch School of Medicine, Maywood, Illinois 60153 ANTHONY A. GRACE. Departments of Psychology and Psychiatry, The University of Pittsburgh, Pittsburgh, Pennsylvania 15260 v vi Contributors HELMUT L. HAAS. Neurophysiology Laboratory, Neurochirurgische Universitatsklinik, CH-8091 Zurich, Switzerland JOHN C. HACKMAN. Department of Neurology, University of Miami School of Medicine, and Neurology Service, Veteran's Administration Medical Center, Miami, Florida 33101 BARBARA K. HENON • Division of Neuroscience, Beckman Research In- stitute of the City of Hope, Duarte, California 91010 LILY YEH JAN • Department of Physiology, University of California, San Francisco, San Francisco, California 94143 YUH NUNG JAN • Department of Physiology, University of California, San Francisco, San Francisco, California 94143 JOHN S. KELLY • Department of Pharmacology, The University of Edin- burgh, Edinburgh EH8 9JZ, England SHIRO KONISHI. Department of Pharmacology, Faculty of Medicine, Tokyo Medical and Dental University, Bunkyo-ku, Tokyo 113, Japan MARK L. MAYER. Laboratory of Developmental Neurobiology, National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, Maryland 20892 DONALD A. McAFEE. Division of Neuroscience, Beckman Research In- stitute of the City of Hope, Duarte, California 91010 MICHEL MOHLETHALER • Department of Physiology, University Medical Center, Geneva, Switzerland ANDREA NISTRI • Department of Pharmacology, st. Bartholomew's Hospital Medical College, University of London, London EC.1M 6BQ, England MARIO RAGGENBASS • Department of Physiology, University Medical Center, Geneva, Switzerland MICHAEL A. ROGA WSKI • National Institute of Neurological and Com- municative Disorders and Stroke, National Institutes of Health, Be- thesda, Maryland 20892 C. P. VA NDERMAELEN • Preclinical CNS Research, Pharmaceutical Re- search and Development, Bristol-Myers Company, Evansville, Indiana 47721 GARY L. WESTBROOK • Laboratory of Developmental Neurobiology, Na- tional Institute of Child Health and Human Development, National In- stitutes of Health, Bethesda, Maryland 20892 Preface Intercellular communication via bioactive substances occurs in virtually all multicellular systems. Chemical neurotransmission in the vertebrate nervous system represents a form of signaling of this type. The biology of chemical neurotransmission is complex, involving transmitter synthesis, transport, and release by the presynaptic neuron; signal generation in the target tissue; and mechanisms for termination of the response. The focus of this book is on one aspect of this scheme: the diverse electrophysiological effects induced by different neurotransmitters on targets cells. In recent years, astonishing progress has been made in elucidating the specific physiological signals mediated by neurotransmitters in the verte- brate nervous system, yet, in our view, this has not been adequately recog- nized, perhaps because the new concepts have yet to filter into neuroscience textbooks. Nevertheless, the principles of neurotransmitter action are critical to advances in many areas of neuroscience, including molecular neurobiol- ogy, neurochemistry, neuropharmacology, physiological psychology, and clinical neuroscience. It was the need for a sourcebook that prompted us to engage a group of neurophysiologists to prepare the chapters in this volume. However, there was an additional reason for this book: more and more it seemed that the field, if not yet having reached maturity, at least was ap- proaching adolescence, with strengths in some areas and healthy conflicts in others. At this stage of development a textbook can help to define a field, clarify problems to be resolved, and identify areas for future investigation. This book is organized into five parts, each containing one or more chapters on chemically related transmitter agents: amino acids, acetylcho- line, biogenic amines, neuropeptides, and purines. In keeping with the broad audience to which the book is directed, most chapters contain introductory material on the anatomy, neurochemistry, and receptor pharmacology of the transmitter system whose physiology is discussed, and the main discussion is directed to the nonspecialist. Nevertheless, readers will require familiarity vii viii Preface with standard concepts in neurophysiology, and as such this volume com- plements, but does not replace, presently available textbooks. For the most part, this book leaves discussion of transmitter actions at the skeletal neuro- muscular junction and in autonomic effector tissues to these textbooks, and focuses on the less familiar context of the central nervous system and pe- ripheral ganglia. The actions of well established transmitters-such as GABA, norepinephrine, and acetylcholine-are explored in this new territory as are a host of novel chemical agents, including neuropeptides and purines. How- ever, many more putative transmitter substances have been discovered using histochemical, biochemical, and, more recently, molecular biological tech- niques than are covered in these chapters. We have of necessity only included chapters on those substances that have been studied most extensively using neurophysiological techniques. We have also decided to limit our coverage to vertebrates, although in some chapters comparisons are made with invertebrate systems. Recent tech- nical developments and the advent of new preparations of the vertebrate nervous system have made vertebrate neurons as accessible to microelectrode recording as invertebrate cells, and this has allowed the field of vertebrate neurotransmitter physiology to flourish on equal footing with work in in- vertebrates. For those who are interested, neurotransmitter actions in inver- tebrates have been covered in a number of excellent books and reviews. We are grateful to those authors who have allowed figures from their original publications to be reproduced in this book and who have generously provided preprints of papers in press. We thank the following individuals for reading and providing useful comments on some of the chapters: B. E. Alger, R. J. Dingledine, J. M. Lakoski, M. R. Martin, and G. L. Westbrook. Finally, our editor at Plenum, Kirk Jensen, deserves special acknowledgment for his advice, support, and forebearance throughout the years that this book evolved from concept to reality. Michael A. Rogawski Jeffery L. Barker Bethesda, Maryland Contents Introduction ................................................................... xix Michael A. Rogawski and Jeffery 1. Barker PART I. AMINO ACIDS 1. GABA: Presynaptic Actions Robert A. Davidoff and John C. Hackman 1. Introduction .......... ; ...................................................... 