The neurobiology of parental behavior

429 Pages·2003·3.168 MB·English

by  Michael Numan, Thomas R Insel

The Neurobiology of
Parental Behavior
Springer
New York
Berlin
Heidelberg
Hong Kong
London
Milan
Paris
Tokyo
Michael Numan Thomas R. Insel
The Neurobiology of
Parental Behavior
With 80 Illustrations
1 3
Michael Numan Thomas R. Insel
Departmentof Psychology Departmentof Psychology
Boston College National Institute of Mental Health
Chestnut Hill, MA 02467 Bethesda, MD 20892
USA USA
[email protected] [email protected]
Series Editors
GregoryF. Ball Jacques Balthazart
Departmentof Psychologicaland Brain University of Lie`ge
Sciences Center for Cellularand Molecular
Johns Hopkins University Neurobiology
Baltimore,MD 21218 BehavioralNeuroendocrinologyResearch
USA Group
[email protected] B-4020 Lie`ge, Belgium
[email protected]
Randy J. Nelson
Departmentsof Psychology &
Neuroscience
Ohio State University
Columbus, OH 43210
USA
[email protected]
LibraryofCongressCataloging-in-PublicationData
Numan,Michael,1946–
Theneurobiologyofparentalbehavior/MichaelNuman,ThomasR.Insel.
p.cm.—(Hormones,brain,andbehaviorseries)
Includesbibliographicalreferencesandindex.
ISBN0-387-00498-X(hbk.:alk.paper)
1. Parentalbehaviorinanimals. 2. Animalbehavior—Endocrineaspects. I. Insel,
ThomasR.,1951– II. Title. III. Series.
QL762.N862003
591.56'3—dc21 2003042473
ISBN0-387-00498-X Printedonacid-freepaper.
(cid:1)2003Springer-VerlagNewYork,Inc.
All rights reserved. This work may not be translated or copied in whole or in part without the
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Series Preface
It is a cliche´ to comment on the explosion of the scientific literature in recent
decades. Most investigators focus on obtaining new data and communicating
thesedatainspecializedjournals. Theintegrationandinterpretationofthisnew
informationhaslaggedbehindthepursuitofexperimentalinvestigations. Novel
studiesareessential,butreviewsarealsoimportantifafieldistoremainhealthy
and advance in productive ways. This is an especially acute problem for inter-
disciplinary fields. Investigators may have specialized knowledge about only
one aspect of a field and fail to appreciate the significanceof theirworkforthe
entire enterprise. The goal of this series is to address this problem forthefield
of behavioral neuroendocrinology.
Books in this series will provide reviews of important and timelytopicscon-
cerning 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 experiencesofvarious
sorts, processed by the central nervoussystem, caninfluenceendocrineactivity.
Thus hormone-behavior relationships are one component of a complex interre-
lation 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 concentra-
tionsintheblood,assesstheneuralsiteofactionofthesehormonesandmeasure
the behavioral consequences of hormonally induced changes in neural activity.
The maturity of this field is reflected by the founding of the SocietyforBehav-
ioral Neuroendocrinology in 1996.
The aims of this series will be to highlight and integrate recent empirical
advances in the field and discuss and analyze methodological challengesfacing
investigators working in this area. The clinical implications of this basic re-
search for problems such as mood disorders, sexual dysfunction, violence and
other behavioral problems will also be considered. Volumeswillincludebooks
focussed on the neuroendocrine regulation of a particular behavior, a summary
of the anatomical localization of hormone sensitive brain networks (e.g., local-
v
vi Series Preface
ization of hormone receptors, metabolizing enzymes, etc.) and a consideration
ofthecellularandmolecularmechanismsmediatinghormoneactioninthebrain.
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 par-
ticular emphasis on behavioral neuroscience, neuroethology and neuroendocri-
nology. Some books in the series will also be useful for upper division
neuroscience and neuroethology courses. It is also hoped that clinical investi-
gatorswillfindthesebooksasusefulsummariesofbasicresearchthatisrelevant
to many health-related questions.
Gregory F. Ball, Baltimore, Maryland
Jacques Balthazart, Lie`ge, Belgium
Randy J. Nelson, Columbus, Ohio
Preface
When we were asked by Greg Ball, Jacques Balthazart, and Randy Nelson if
