Neurobiology of Social Behavior: Toward an Understanding of the Prosocial and Antisocial Brain

346 Pages·2014·4.81 MB·English

by  Michael Numan

NEUROBIOLOGY
OF SOCIAL
BEHAVIOR
TOWARD AN UNDERSTANDING
OF THE PROSOCIAL AND
ANTISOCIAL BRAIN
M N
ichael uMaN
AMSTERDAM • BOSTON • HEIDELBERG • LONDON
NEW YORK • OXFORD • PARIS • SAN DIEGO
SAN FRANCISCO • SINGAPORE • SYDNEY • TOKYO

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Dedicated to my wife, Marilyn, and in memory of Jay Rosenblatt
Preface
In writing this book on the Neurobiology of regulating normal aspects of the behavior is
Social Behavior, my goal was to present a broad presented, and this is then followed by an
and comprehensive review of the neural basis of examination of how dysfunctions within these
mammalian social behaviors, both prosocial and neural systems can give rise to abnormal social
antisocial. This book is meant to be accessible behavior. The role of genes, gene–environment
and important for scholars and researchers who interactions, and/or epigenetics in the devel-
study the neurobiology of social behavior from opment of social behaviors is also discussed in
different levels of analysis. Therefore, the book most chapters. In integrating animal and human
has much to offer for molecular and developmen- studies, an overarching principle is that there
tal neurobiologists, behavioral neuroscientists, are core allocortical and subcortical circuits that
and social-affective-cognitive neuroscientists, influence social behavior across mammalian
and it is suitable for both graduate students and species. Research on the neural basis of social
advanced researchers. Since the neural basis of behavior in animals is shown to provide basic
social behavior pathologies is discussed in most and important information about the neurobiol-
chapters, the book will also be valuable for clini- ogy of social behavior in humans.
cians. Although most neuroscientists have par- I am a behavioral neuroscientist, and my
ticular areas of expertise, an underlying premise own research program examines the neural and
of this book is that the integration of genetic, neurochemical systems that regulate maternal
developmental, neural circuit, and functional behavior in rodents. As a result of an invitation
magnetic resonance imaging (fMRI) research in by Stephanie Brown, in 2012 I wrote a chapter
the analysis of social behaviors promotes a more entitled “Neural circuits regulating maternal
complete understanding of the neural underpin- behavior: Implications for understanding the
nings of such behaviors in animals and humans. neural basis of social cooperation and competi-
The book begins with chapters on functional tion” (see reference [698] in the References sec-
neuroanatomy and molecular genetics and epi- tion of this book for the full citation). Writing
genetics. Chapters on aggression, sexual behav- this chapter and interacting with Stephanie and
iors and sexual differentiation, parental behavior, other colleagues at a symposium at the Uni-
monogamy, and human sociality follow these versity of Michigan made me think about the
introductory chapters. All chapters integrate broader implications of my research; this experi-
animal and human studies, but the final chapter ence was one of the driving forces that led me
deals with highly developed human social char- to write this current book on the neurobiology
acteristics, such as empathy, trust, cooperation, of social behavior. Indeed, one of the themes
and altruism. within the Neurobiology of Social Behavior is that
In each chapter on particular social behav- the neural circuits underlying mother–infant
iors, a detailed analysis of the neural systems bonding may have provided the primordial
ix
x
PREFACE
neural scaffold upon which other types of strong and developmental processes affect the neu-
prosocial bonds are built. ral circuits that control social behavior. These
Another theme that runs through this book interests flourished during my postdoctoral
is that there are distinct prosocial and antisocial research with Jay Rosenblatt at the Institute of
neural circuits, and that social stimuli can be Animal Behavior at Rutgers University. During
routed over one or the other circuit, leading to my independent academic career at Boston Col-
either prosocial or antisocial actions and feeling lege, the National Institutes of Health and the
states. Importantly, just in which circuit a social National Science Foundation provided support
stimulus is processed through can be influenced for my research program, and special thanks are
by several factors that include evolutionary due to Kathie Olsen. The way I think about how
forces and genetics, early life experiences, adult the brain works to regulate behavior has been
experiences and cognitive factors, and physi- strongly influenced by the research and schol-
ological state. arship of Donald Pfaff and Larry Swanson. So
When comparing a neural circuitry analysis many other scientists have greatly impacted
derived from animal research with fMRI data my thinking, and this is amply demonstrated
derived from human research, although both by the detailed analysis and discussion of their
sets of data may point to a certain brain region research findings in this book. My students
as being important for a particular aspect of have also been a tremendous source of support
social behavior, the animal research can offer for me, and they have provided independent
additional information about the neurochemical insights that strongly influenced the direction of
microcircuitry within a particular brain region our research program. In particular, my former
of interest that fMRI and other imaging data are graduate students, Teige Sheehan and Danielle
not yet able to provide. Throughout this book, Stolzenberg, created great research under my
I make the point that by understanding such mentorship.
