Developmental Neurobiology of the Autonomic Nervous System

Contemporary Neuroscience Developmental Neurobiology of the Autonomic Nervous System, edited by Phyllis M. Gootman Neurobiology of the Trace Elements, edited by Ivor E. Dreosti and Richard M. Smith

Volume 1: Trace Element Neurobiology and Deficiencies Volume 2: Neurotoxicology and Neuropharmacology

Developmental Neurobiology of the Autonomic Nervous System

Edited by

Phyllis M. Gootman

Springer Science+Business Media, LLC

Library of Congress Cataloglng-In-Publlcatlon Data Main entry under title: Developmental neurobiology of the autonomic nervous system. (Contemporary neuroscience) Includes bibliographies and index. 1. Nervous system. Autonomic-Growth. I. Gootman. Phyllis M.• 1938- . II. Series. [DNLM: 1. Autonomi Nervous System-embryology. 2. Autonomic Nervous System-growth &development. 3. Neurobiology. WL 600 04895) QP368.D48 1986 612'.64018 86-3077 ISBN 978-1-4757-4958-8 ISBN 978-1-59259-459-7 (eBook) DOI 10.1007/978-1-59259-459-7 © 1986 Springer Science+Business Media New York Originally published by The Humana Press Inc. in 1986 Softcover reprint of the hardcover 1st edition 1986 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.

DEDICATION I dedicate this book to my husband, Dr. Norman Gootman, and to my children, Sharon Hillary and Craig Seth, for their understanding and help.

Pre/ace For many years there were few studies concerning the role of the autonomic nervous system in visceral regulation, but examination of abstracts recently published in Federation Proceedings shows the rapid change that has occurred over the past fifteen years. Topics of special interest among the scientists abstracted include not just autonomic function in the adult, but also the maturation of autonomic function. The growing availability of sophisticated electrophysiological, tissue culture, and histochemical techniques has engendered a surge in the amount of experimental information available on autonomic maturation such that a symposium published in 1981 (Ciba Symposium #83, "Development of the Autonomic Nervous System," edited by G. Burnstock, Pittman Medical Ltd., NY, 1981) is already severely dated. Thus, the field is ready for another somewhat more detailed examination of aspects of the recent findings on autonomic nervous system development. This book is intended to bring scientists in related fields up to date on those recent advances. The editor would particularly like to thank Dr. Nancy M. Buckley for her help in preparation of this book. Phyllis M. Gootman

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Introduction This book, covering many key aspects of autonomic nervous system maturation, was suggested by the success of a symposium on the developing autonomic nervous system held at the Spring 1982 meeting of the Federation of American Scientists for Experimental Biology (Federation Proceedings 1983, 42, 1609). It was obvious from the FASEB symposium that there is increasing interest in the developing autonomic nervous system, particularly with respect to its role in regulating visceral function. Some additional topics that were not covered in the FASEB symposium are also included in this book. The editor feels that the readers of this volume are, in all probability, already cognizant of the state of knowledge of the adult autonomic nervous system. Therefore, a review of classical autonomic physiology, pharmacology, and neuroanatomy is not provided. For a recent detailed discussion of the ontogeny and phylogeny of the developing nervous system, I would recommend the book published not long ago by D. Purves and J. W. Lichtman, Principles of Neural Development (Sinauer, Sunderland, MA, 1985). Another recent book, Autonomic Nerve Funtion in the Vertebrates by F. Nilsson (Springer-Verlag, New York, 1984), presents a comparative examination of autonomic nervous system function in vertebrates. For a summary of recent advances in the many aspects of catecholamines as they bear on autonomic nervous system research, I would recommend the series of three books edited by E. Usdin, A. Carlsson, A. Dahlstrom, and J. Engel; Catecholamines, Part A: Basic and Peripheral Mechanisms; Part B: Neuropharmacology and Central Nervous System-Theoretical Aspects; Part C: Neuropharmacology and the Central Nervous System-Therapeutic Aspects (Liss, NY, 1984). It is obvious from the table of contents of our book that there are areas of autonomic function that have not been covered. For example, central transmitters and pathways are not discussed because of very limited information and the fact that most chapters are concerned with the autonomic nervous system, which is, of course, a peripheral nervous system. Nevertheless, the editor feels that the level of information available in this volume, ix

