The Neurobiology of Parental Behavior
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1 The Neurobiology of Parental Behavior
2 Springer New York Berlin Heidelberg Hong Kong London Milan Paris Tokyo
3 Michael Numan Thomas R. Insel The Neurobiology of Parental Behavior With 80 Illustrations 1 3
4 Michael Numan Department of Psychology Boston College Chestnut Hill, MA USA Thomas R. Insel Department of Psychology National Institute of Mental Health Bethesda, MD USA Series Editors Gregory F. Ball Department of Psychological and Brain Sciences Johns Hopkins University Baltimore, MD USA Randy J. Nelson Departments of Psychology & Neuroscience Ohio State University Columbus, OH USA Jacques Balthazart University of Liège Center for Cellular and Molecular Neurobiology Behavioral Neuroendocrinology Research Group B-4020 Liège, Belgium Library of Congress Cataloging-in-Publication Data Numan, Michael, 1946 The neurobiology of parental behavior / Michael Numan, Thomas R. Insel. p. cm. (Hormones, brain, and behavior series) Includes bibliographical references and index. ISBN X (hbk. : alk. paper) 1. Parental behavior in animals. 2. Animal behavior Endocrine aspects. I. Insel, Thomas R., 1951 II. Title. III. Series. QL762.N '3 dc ISBN X Printed on acid-free paper Springer-Verlag New York, Inc. All rights reserved. This work may not be translated or copied in whole or in part without the written permission of the publisher (Springer-Verlag New York, Inc., 175 Fifth Avenue, New York, NY 10010, USA), except for brief excerpts in connection with reviews or scholarly analysis. Use in connection with any form of information storage and retrieval, electronic adaptaion, computer software, or by similar or dissimilar methodology now known or hereafter developed is forbidden. The use in this publication of trade names, trademarks, service marks, and similar terms, even if they are not identified as such, is not to be taken as an expression of opinion as to whether or not they are subject to proprietary rights. Printed in the United States of America SPIN Springer-Verlag New York Berlin Heidelberg A member of BertelsmannSpringer Science Business Media GmbH
5 Series Preface It is a cliché to comment on the explosion of the scientific literature in recent decades. Most investigators focus on obtaining new data and communicating these data in specialized journals. The integration and interpretation of this new information has lagged behind the pursuit of experimental investigations. Novel studies are essential, but reviews are also important if a field is to remain healthy and advance in productive ways. This is an especially acute problem for interdisciplinary fields. Investigators may have specialized knowledge about only one aspect of a field and fail to appreciate the significance of their work for the entire enterprise. The goal of this series is to address this problem for the field of behavioral neuroendocrinology. Books in this series will provide reviews of important and timely topics concerning how hormones influence brain functions, especially behavior. It has been known for many years that hormones have profound effects on behavior. However, it is also the case that behavioral and physical experiences of various sorts, processed by the central nervous system, can influence endocrine activity. Thus hormone-behavior relationships are one component of a complex interrelation among hormones, brain and behavior. Scientists interested in this field are drawn from diverse disciplines in the biological and behavioral sciences including endocrinology, neuroscience, anatomy, psychology, and ethology. In recent years a new generation of truly interdisciplinary studies has emerged in which investigators simultaneously manipulate circulating hormone concentrations in the blood, assess the neural site of action of these hormones and measure the behavioral consequences of hormonally induced changes in neural activity. The maturity of this field is reflected by the founding of the Society for Behavioral Neuroendocrinology in The aims of this series will be to highlight and integrate recent empirical advances in the field and discuss and analyze methodological challenges facing investigators working in this area. The clinical implications of this basic research for problems such as mood disorders, sexual dysfunction, violence and other behavioral problems will also be considered. Volumes will include books focussed on the neuroendocrine regulation of a particular behavior, a summary of the anatomical localization of hormone sensitive brain networks (e.g., local- v
6 vi Series Preface ization of hormone receptors, metabolizing enzymes, etc.) and a consideration of the cellular and molecular mechanisms mediating hormone action in the brain. This series is planned to produce two to four volumes a year. The books will be aimed at advanced graduate students as well as established investigators working in the fields of neuroscience, physiology and psychology with a particular emphasis on behavioral neuroscience, neuroethology and neuroendocrinology. Some books in the series will also be useful for upper division neuroscience and neuroethology courses. It is also hoped that clinical investigators will find these books as useful summaries of basic research that is relevant to many health-related questions. Gregory F. Ball, Baltimore, Maryland Jacques Balthazart, Liège, Belgium Randy J. Nelson, Columbus, Ohio
