Processing of Sensory Information in the Superficial Dorsal Horn of the Spinal Cord NATO ASI Series Advanced Science Institutes Series A series presenting the results of activities sponsored by the NATO Science Committee, which aims at the dissemination pf advanced scientific and technological knowledge, with a view to strengthening links between scientific communities. The series is published by an international board of publishers in conjunction with the NATO Scientific Affairs Division A Life Sciences Plenum Publishing Corporation B Physics New York and London C Mathematical Kluwer Academic Publishers and Physical Sciences Dordrecht, Boston, and London D Behavioral and Social Sciences E Applied Sciences F Computer and Systems Sciences Springer-Verlag G Ecological Sciences Berlin, Heidelberg, New York, London, H Cell Biology Paris, and Tokyo Recent Volumes in this Series Volume 170-ras Oncogenes edited by Demetrios Spandidos Volume 171-Dietary w3 and w6 Fatty Acids: Biological Effects and Nutritional Essentiality edited by Claudio Galli and Artemis P. Simopoulos Volume 172-Recent Trends in Regeneration Research edited by V. Kiortsis, S. Koussoulakos, and H. Wallace Volume 173-Physiology of Cold Adaptation in Birds edited by Claus Bech and Randi Eidsmo Reinertsen Volume 174-Cell and Molecular Biology of Artemia Development edited by Alden H. Warner, Thomas H. MacRae, and Joseph C. Bagshaw Volume 175-Vascular Endothelium: Receptors and Transduction Mechanisms edited by John D. Catravas, C. Norman Gillis, and Una S. Ryan Volume 176-Processing of Sensory Information in the Superficial Dorsal Horn of the Spinal Cord edited by F. Cervero, G. J. Bennett, and P. M. Headley Series A: Life Sciences Processing of Sensory Information in the Superficial Dorsal Horn of the Spinal Cord Edited by F. Cervera University of Bristol Medical School Bristol, United Kingdom G. J. Bennett National Institute of Dental Research National Institutes of Health Bethesda, Maryland and P. M. Headley University of Bristol Medical School Bristol, United Kingdom Plenum Press New York and London Published in cooperation with NATO Scientific Affairs Division Proceedings of a NATO Advanced Research Workshop on Processing of Sensory Information in the Superficial Dorsal Horn of the Spinal Cord, held May 22-27, 1988, in EI Escorial, Spain Library of Congress Cataloging in Publication Data NATO Advanced Research Workshop on Processing of Sensory Information in the Superficial Dorsal Horn of the Spinal Cord (1988: San Lorenzo del Escorial, Spain) Processing 01 sensory information in the superficial dorsal horn of the spinal cord I edited by F. Cervera, G. J. Bennett, and P. M. Headley. p. cm.-(NATO ASI series. Series A, Life sciences; v. 176) "Proceedings of a NATO Advanced Research Workshop on Processing of Sen· sory Information in the Superficial Dorsal Horn of the Spinal Cord, held May 22-27,1988, in EI Escorial, Spaln"-T.p. verso. "Published in cooperation with NATO Scientific Affairs Division." Includes bibliographies and indexes. ISBN 978-1-4612-8101-6 e-1SBN-13:978-1-4613-0825-6 001:10.1007/978-1-4613-0825-6 1. Spinal cord-Congresses. 2. Afferent pathways-Congresses. I. Cervera, Fernando. II. Bennett, G. J.(Gary J.) III. Headley, P. M. IV. North Allantic Treaty Organization. Scientific Affairs Division. V. Title. VI. Series. QP371.N37 1989 599'.0188-dc20 DNLMIDLC 89·16161 for Library of Congress CI P © 1989 Plenum Press, New York Softcover reprint of the hardcover I st edition 1998 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 Publlsher PREFACE This book constitutes the proceedings of a NATO Advanced Research Workshop held in El Escorial (Spain) from 22 - 27 May 1988 with the title Processing of sensory information in the superficial dorsal hom of the spinal cord. Included in the book are reports of most of the main lectures given at the meeting, section introductions written by each session Chairman, section reports compiled by session rapporteurs and some short papers invited from authors of communications given in poster form. The latter were selected on the basis of being immediately relevant to the topic of the workshop and of originating from a laboratory not represented by the main speakers. All in all we believe that the reader can get a fair idea of the structure and general character of this Workshop. The overall aim of the meeting was to review the current state of knowledge on the role of the superficial dorsal horn of the mammalian spinal cord as a nucleus of relay and modulation of the somatic and visceral sensory input to the central nervous system. In this context, the contribution of this spinal cord region to the appreciation of pain was a central topic of discussion. Over the last decade there has been a considerable increase in anatomical, physiological and neurochemical studies of the superficial dorsal horn. This surge of interest has had the beneficial effect of exposing the limitations of the old concepts and of forcing a change of direction of research in this field. However, such major revision has also produced a plethora of publications and a number of different views and contradictory opinions. With this Workshop and through the vehicle of its proceedings we hope to provide a review of the new data so as to test the strength of the ideas emerging from recent work and to identify directions for future research. Unfortunately, not every scientist working in the field has contributed to our book. Some could not come to the meeting, a few speakers did not submit a paper and, inevitably, limitations of time, space and funds meant a restricted programme