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Introduction

supplied by experts from around the world, will be of considerable interest to the reader. A chapter is included by Dr. Julian Smith on the ontogeny of the autonomic nervous system and its very earliest divergence and differentiation. Since the field of development of parasympathetic function is limited, we are fortunate to have a chapter by Dr. Ezio Giacobini on the development of peripheral parasympathetic neurons and synapses. Doctor Theodore A. Slotkin covers the development of sympathetic-adrenal medullary aspects. Because of the amount of information available with respect to autonomic innervation of the developing myocardium, four chapters have been devoted to various aspects of autonomic regulation of the heart. The chapter by Drs. Margaret L. Kirby and Donald E. Stewart is concerned with the development of autonomic innervation of the avian heart, and Dr. Howard L. Cohen's chapter is concerned primaily with the development of autonomic innervation of the mammalian heart. Doctor Theodore A. Slotkin examines an aspect of sympathetic innervation of the developing heart, i.e., endocrine control of synaptic development. Doctors Robert F. Reder, Gfer Binah, and Peter Danilo, Jr. cover the electrophysiology of the developing myocardium. Development of the autonomic innervation of regional circulations is covered in the chapters by Drs. Nancy M. Buckley, Phyllis M. Gootman, Geoffrey Burnstock, and Tim Cowen, and, to some degree, by Dr. Peter G. Smith. There is one chapter that at first glance might appear to belong in a book on respiratory function. Though control of respiration is a somatic function (Le., skeletal muscles are innervated by alpha-motoneurons), the close interrelationship between circulatory regulation and respiration convinced the editor to include such a chapter. Thus, information concerned with the state of knowledge of development of respiratory regulation is available from Dr. Andrew M. Steele's chapter on development of central respiratory function.

Contributors OFER BINAH • Rappaport Family Institute for Research in the Medical Sciences, Technion-Israel Institute of Technology, Faculty of Medicine, Haifa, Israel NANCY M. BUCKLEY • Department of Physiology and Biophysics, Albert Einstein College of Medicine, New York, New York GEOFFREY BURNSTOCK • Department of Anatomy and Embryology and Centre for Neuroscience, University College London, London, UK HOWARD L. COHEN • Department of Physiology, Downstate Medical Center, Brooklyn, New York TIM COWEN • Department of Anatomy and Embryology and Center for Neuroscience, University College London, London UK PETER DANILO, Jr. • Department of Pharmacology, College of Physicians and Surgeons of Columbia University, New York, New York EZIO GIACOBINI • Department of Pharmacology, Southern Illinois University School of Medicine, Springfield, Illinois PHYLLIS M. GOOTMAN • Department of Physiology, Downstate Medical Center, Brooklyn, New York MARGARET L. KIRBY • Department of Anatomy, Medical College of Georgia, Augusta, Georgia ROBERT F. REDER • Department of Medical Affairs, Knoll Pharmaceutical Company, Whippany, New Jersey THEODORE A. SLOTKIN • Department of Pharmacology, Duke University Medial Center, Durham, North Carolina JULIAN SMITH • Institut d'Embryologie du CNRS et du College de France, Nogent-sur-Marne, France PETER G. SMITH • Department of Pharmacology, Duke University Medical Center, Durham, North Carolina ANDREW M. STEELE • Schneider Children's Hospital of Long Island Jewish Medical Center, New Hyde Park, New York DONALD E. STEWART • Department of Anatomy, Medical College of Georgia, Augusta, Georgia

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Contents

Preface. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. vii Introduction. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. ix

ChaDter 1

ONTOGENY OF THE AUl'ONOMIC NERVOUS SYSTEM: CELL LINE DIVERGENCE AND DIFFERENTIATION Julian Smith 1. Origin of Autonomic Ganglion Cells. . . . . . . . . . . . . . . . . . . . . . . .. 2 2. Cell Line Segregation and Plasticity. . . . . . . . . . . . . . . . . . . . . . . . .. 4 2.1. A Neuronal Precursor Line in the Neural Crest .......... 5 2.2. Segregation of Autonomic and Sensory Cell Lines ....... : 5 2.3. Neuronal Potentialities in a Satellite Cell Precursor Population ............................................ 7 2.4. Plasticity of Chemical Differentiation in Autonomic Ganglia ............................................... 8 3. Establishment of Chemical Diversity in the Autonomic Neuron Population. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 10 3.1. Chemical Differentiation of Neural Crest Cells During Development . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 11 3.2. Environmental Factors Involved in the Chemical Differentiation of Autonomic Neurons In Vivo. . . . . . . . .. 12 3.3. Neural Crest Differentiation Studied in Culture In Vitro ............................................. 15 4. Conclusions.............................................. 18 References ................................................ 20

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DEVELOPMENT OF PERI~HERAL PARASYMPATHETIC NEURONS AND SYNAPSES Ezio Giacobini 1. Introduction.............................................. 2. Early Chemical Differentiation of Autonomic Neurons and Synapses In Vivo ......................................... 2.1. Cholinergic Synapses and Neurons in Sympathetic Ganglia .............................................. 3. Stages of Chemical Differentiation of Autonomic Synapses ... 3.1. Factors Directed Toward Parasympathetic Neurons and Synapses. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4. Synaptogenesis in PNS . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 4.1. Sympathetic Ganglia .................................. 5. Biochemical Development of Neuroeffector Junctions ......... 5.1. Autonomic Ganglia and Their Targets .................. 6. Synaptic Regression: The Final Act of Synaptic Development . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 7. Conclusions .............................................. References. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . ..