7 Preface When we were asked by Greg Ball, Jacques Balthazart, and Randy Nelson if we could prepare a volume on parental behavior for Springer s Hormones, Brain, and Behavior book series, our initial response was one of trepidation because we knew the level of work and commitment such an endeavor would involve. However, we ultimately cleared our decks to make room for this project because we thought that the time was right for such a book, and we knew that if we developed it properly it would make an important scientific contribution. Although there are several excellent review chapters and edited books dealing with various aspects of the biology of parental behavior, we are not aware of any recent monograph on this important topic. In The Neurobiology of Parental Behavior we take an integrative and multilayered approach to the study of the biology of parental behavior. The research that we review, which includes an analysis of the role of developmental factors, experiential factors, hormones, genes, neurotransmitters/neuromodulators, and neural circuits in the control of parental behavior, is all aimed at defining the neural underpinnings of this important behavior. Therefore, diverse sources of data are integrated in a unified way with a common goal in mind. In addition to filling a need within the field of parental behavior, this book also contributes importantly to the growing area of emotional and motivational neuroscience. A major part of neuroscience research at the whole organism level has been focused on cognitive neuroscience, with an emphasis on the neurobiology of learning and memory, but there has been a recent upsurge in research that is attempting to define the neural basis of basic motivational and emotional systems that regulate such behaviors as food intake, aggression, reproduction, reward-seeking behaviors, and anxiety-related behaviors. Our book nicely fits into this latter category. As an undergraduate student at Brooklyn College, one of us (Michael Numan) read Lehrman s outstanding review on the role of hormones in the parental behavior of birds and mammals and was completely enthralled (Lehrman, 1961). That one chapter defined the field at that time, and it intelligently indicated the complexity and richness of the research issues that could be studied. Here was a behavior that was essential for the reproductive success of birds and mammals, that was influenced by genes and hormones, but that also had an ontogenetic vii
8 viii Preface course that allowed for the influence of experiential factors. After reading that chapter, one could become preoccupied with the question of how experience and/or hormones might modify the brain so that an organism s responsiveness to infant-related stimuli could change. We hope that the present book not only clearly reviews and integrates the large body of work that has appeared on the biology of parental behavior since Lehrman wrote his chapter, but that it is also a worthy descendant of Lehrman s work, shedding light on some of the important issues that he raised. In this book we emphasize research findings obtained from rodents, sheep, and primates. Our goal, of course, is to provide a foundation that may help us understand the neurobiology of human parental behavior. Indeed, our last chapter attempts to integrate the nonhuman research data with some human data in order to make some inroads toward an understanding of postpartum depression, child abuse, and child neglect. Clearly, motivational and emotional neuroscience has close ties to psychiatry, and this will be very evident in the final chapter. By understanding the neurobiology of parental behavior we are also delving into neurobiological factors that may have an impact on core human characteristics involved in sociality, social attachment, nurturing behavior, and love. In this very violent world, it is hard to conceive of a group of characteristics that is more worthy of study. In preparing this book, each of us owes a debt of gratitude to our former teachers and colleagues. Michael Numan was strongly influenced by David Raab and Barton Meyers while he was an undergraduate, by Howard Moltz, his doctoral dissertation advisor, and by Jay Rosenblatt, his postdoctoral research advisor. In fact, Jay Rosenblatt has remained an important influence and friend for almost 30 years. Don Pfaff, by inviting Michael Numan to write a major review chapter on maternal behavior (Numan, 1988, 1994), helped him hone those integrative skills needed to write this current contribution. Finally, Michael Numan deeply appreciates the advice, support, and encouragement that he has always received from his wife and colleague, Marilyn. In addition, Marilyn Numan has prepared most of the figures in this book, and she critically evaluated and commented upon many of the chapters. Tom Insel has enjoyed the generosity of a number of colleagues, friends, and mentors including Paul MacLean, Myron Hofer, Michael Kuhar, and Dennis Murphy. In addition, he owes much to a generation of postdoctoral fellows who have worked on neuropeptides and maternal behavior, including Marianne Wamboldt, Allan Johnson, Zuoxin Wang, Larry Young, and Darlene Francis. Paul Plotsky and David Rubinow kindly critiqued parts of the text and Svetlana Gurvitch assisted with illustrations. Most of all, Deborah Insel has been a patient and supportive spouse who endured the prolonged labor and delivery of this volume. During the course of writing this book, Michael Numan s research was supported in part by National Science Foundation Grant IBN and Tom Insel was supported in part by the Center for Behavioral Neuroscience, an STC program of the National Science Foundation, under Agreement No. IBN , and by NIMH from RO1-MH and a NARSAD Distinguished Investigator Award.
9 Contents Series Preface Preface v vii 1. Introduction 1 2. Hormonal and Nonhormonal Basis of Maternal Behavior 8 3. Experiential Factors Influencing Maternal Behavior Motivational Models of the Onset and Maintenance of Maternal Behavior and Maternal Aggression Neuroanatomy of Maternal Behavior Neurochemistry and Molecular Biology of Maternal Behavior Paternal Behavior Neural Basis of Parental Behavior Revisited Human Implications 316 Cumulative References 343 Index 409 ix
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