wecouldprepareavolumeonparentalbehaviorforSpringer’sHormones,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,weultimatelyclearedourdeckstomakeroomforthisprojectbecause
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.
Althoughthereareseveralexcellentreviewchaptersandeditedbooksdealing
with various aspects of the biology of parental behavior, we are not aware of
anyrecentmonographonthisimportanttopic. InTheNeurobiologyofParental
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 im-
portant 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 thefield
of parental behavior, this book also contributes importantly to the growingarea
of emotional and motivational neuroscience. A major part of neuroscience re-
search at the whole organism level has been focused on cognitiveneuroscience,
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
ofbasicmotivationalandemotionalsystemsthatregulatesuchbehaviorsasfood
intake, aggression, reproduction, reward-seeking behaviors, and anxiety-related
behaviors. Our book nicely fits into this latter category.
AsanundergraduatestudentatBrooklynCollege,oneofus(MichaelNuman)
read Lehrman’s outstanding review on the role of hormones in the parental
behaviorofbirdsandmammalsandwascompletelyenthralled(Lehrman,1961).
That one chapter defined the field at that time, and it intelligently indicatedthe
complexity and richness of the research issues that could be studied. Herewas
abehaviorthatwasessentialforthereproductivesuccessofbirdsandmammals,
that was influenced by genes and hormones, but that also had an ontogenetic
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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, butthatitisalso
a worthy descendant of Lehrman’s work, shedding light on some of the impor-
tant 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
understandtheneurobiologyofhumanparentalbehavior. Indeed,ourlastchap-
ter attempts to integrate the nonhuman research data with some human data in
order to make some inroads toward an understanding of postpartumdepression,
childabuse,andchildneglect. Clearly,motivationalandemotionalneuroscience
has close ties to psychiatry, and this will be very evident in the final chapter.
Byunderstandingtheneurobiologyofparentalbehaviorwearealsodelvinginto
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 whilehewasan undergraduate,byHowardMoltz,his
doctoral dissertation advisor, and by Jay Rosenblatt, his postdoctoral research
advisor. In fact, Jay Rosenblatt has remained an important influenceandfriend
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, Mi-
chaelNumandeeplyappreciatestheadvice,support,andencouragementthathe
hasalwaysreceivedfromhiswifeandcolleague,Marilyn. Inaddition,Marilyn
Numanhaspreparedmostofthefiguresinthisbook,andshecriticallyevaluated
and commented upon many of the chapters.
Tom Insel has enjoyed the generosity of anumberofcolleagues,friends,and
mentors including Paul MacLean, Myron Hofer, Michael Kuhar, and Dennis
Murphy. Inaddition,heowesmuchtoagenerationofpostdoctoralfellowswho
haveworkedonneuropeptidesandmaternalbehavior,includingMarianneWam-
boldt, Allan Johnson, Zuoxin Wang, Larry Young, and Darlene Francis. Paul
PlotskyandDavidRubinowkindlycritiquedpartsofthetextandSvetlanaGurv-
itchassistedwithillustrations. Mostofall,DeborahInselhasbeenapatientand
supportivespousewhoenduredtheprolongedlaboranddeliveryofthisvolume.
During the course of writing this book, Michael Numan’s research was sup-
ported in part by National Science Foundation Grant IBN-9728758 and Tom
Insel was supported in part by the Center for Behavioral Neuroscience,anSTC
program of the National Science Foundation, under Agreement No. IBN-
9876754, and by NIMH from RO1-MH-56538 and a NARSAD Distinguished
Investigator Award.
Contents
Series Preface v
Preface vii
1. Introduction 1
2. Hormonal and Nonhormonal Basis of Maternal Behavior 8
3. Experiential Factors Influencing Maternal Behavior 42
4. Motivational Models of the Onset and Maintenance of
Maternal Behavior and Maternal Aggression 69
5. Neuroanatomy of Maternal Behavior 107
6. Neurochemistry and Molecular Biology of Maternal Behavior 190
7. Paternal Behavior 246
8. Neural Basis of Parental Behavior Revisited 268
9. Human Implications 316
Cumulative References 343
Index 409
ix