29 30 30 40 41 46 47 54 54 57 58 59

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DEVELOPMENT OF TH~SYMPATHOADRENAL AXIS Theodore A. Slotkin 1. Introduction.............................................. 69 2. Maturation of the Chromaffin Cell. . . . . . . . . . . . . . . . . . . . . . . . .. 72 2.1. Ultrastructural and Biochemical Characteristics. . . . . . . . .. 72 2.2. Factors Controlling Chromaffin Cell Development ....... 74 3. Role of Innervation in Onset of Adrenomedullary Function ... 77 3.1. Development of Innervation by the Splanchnic Nerve ... 77 3.2. Adrenomedullary Function Prior to Neurogenic Control. ............................................. 83 4. The Functional Significance of Adrenomedullary Catecholamine Release in the Fetus and Neonate ............ 85 5. Conclusions .............................................. 89 References ................................................ 91

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ENDOCRINE CONTROL (SF SYNAPTIC DEVELOPMENT IN THE SYMPATHETIC NERVOUS SYSTEM: THE CARDIAC-SYMPATHETIC AXIS Theodore A. Slotkin 1. Introduction .............................................. 97 2. Development of Synaptic Function in the Cardiac-Sympathetic Axis ................................. 98 2.1. Development of Noradrenergic Receptors and Responses in the Myocardium ........................ 100 2.2. Development of Postganglionic Synaptic Transmission ....................................... 100 2.3. Development of Ganglionic Synaptic Transmission ....................................... 104 2.4. Development of Baroreceptor Regulation of Sympathetic Tone ................................... 105 3. Role of Thyroid Hormones in Development of Sympathetic Function . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 107 3.1. Hyperthyroidism.................................... 108 3.2. Hypothyroidism .................................... 119 4. Role of Glucocorticoids in Development of Sympathetic Function . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 124 5. Conclusions............................................. 127 References. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 128

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DEVELOPMENT OF ANS fNNERVATION TO THE AVIAN HEART Margaret L. Kirby and Donald E. Stewart 1. Introduction............................................. 135 2. Autonomic Innervation of the Adult Avian Heart ........... 136 3. Preganglionic Autonomic Neurons ........................ 137 3.1. Parasympathetic .................................... 137 3.2. Sympathetic ........................................ 138

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4. Postganglionic Autonomic Neurons ........................ 4.1. Neural Crest. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 4.2. Cardiac Ganglia ..................................... 4.3. Sympathetic Trunks ................................. 4.4. Catecholamines in the Developing Heart .............. 5. Receptor Development ................................... 5.1. Muscarinic Receptors ................................ 5.2. I3-Adrenergic Receptors .............................. 6. Lesions of Autonomic Innervation to the Heart ............. 6.1. Surgical Lesions ..................................... 6.2. Chemical Lesions ................................... 7. Conclusions............................................. References ...............................................

139 139 140 141 145 148 148 150 151 151 153 153 154

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DEVELOPMENT OF AUCfoNOMIC INNERVATION IN MAMMALIAN MYOCARDIUM Howard L. Cohen 1. 2. 3. 4. 5. 6. 7. 8. 9. 10. 11. 12. 13. 14. 15. 16. 17. 18.

Introduction............................................. Sympathetic Innervation of the Myocardium ............... General Criteria for Functional Synapses ................... Development of Sympathetic Neurons. . . . . . . . . . . . . . . . . . . .. Nerve Growth Factor. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. Norepinephrine.......................................... Norepinephrine Uptake Mechanisms ...................... Synaptic Vesicles ......................................... Neonatal Sympathetic Dominance ......................... Presynaptic Influences on Myocardial Development. . . . . . . .. Parasympathetic Innervation of the Myocardium ............ Acetylcholine ............................................ Acetylcholinesterase ...................................... Sympathetic-Parasympathetic Interactions .................. Myocardial Beta Adrenoceptors ........................... AC-cAMP............................................... Myocardial a-Adrenoceptors .............................. Myocardial Cholinergic Receptors ......................... References. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . ..

