The Pain System The Neural Basis of Nociceptive Transmission in the Mammalian Nervous System
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1 The Pain System The Neural Basis of Nociceptive Transmission in the Mammalian Nervous System
2 Pain and Headache Vol. 8 Series Editor Philip L. Gildenberg, Houston, Tex. KARGER S.Karger Basel Miinchen: Paris London New York Tokyo Sydney
3 The Pain System The Neural Basis of Nociceptive Transmission in the Mammalian Nervous System W.D. Willis, Jr. Marine Biomedical Institute and Departments of Anatomy and of Physiology and Biophysics, University of Texas Medical Branch, Galveston, Tex., USA 152 figures and 4 tables, 1985 KARGER S.Karger Basel Munchen. Paris London New York. Tokyo Sydney
4 Pain and Headache National Library of Medicine, Cataloging in Publication Willis, William D., The pain system: the neural basis of nociceptive transmission in the mammalian nervous system W.D. Willis, Jr. -Basel; New York: Karger, (Pain and headache; v. 8) Bibliography: p. Includes index. I. Neural Transmission 2. Nociceptors - physiology 3. Pain - physiology I. Title II. Series WI PA293 v. 8 [WL 104 W135p] ISBN Drug Dosage The author and the publisher have exerted every effort to ensure that drug selection and dosage set forth in this text are in accord with current recommendations and practice at the time of publication. However, in view of ongoing research, changes in government regulations, and the constant flow of information relating to drug therapy and drug reactions, the reader is urged to check the package insert for each drug for any change in indications and dosage and for added warnings and precautions. This is particularly important when the recommended agent is a new and/or infrequently employed drug. All rights reserved. No part of this publication may be translated into other languages, reproduced or utilized in any form or by any means, electronic or mechanical, including photocopying, recording, microcopying, or by any information storage and retrieval system, without permission in writing from the publisher. \!:) Copyright 1985 by S. Karger AG, P.O. Box, CH-4009 Basel (Switzerland) Printed in Switzerland by Thiir AG Offsetdruck, Pratteln ISBN
5 Contents Preface... IX Chapter 1 Introduction 5 Conclusions Chapter 2 Evidence for Nociceptive Transmission Systems 7 Nociceptors Nociceptive Ascending Tracts Participation of Higher Centers in Nociception Experimental Approaches to the Investigation of Pain Transmission Systems. 17 Criteria for Identification of Nociceptive Neurons Conclusions Chapter 3 Nociceptors 22 Historical Overview Nociceptors Cutaneous Nociceptors AI) Mechanical Nociceptors C Polymodal Nociceptors Other Types of Cutaneous Nociceptors Role of Cutaneous Nociceptors in Pain Sensation First and Second Pain Electrical Stimulation of Peripheral Nerve Fibers Correlation of Human Pain Sensation with Responses of Nociceptors in Humans
6 Contents VI Correlation of Human Pain Sensation with Responses of Nociceptors in Animals Hyperalgesia Chemical Basis for Activation and Sensitization of Nociceptors Anatomical Distribution of Hyperalgesia Muscle Nociceptors Group III Muscle Receptors Group IV Muscle Receptors Role of Muscle Nociceptors in Pain Joint Nociceptors Role ofjoint Nociceptors in Pain Visceral Nociceptors and Referred Pain Nociceptors in the Cardiovascular System and Their Role in Cardiac Pain.. 66 Nociceptors in the Respiratory System Lung Irritant Receptors Type J Receptors Role of Respiratory Nociceptors in Pain Nociceptors in the Gastrointestinal Tract Role of Gastrointestinal Nociceptors in Pain Nociceptors in the Genitourinary Tract , 71 Role of Genitourinary Nociceptors in Pain..., 73 Conclusions Chapter 4 Nociceptive Afferent Input to the Dorsal Hom 78 Historical Overview Dorsal Root Ventral Root Segregation of Large and Small Afferent Fibers in the Dorsal Root Lissauer's Tract Terminations of Fine Afferent Fibers in the Dorsal Hom " 92 Synaptic Endings of Primary Afferent Fibers in the Dorsal Hom Transmitters Associated with Fine Afferent Fibers Cell Types in the Dorsal Hom Lamina I Lamina II... ' Laminae III and IV Lamina V Lamina VI Intermediate Region and Ventral Hom Responses of Dorsal Hom Intemeurons to Noxious Inputs Other than from Skin Pharmacological Responses of Nociceptive Dorsal Hom Neurons Conclusions