of invited speakers and talks. We regret the gaps but believe that the reader will nevertheless find that most of the new data and ideas and virtually all the active research groups are represented in this volume. Contrary to common practice with this type of publication, we have had all the submitted papers refereed. Reviewers were selected mainly from the participants to the meeting so that they could provide an informed view on the papers from their direct knowledge of the presentation and of the subsequent discussion. Although refereeing has inevitably lengthened publication time we firmly believe that it has been worth it since many papers have been improved and clarified following the reviewers comments. v The meeting was sponsored by the Scientific Affairs Division of NATO and we wish to express our appreciation to NATO for their help and financial support, and particularly to Dr Craig Sinclair who shared with us a few days of the Workshop and provided helpful comments and advice. Two UK organizations, the Well come Trust and The Physiological Society helped to fund the attendance of young British scientists and we are most grateful for their help. Finally two members of the pharmaceutical industry - Merck Sharp and Dohme and Parke Davis - also provided funds to help with the running of the meeting. A number of individuals have helped beyond the call of duty with the organization of the meeting and with the editing of this book. We have been particularly fortunate to have the secretarial help of Mrs Ruth Alexander throughout the running of the Workshop and the preparation of this book. To her, to the referees of the contributions and to everyone else who has helped us with this project we offer our thanks. F.Cervero G.!. Bennett P.M. Headley vi CONTENTS The Superficial Dorsal Horn F. Cervero .................................................................................................................................... 1 SECTION I: AFFERENT INPUTS TO THE SUPERFICIAL DORSAL HORN Introduction ............................................................................................................................... 13 Distribution of unmyelinated primary afferent fibres in the dorsal horn Y. Sugiura, N. Terui, Y. Hosoya and K. Kohno ................................................................... 15 Spinal projections of thin myelinated deep afferents and their topical relation to dorsal horn neurones processing deep input U. Hoheisel and S. Mense ....................................................................................................... 29 The distribution of muscle and cutaneous projections to the dorsal horn of the upper cervical cord of the cat V.C. Abrahams .......................................................................................................................... 41 Electron microscopic localization of peptide-like immunoreactivity in labelled dorsal root terminals in the spinal substantia gelatinosa of the monkey A.R. Light and A.M. Kavookjian ........................................................................................... 57 Immunoreactivity of rat primary afferent neurones with C-and A-fibres S.N. Lawson, P. McCarthy and P.J. WaddelL ..................................................................... 71 Coexistence of peptides in primary afferent neurones V.S. Seybold, M.M. Tuchscherer and M.G. Garry .............................................................. 75 Laminar and segmental termination in the dorsal horn of the spinal cord of an articular nerve of the forepaw in the cat E. Rausell and C. Avendano ................................................................................................... 83 vii Spinal termination of primary alTerents of the cat's knee joint H.-G. Schaible, B. Heppelmann, AD. Craig and RF. Schmidt ....................................... 89 Cell size and Nissl pattern analyses of primary alTerent neurons innervating the molar tooth pulp and cornea of the rat T. Sugimoto, S. Wakisaka, M. Takemura and M. Aoki ...................................................... 95 Visceral and somatic alTerent origin of calcitonin gene-related peptide immunoreactivity in the superficial and deep laminae of the thoracic spinal cord of the rat K.A Sharkey, J.A. Sobrino and F. Cervero .......................................................................... 99 Discussion G. Grant ................................................................................................................................... 103 SECTION II: RECEPTIVE FIELD PROPERTIES OF LAMINA I NEURONS Introduction A.Iggo ........................................................................................................................................ 109 Characterization of lamina I projection neurons: physiology and anatomy J.L.K. Hylden, RL. Nahin, F. Anton and R Dubner ....................................................... 113 Input to and output from lamina I neurones in the cat spinal cord K.-D. Kniffki ............................................................................................................................ 129 The influence of cutaneous inputs on the activity of neurones in the substantia gelatinosa W.M. Steedman. ...................................................................................................................... 145 Superficial dorsal hom neurons in the rat responsive to visceral and cutaneous inputs T.J. Ness and G.F. Gebhart. .................................................................................................. 