microcircuitry, one gains a fuller appreciation of My wife and colleague, Marilyn, has been the
how social stimuli can be processed over either most important source of intellectual and social
prosocial or antisocial circuits, and how such support throughout my career. In addition, Mar-
processing can be modulated by a variety of ilyn read, edited, and commented on each chap-
factors. ter in this book and she also prepared all of the
I have been inspired, encouraged, and sup- original figures. This book would not be as good
ported by many mentors, colleagues, and as it is without her important input and efforts.
students throughout my career. During my Finally, the staff at Elsevier produced what I
doctoral graduate studies at the University of think is a beautiful book, and they supported me
Chicago, Howard Moltz, Eckhard Hess, and each step of the way during the long process of
Pete Grossman initiated my interests in under- writing and organizing the Neurobiology of Social
standing how evolutionary forces, genetics, Behavior.
About the Author
Michael Numan received his PhD from the a Professor of Psychology and Behavioral Neu-
University of Chicago. He is a Fellow of the roscience at Boston College. He is the author of a
American Association for the Advancement of previous book, with Thomas Insel, The Neurobi-
Science (AAAS) and the Association for Psycho- ology of Parental Behavior. He lives with his wife,
logical Science (APS). Most of his research, which Marilyn, in the Santa Fe-Albuquerque region of
focuses on the neural mechanisms r egulating New Mexico.
maternal behavior, was conducted while he was
xi
C H A P T E R
1
An Introduction to Neural Systems
1.1 INTRODUCTION behaviors, acceptance, caregiving, and other
prosocial behaviors, while negative social
The purpose of this book is to provide a stimuli activate neural pathways that cause
comprehensive understanding of the neurobi- avoidance, rejection, competition, or even
ology of social behavior in mammals, includ- attack (antisocial behaviors). In other words,
ing humans. Social behavior, broadly defined, it may be valuable to view social behaviors
comprises those behaviors that are exhibited as being influenced by two elementary neu-
by conspecifics as they interact and includes ral networks: social stimuli can be processed
both affiliative (prosocial) and antagonistic by either an aversion/rejection network or an
(antisocial) interactions. The social behaviors attraction/acceptance network, with such dif-
and processes that will be examined include ferential neural processing leading to different
aggression and competition, sexual behaviors, social outcomes [698]. Further, social stimuli
parental behaviors, the formation of social may be automatically (innately) routed over
attachments, cooperation, and altruism. Each of either attraction or aversion networks, or such
these social behaviors will be analyzed across valence properties may be acquired through
the different levels of investigation that have learning mechanisms. These core neural pro-
been used to study the behavior, from molecu- cesses may then set the foundation for more
lar neurobiology to neural circuits to functional complex social interactions. But what are the
magnetic resonance imaging (fMRI) data. The neural systems that regulate core approach and
first two chapters of the book provide the nec- avoidance processes, processes that are embed-
essary background in functional neuroanatomy ded within and influence more complex social
(Chapter 1) and molecular biology and genetics interactions? In what follows, an overview will
(Chapter 2) that will serve as a foundation for a be presented of functional neuroanatomy with
full appreciation of the neurobiology of social an aim to explain such approach and avoid-
behavior that will be presented in the subse- ance systems in mammals. Animals approach
quent chapters. or avoid a broad range of stimuli, not just social
One important aspect of this book is to stimuli. Research findings will be presented
uncover the neural mechanisms that deter- from both social and nonsocial contexts with
mine whether social stimuli are assigned either the understanding, which will be borne out in
a positive or a negative valence by the per- subsequent chapters, that there is overlap in
ceiver, with positive social stimuli activating the neural systems influencing social and non-
neural pathways that cause contact seeking social motivational processes (see [82]).
Neurobiology of Social Behavior
1
http://dx.doi.org/10.1016/B978-0-12-416040-8.00001-8 © 2015 Elsevier Inc. All rights reserved.