3 2. Presynaptic Inhibition ..................................................... 3 3. Primary Afferent Depolarization .......................................... 4 4. The Eccles' Hypothesis .................................................... 6 5. Mechanisms of PAD ........................................................ 6 5.1. K+ and PAD ........................................................... 8 5.2. Two Components to PAD ............................................ 8 6. Distribution of GABA in the Spinal Cord ................................ 8 7. GABA and Afferent Terminals ............................................ 9 7.1. Afferent Terminals in the Cat Spinal Cord ........................ 10 7.2. The Isolated Spinal Cord ............................................ 11 7.3. The Dorsal Root Ganglion ........................................... 13 7.4. Sensory Neurons in Culture ........................................ 16 7.5. The Dorsal Column Nuclei .......................................... 16 7.6. Characteristics of the GABA Receptor on Afferent Neurons ..... 16 8. GABA Metabolism and PAD ............................................. 24 9. GABA Desensitization .................................................... 24 ix X Contents 10. GABA and Other Presynaptic Terminals ................................ 26 10.1. Sympathetic Ganglia ............................................... 26 10.2. Olfactory Cortex .................................................... 28 11. Autoreceptors .............................................................. 28 12. Summary ................................................................... 28 References .................................................................. 29 2. GABA and Glycine: Postsynaptic Actions B. E. Alger 1. Background ................................................................ 33 1.1. GAB A in the Invertebrate Nervous System ........................ 34 1.2. GABA in the Vertebrate CNS ....................................... 35 1.3. Glycine in the Vertebrate CNS ...................................... 37 1.4. GABA Receptor Complexes ......................................... 38 2. Physiological Actions in the Central Nervous System ................. 39 2.1. Release Mechanisms ................................................. 40 2.2. Membrane Mechanisms ............................................. 44 2.3. Termination of Transmitter Action ................................ 52 2.4. Use-Dependence of IPSPs ........................................... 53 3. Modes of Inhibitory Action ............................................... 57 3.1. Prevention of Impulse Generation .................................. 57 3.2. Dendritic Inhibition .................................................. 58 3.3. Dendrodendritic Inhibition ......................................... 59 4. Physiological Actions of GABA in Peripheral Systems ................ 62 4.1. Sympathetic Ganglia ................................................. 62 4.2. Parasympathetic Ganglia ............................................ 63 4.3. Myenteric Plexus ..................................................... 63 5. Conclusions and Functional Considerations ............................ 64 References .................................................................. 65 3. GABA and Glycine: Ion Channel Mechanisms Jeffery L. Barker 1. Introduction ................................................................ 71 2. Electropharmacology of CI- Conductance Mechanisms ............... 72 2.1. Current-Clamp Observations ........................................ 72 2.2. Voltage-Clamp Observations ........................................ 74 3. Synaptically Activated CI- Conductance Mechanisms ................ 89 3.1. Long-Lasting Synaptic Conductance in Cultured Hippocampal Neurons ............................................... 92 3.2. Pharmacological Modulation of IPSCs in Cultured Hippocampal Neurons ............................................... 95 Contents xi 4. Conclusions ................................................................ 97 References .................................................................. 98 4. Glutamate Andrea Nistri 1. Introduction .............................................................. 101 1.1. Overview and Synaptic Pathways ................................ 101 1.2. Distribution and Release .......................................... 103 2. Physiological Actions of Glutamate ................................... 105 2.1. Invertebrate Preparations .......................................... 105 2.2. The Lamprey, a Lower Vertebrate ................................ 106 2.3. Amphibia and Mammals .......................................... 107 3. Glutamate Agonists ...................................................... 111 4. Excitatory Amino Acid Receptors ..................................... 114 5. Implications for Clinical Medicine and Neurotoxicology ........... 116 6. Conclusion ............................................................... 117 References ................................................................ 118 5. Excitatory Amino Acids: Membrane Physiology Mark 1. Mayer and Gary 1. Westbrook 1. Introduction .............................................................. 125 1.1. Receptor Pharmacology ............................................ 125 1.2. Physiology .......................................................... 126 2. Intracellular Recording, Voltage Clamp and Patch Clamp .......... 127 2.1. N-Methyl-D-aspartic Acid (NMDA) ............................... 127 2.2. Glutamate and Aspartate .......................................... 130 3. Excitatory Synaptic Transmission ..................................... 135 3.1. The la EPSP ........................................................ 135 3.2. Excitatory Transmission in the Hippocampus .................. 136 3.3. Excitatory Transmission in Spinal Cord Cultures .............. 136 4. Summary and Commentary ............................................ 137 References ................................................................ 137 PART II. ACETYLCHOLINE 6. Acetylcholine John S. Kelly and Michael A. Rogawski 1. Introduction .............................................................. 143

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