159 Identification of a sub-population of viscero-somatic neurones unique to the superficial dorsal hom B.M. Lumb and F. Cervero ................................................................................................... 163 Discussion D. Le Bars ................................................................................................................................ 167 SECTION III: SPINAL AND SUPRASPINAL OUTPUTS FROM THE SUPERFICIAL DORSAL HORN Introduction ............................................................................................................................. 179 viii Characterization of long ascending tract projection neurons and non tract neurons in the superficial dorsal horn (SDH) J.A Beal, K.N. Nandi and D.S. Knight ............................................................................... 181 Projections and neurochemical specificity of the different morphological types of marginal cells A. Coimbra and D. Lima ....................................................................................................... 199 Projections of the superficial dorsal horn to the midbrain and thalamus W.D.Willis Jr. .......................................................................................................................... 217 Discussion J. Schouenborg ........................................................................................................................ 239 SECTION IV: DEVELOPMENT AND PLASTICITY IN THE SUPERFICIAL DORSAL HORN Introduction A.I. Basbaum ........................................................................................................................... 247 The significance of plastic changes in lamina 1 systems S.B. McMahon and P.O. Wall ............................................................................................... 249 Molecular events in the spinal cord following sensory stimulation S. Williams, A Pini, G. Evan and S.P. Hunt ...................................................................... 273 Denervation induced changes in somatotopic organization: the ineffective projections of afferent fibres and structural plasticity P.J. Snow and P. Wilson ......................................................................................................... 285 Physiological and pharmacological induction of c-fos protein immunoreactivity in superficial dorsal horn neurones J.D. Leab, T. Herdegen and M. Zimmermann .................................................................. 307 Modality properties and inhibitory receptive fields of dorsal horn neurones in cats with dorsolateral funiculus lesions LM. Pubols, H. Hirata and P.B. Brown .............................................................................. 311 Discussion G.J. Bennett ............................................................................................................................. 317 SECTION V: NEUROTRANSMITTERS AND PEPTIDES IN THE SUPERFICIAL DORSAL HORN Introduction P.M. Headley ........................................................................................................................... 327 ix Glutamate and other putative mediators of fast synaptic action in the superficial dorsal hom E.R. Perl and S.P. Schneider ................................................................................................. 331 Peripheral stimuli releasing neuropeptides in the dorsal hom of the cat A W. Duggan, C.R Morton, LA Hendry and W.D. Hutchison. ..................................... 347 Somatic, articular and visceral noxious-stimulus-evoked expression of c-fos in the spinal cord of the rat: ditTerential patterns of activity and modulation by analgesic agents AI. Basbaum, R Presley, D. Menetrey, S.1. Chi and J.D. Levine .................................. 365 In situ hybridization histochemical and immunocytochemical analysis of opioid gene products in a rat model of peripheral inflammation M.A Ruda, L. Cohen, S. Shiosaka, O. Takahashi, B. Allen, E. Humphrey and M.J. Iadarola .................................................................................................................... 383 In vitro studies on neurones of the superficial dorsal hom in slices of 9- 16 day old rat spinal cord C.A Allerton, P.R Boden and RG. Hill ............................................................................ 395 Opioid and serotonergic etTects on lamina I and deeper dorsal hom neurones P.J. Hope, N. EI-Yassir, S.M. Fleetwood-Walker and R Mitchell ................................. 399 Discussion S.P. Hunt .................................................................................................................................. 403 SECTION VI: SUPERFICIAL DORSAL HORN CHANGES FOLLOWING PERIPHERAL INJURY Introduction P.D. Wall .................................................................................................................................. 407 Opioid receptors in the dorsal hom of intact and deatTerented rats: autoradiographic and electrophysiological studies J.M. Besson, M.C. Lombard, J.M. Zajac, D. Besse, M. Peschanski and B.P. Roques .............................................................................................................................. 415 Neuronal plasticity in the superficial dorsal hom following peripheral tissue inflammation and nerve injury R Dubner, J.L.K. Hylden, RL. Nahin and RJ. Traub .................................................... 429 Afferent induced alterations of receptive field properties C.J. Woolf. ................................................................................................................................ 443 x