2
1. AN INTRODUCTION TO NEURAL SYSTEMS
1.2 A SCHEMATIC OVERVIEW OF less than six well-differentiated layers [951].
THE MAMMALIAN BRAIN Isocortex makes up most of the occipital, pari-
etal, temporal, and lateral prefrontal parts of
Based on the neuroanatomy in Swanson the cortex. Examples of allocortex include the
[951], Figure 1.1 depicts the general organi- olfactory (piriform) cortex, parts of the amyg-
zation of the mammalian brain. Moving from dala, the hippocampal formation, and parts of
rostral to caudal, the brain is broken down into the medial and orbital prefrontal cortex. Some
two great divisions: the cerebral hemispheres important subcortical cerebral nuclei include
(telencephalon) and the brainstem. Caudal to the caudate nucleus (dorsal striatum), nucleus
the brainstem lies the spinal cord. The cerebral accumbens (ventral striatum), globus pallidus
hemispheres are divided into the cerebral cor- (dorsal pallidum), ventral pallidum, septal
tex and the underlying, and therefore subcor- area, and some nuclei within the amygdala.
tical, cerebral nuclei. The cerebral cortex can The brainstem, upon which sits the cerebral
be divided into isocortex (neocortex) and allo- hemispheres, is composed of the thalamus and
cortex, with the former containing six well- hypothalamus (diencephalon), and the lower
defined cellular layers, while the latter contains brainstem, which includes the midbrain, pons,
FIGURE 1.1 A schematic overview of the
mammalian brain. The telencephalon (cerebral
Cerebral
hemispheres) is composed of outer cortical cortex
layers and underlying cerebral nuclei. Caudal
to the telencephalon is the brainstem, contain-
ing the diencephalon, midbrain, pons, cerebel- Cerebral nuclei
lum, and medulla. The spinal cord lies caudal
to the medulla. Each section of the brainstem
Telencephalon
lists certain structures that are emphasized in
this book. This listing is not meant to represent
the exact anatomical location of the labeled Thalamus
structures but simply indicates their general Hypothalamus
location. For example, within the diencepha-
lon, the thalamus is dorsal, not anterior, to the
hypothalamus. Abbreviations: CB = cerebel- PAG
lum; DR = dorsal raphe nucleus; MR = median Diencephalon VTA/SN
raphe nucleus; MRF = medullary reticular for- Midbrain
DR
mation; PAG = periaqueductal gray; SN = sub-
MR
stantia nigra; VTA = ventral tegmental area.
CB CB
Pons
MRF Medulla
Spinal cord
1.3 FuNCTIoNAl NEuRoANATomy 3
cerebellum, and medulla. Some of the lower Lateral Medial Lateral
brainstem nuclei that will be shown to play
important roles in social behavior are the mid-
brain periaqueductal gray (PAG), dopamine
neurons within the ventral tegmental area of
the midbrain, and the serotonin neurons of Rostral
LPOA MPOA MPOA LPOA
the raphe nuclei located in the midbrain and
pons. The term brainstem motor area (BSMA) Z Z
V V
will be used to refer to a group of nuclei in P P
the lower brainstem with indirect and direct
connections to cranial and spinal motor neu- LH AHN AHN LH
rons. Most relevant with respect to the BSMA,
the PAG and the midbrain locomotor region
PVN PVN
(located lateral to the PAG) both project to the
medullary reticular formation, whose axons
project to cranial and spinal motor neurons VMN VMN
[361,420,1069]. As will become important, LH LH
the descending projection of the midbrain
PAG to the medullary reticular formation is
PH PH
an important route through which PAG out-
Caudal
put affects the display of reflex-like defensive Z Z
V V
P P
and aggressive responses, such as behav-
ioral immobility, escape responses, or biting,
and reflexive responses related to sexual and
parental behaviors.