159 160 162 162 164 164 165 167 168 168 170 173 174 177 178 180 181 182 182

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AUTONOMIC EFFECTS ~ THE DEVELOPING HEART Robert F. Reder, Ofer Binah, and Peter Danilo, Jr. 1. Introduction ............................................. 2. Transmembrane Action Potential Characteristics of Embryonic Hearts. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 3. Developmental Changes in Ionic Currents-Embryonic and Fetal Hearts ............................................. 4. Neonatal Hearts ......................................... 5. Effects of Autonomic Nervous System Agonists and Antagonists .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 6. Effects of Sympathetic Agonists and Antagonists .... . . . . . . . 7. Effects of Parasympathetic Agonists and Antagonists ........ 8. Conclusions ............................................. References ...............................................

193 194 195 199 201 202 206 207 208

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DEVELOPMENT, AGING, AND PLASTICITY OF PERIVASCULAR AUTONOMIC NERVES Tim Cowen and Geoffrey Burnstock 1. 2. 3. 4. 5. 6.

Introduction............................................. Perinatal Development . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. Postnatal Development ................................... Old Age ................................................. Plasticity ................................................ Conclusions............................................. References. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . ..

211 212 216 221 224 225 226

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REGULATION OF REGIO~AL VASCULAR BEDS BY THE DEVELOPING AUTONOMIC NERVOUS SYSTEM Nancy M. Buckley 1. Introduction............................................. 233 2. Innervation of Blood Vessels .............................. 234

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3. Responses of Isolated Blood Vessels to Autonomic Neurotransmitters ........................................ 4. Responses of Regional Circulations to Autonomic Stimuli. . .. 4.1. Exogenous Administration of Neurotransmitters ....... 4.2. Direct Stimulation of the Efferent Nerve Supply ....... 4.3. Reflex Stimulation (Baroreceptor and Chemoreceptor) .. 5. Conclusions ............................................. References ...............................................

236 237 237 240 244 246 247

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RELATIONSHIPS BEtwEEN THE SYMPATHETIC NERVOUS SYSTEM AND FUNCTIONAL DEVELOPMENT OF SMOOTH MUSCLE END ORGANS Peter G. Smith 1. Introduction ............................................. 2. Ontogeny of SNS Control of End Organ Activity in Sprague-Dawley Rats. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 3. Ontogeny of Nonvascular Smooth Muscle Activity in Sprague-Dawley Rats. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 3.1. Normal Development. ............................... 3.2. Effects of Disturbances in Sympathetic Innervation ..... 4. Ontogeny of Nonvascular Smooth Muscle Function in SHR and WKY ............................................... 5. Ontogeny of Vascular Smooth Muscle Function ............. 5.1. Neurogenic Control of Vascular Smooth Muscle Function in Sprague-Dawley Rats ..................... 5.2. Neurogenic Control of Vascular Smooth Muscle Function in SHR and WKY ........................... 5.3. Postnatal Maternal Stress ............................ 6. Conclusions ............................................. References ...............................................

251 253 256 256 260 262 264 265 267 270 274 275

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DEVELOPMENT O~-CENTRAL AUTONOMIC REGULATION OF CARDIOVASCULAR FUNCTION Phyllis M. Gootman 1. Introduction ............................................. 279 1.1. General Methodology. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 281

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Contents 2. Results and Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.1. Effects of Stress on Cardiovascular Function. . . . . . . . . . . 2.2. Effects of Afferent Stimulation on Cardiovascular Function ........................................... 2.3. Cardiovascular Responses to Alterations in Afferent Discharge From the Upper Gastrointestinal Tract ....... 2.4. Age-Related Responses of Isolated Blood Vessels ...... 2.5. Cardiovascular Responses to Stimulation of Vasoactive Sites in the Central Nervous System .................. 2.6. Location of Vagal Cardiac Motor Neurons ............. 2.7. Spontaneous Efferent Sympathetic Discharge .......... 3. Conclusions ............................................. References ...............................................

282 282 286 296 299 300 310 314 318 318

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DEVELOPMENTALCH~GESINNEURALCONTROL OF RESPIRATION Andrew M. Steele

1. Introduction............................................. 327 2. Generation of the Respiratory Rhythm. . . . . . . . . . . . . . . . . . . .. 330 2.1. Anatomic and Functional Organization of Respiratory Neurons ............................................ 334 2.2. Neural Mechanisms ................................. 337 3. Maturation-Related Characteristics of the Respiratory Pattern. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 342 3.1. Apnea .............................................. 343 3.2. Behavioral State ..................................... 349 4. Afferent Inputs to the RRG ............................... 353 4.1. Pulmonary Afferents ................................ 354 4.2. The Larynx ......................................... 364 4.3. Chest Wall Afferents ................................ 368 4.4. Chemical Drive to the RRG .......................... 370 5. Conclusions ............................................. 378 References ..................... '.' ........................ 379 Appendix: List of Abbreviations. . . . . . . . . . . . . . . . . . . . . . . . . .. 403 Index ................................................... 409