7 Contents VII Chapter 5 Ascending Nociceptive Tracts 145 Historical Overview Spinothalamic Tract Cells of Origin Organization of the Spinothalamic Tract in the Spinal Cord and Brain Stem Thalamic Nuclei of Termination Identification of Spinothalamic Tract Cells in Physiological Experiments Responses of Spinothalamic Tract Cells to A and C Fiber Volleys Responses of Spinothalamic Tract Cells to Natural Forms of Stimulation. 164 Responses of Spinothalamic Tract Cells Projecting to the Medial Thalamus 172 Effects of Capsaicin Influence of Anesthesia Receptive Field Organization Prolonged Inhibition following Peripheral Nerve Stimulation 181 Pharmacology of Spinothalamic Tract Cells 184 Role of Spinothalamic Tract in Pain Transmission 184 Spinoreticular Tract Cells of Origin Organization of the Spinoreticular Tract in the Spinal Cord and Brain Stem 191 Nuclei of Termination in the Reticular Formation Identification of Spinoreticular Neurons in Physiological Experiments Electrophysiological Response Properties of Spinoreticular Neurons and Role in Pain Spinomesencephalic Tract Cells of Origin Organization of the Spinomesencephalic Tract in the Spinal Cord and Brain Stem Nuclei of Termination in the Midbrain Identification of Spino mesencephalic Neurons in Physiological Experiments 195 E1ectrophysio10gical Response Properties of Spinomesencephalic Tract Cells and Role in Pain Dorsally Situated Ascending Pathways That May Be Nociceptive Spinocervical Tract Lateral Cervical Nucleus Cells of Origin Organization of Spinocervical Tract and Destination of Terminals 199 Identification of Spinocervical Tract Neurons Response Properties of Spinocervical Tract Cells 200 Postsynaptic Dorsal Column Pathway Cells of Origin Organization of the Postsynaptic Dorsal Column Pathway and Destination of Terminals Identification of Postsynaptic Dorsal Column Neurons Response Properties of Postsynaptic Dorsal Column Cells 205
8 Contents VIII Role of the Spinocervical Tract and of the Postsynaptic Dorsal Column Pathway in Pain Conclusions Chapter 6 Nociceptive Transmission to Thalamus and Cerebral Cortex 213 Historical Overview Thalamic Nuclei Receiving Nociceptive Input from the Spinothalamic Tract: Ventral Posterior Lateral Nucleus Evidence that Nociceptive Spinothalamic Tract Axons End in the VPL Nucleus Nociceptive Responses of Neurons in the VPL Nucleus Monkey Cat Rat Thalamic Nuclei Other than VPL Receiving Input from the Spinothalamic Tract Medial Part of the Posterior Complex (PO,J Intralaminar Nuclei Nucleus Submedius Thalamic Reticular Nucleus Thalamic Nuclei in Which Alternative Nociceptive Tracts End Nociceptive Responses of Neurons in the Somatosensory Cerebral Cortex Monkey SI Cortex Rat SI Cortex Monkey SII Cortex Cat SII Cortex Role of the Thalamus and Cortex in Pain Conclusions Chapter 7 Overview and Future Directions Nociceptors Input System Nociceptive Tracts Thalamocortical Mechanisms..... Plasticity Descending Control Systems Conclusions References Subject Index
9 Preface This review is intended to provide an overview of our current understanding of the nociceptive transmission system. However, because of limitations of time and space, the emphasis will be on nociceptive systems supplying the body. The trigeminal system will be discussed only when findings on the trigeminal system are helpful as a confirmation of principles pertinent to both the trigeminal and body nociceptive systems or where the evidence is most complete in the trigeminal system. I would like to thank my colleagues who participed in the experiments described here that were done in my laboratory, including A.E. Applebaum, J.E. Beall, R.N. Bryan, J.M. Chung, c.l. Clifton, R.E. Coggeshall, J.D. Coulter, K. Endo, Z.R. Fang, R.D. Foreman, K.D. Gerhart, G.I. Giesler, L.H. Haber, M.B. Hancock, Y. Hori, L.M. Jordan, D.R. Kenshalo, Jr., G.A. Kevetter, K.H. Lee, R.B. Leonard, R.F. Martin, R.I. Milne, B.D. Moore, R.F. Schmidt, B.J. Schrock, H.R. Spiel, D.L. Trevino, W.H. Vance, W.S. Wi/lcockson, and R.P. Yezierski. I would also like to express my appreciation to Phyllis Waldrop for typing the manuscript, to Margie Watson for proofreading, and to Calvin Cargill and Helen Willcockson for the illustrations. The work that was done in my laboratory was supported by NIH grants NS and NS and by a grant from the Moody Foundation. Galveston, 1984 W.D. Willis, Jr.
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