3rd
ventricle
1.3 FUNCTIONAL FIGURE 1.2 Horizontal section through the hypo-
NEUROANATOMY thalamus. The third ventricle is shown as a thick black line
down the midline. Moving from medial to lateral, the hypo-
thalamus contains a periventricular zone (PVZ), a medial
1.3.1 The Hypothalamus
zone, and a lateral zone. Other abbreviations: AHN = ante-
rior hypothalamic nucleus; LH = lateral hypothalamus;
1.3.1.1 Introduction
LPOA = lateral preoptic area; MPOA = medial preoptic
The three major functions of the hypothala- area; PH = posterior hypothalamus; PVN = paraventricular
nucleus; VMN = ventromedial nucleus.
mus are its regulatory influences over the auto-
nomic nervous system and the pituitary gland,
and its involvement in the control of a variety
of motivated behaviors, including social behav- zone. The periventricular zone contains those
iors [716,813,950]. Figure 1.2 shows a horizontal neurons primarily involved in neuroendocrine
section through the hypothalamus, display- and autonomic regulation, while it is the nuclei
ing its rostral-to-caudal and medial-to-lateral of the medial and lateral zones that play domi-
organization. With respect to its organization nant roles in the control of motivated behav-
from medial to lateral, the hypothalamus con- iors, which involve influences over the somatic
tains a periventricular zone (which surrounds motor mechanisms that control both the reflex-
the third ventricle) and a medial and lateral ive and voluntary aspects of these behaviors.
4
1. AN INTRODUCTION TO NEURAL SYSTEMS
The social behaviors influenced by the hypo- behavioral change. As examples, food depriva-
thalamus include reproductive behaviors (sex- tion increases an organism’s responsiveness to
ual and parental) and aggressive and defensive food-related cues, the hormonal events asso-
behaviors. As will be seen, it is likely that sepa- ciated with pregnancy termination increase a
rate and distinct neuronal populations within female’s responsiveness to infant stimuli, and
the hypothalamus regulate different social gonadal steroids influence the occurrence of
behaviors. male and female sexual responses to sexual
Given the involvement of the hypothala- stimuli. Another definition of motivation refers
mus in social and other motivated behaviors, to those internal processes that arouse and direct
one would expect that it would be a recipient behavior toward a particular goal, giving rise to
of significant sensory inputs, and indeed this is the term goal-directed behavior. Two major types of
the case [759,813]. The hypothalamus receives goal-directed responses are approach responses
olfactory inputs from the amygdala and other (also called appetitive or reward-seeking
olfactory areas. Afferents from the brainstem responses) toward a desired or pleasant stimu-
carry tactile and pain inputs, and the hypothal- lus, and avoidance or rejection responses toward
amus receives multimodal sensory inputs from aversive or noxious stimuli [868]. As will be
the prefrontal cortex and from the hippocam- described below, rejection responses can include
pus, the latter arriving either directly or indi- approaching an aversive/unpleasant stimulus
rectly via the septal area. Finally, an organism’s in order to attack it. The mechanisms underpin-
internal state importantly influences its social ning such responses would define appetitive
behavior, and primary among these internal motivation and aversive motivation. Therefore,
factors are hormones. Neurons in the hypothal- I am broadening the typical view of aversion to
amus contain receptors for prolactin, estradiol, mean more than avoidance or withdrawal. An
testosterone, progesterone, and adrenal corti- aversive stimulus is one that an organism does
costeroids [813,950]. A simple view is that hor- not like, and goal-directed responses can either
mones and other internal physiological stimuli avoid/escape from that stimulus or approach
bias how various sensory inputs are processed the stimulus to actively reject it.
by the hypothalamus, which in turn affects the In describing motivated behavior with
hypothalamic efferent pathways that are acti- respect to a desired or rewarding stimulus (one
vated. With respect to social behavior, such with a positive valence), such behavior can be
effects would allow an organism to respond in separated into an appetitive goal-directed phase
one way or another to particular social stimuli, and a consummatory or terminal phase. Dur-
depending on the current hormonal milieu ing the appetitive or reward-seeking phase, the
that is affecting the operation of specific neural organism searches its environment to acquire
circuits. the particular goal object. For example, a hungry
animal will search for food, a sexually motivated
1.3.1.2 Motivation: Appetitive, Avoidance/
organism will search for a mate, and a maternal
Rejection, and Consummatory Behaviors
female will seek out her infants or will search
Several definitions of motivation exist for displaced infants in order to transport them
[90,716,764,1021]. In its simplest definition, to a secure area. The consummatory phase is
motivation is an internal process that modi- composed of those behaviors that occur once the
fies an organism’s responsiveness to a constant desired goal is obtained, and the behaviors that
stimulus. That is, if an organism shows a change occur during this phase are elicited by proximal
in the way it responds to a constant stimulus, cues from the goal object. Examples of consum-
some internal alteration must be mediating the matory responses toward a desired stimulus