Neurobiology of Social Behavior

Toward an Understanding of the Prosocial and Antisocial Brain

Michael Numan

• Publisher: Academic Press
• Year: 2014
• ISBN:
  9780123914750
• Topic: Psychology
• Subtopic: Neuropsychology
• Index: Psychology

Social neuroscience is a rapidly growing, interdisciplinary field which is devoted to understanding how social behavior is regulated by the brain, and how such behaviors in turn influence brain and biology. Existing volumes either fail to take a neurobiological approach or focus on one particular type of behavior, so the field is ripe for a comprehensive reference which draws cross-behavioral conclusions. This authored work will serve as the market's most comprehensive reference on the neurobiology of social behavior.

The volume will offer an introduction to neural systems and genetics/epigenetics, followed by detailed study of a wide range of behaviors – aggression, sex and sexual differentiation, mating, parenting, social attachments, monogamy, empathy, cooperation, and altruism. Research findings on the neural basis of social behavior will be integrated across different levels of analysis, from molecular neurobiology to neural systems/behavioral neuroscience to fMRI imaging data on human social behavior. Chapters will cover research on both normal and abnormal behaviors, as well as developmental aspects.

• 2016 PROSE Category winner - Honorable Mention for Biomedicine and Neuroscience
• Presents neurobiological analysis of the full spectrum of social behaviors, while other volumes focus on one particular behavior
• Integrates and discusses research from different levels of analysis, including molecular/genetic, neural circuits and systems, and fMRI imaging research
• Covers both normal and abnormal behaviors
• Covers aggression, sex and sexual differentiation, mating, parenting, social attachments, empathy, cooperation, and altruism

Chapter 1

An Introduction to Neural Systems

Abstract

A primer of the neural systems involved in social behavior across mammals is presented. Definitions of motivation and distinctions between proactive goal-directed (approach or avoidance) and reflexive consummatory behaviors are described. Interactions between the hypothalamus and mesolimbic dopamine (DA) system regulate goal-directed behaviors by influencing whether stimuli are processed across amygdala–striatal–pallidal circuits. Different hypothalamic nuclei regulate different social behaviors, and the interaction between a hypothalamic nucleus and the mesolimbic DA system is conceived as one between a specific and a nonspecific motivational system. Distinct amygdala neurons process either appetitive (pleasant) or aversive stimuli, leading to either approach/attraction or avoidance/rejection responses. The prefrontal cortex, through distinct connections, can either upregulate or downregulate a variety of motivational and emotional processes via influences on the amygdala, nucleus accumbens (ventral striatum), and hypothalamus. The use of functional magnetic resonance imaging and optogenetic methods in defining neural processes relevant to social behavior is described.

Keywords

Amygdala; Approach; Avoidance; Hypothalamus; Mesolimbic dopamine system; Motivation; Nucleus accumbens; Prefrontal cortex; Ventral tegmental area

1.1. Introduction

The purpose of this book is to provide a comprehensive understanding of the neurobiology of social behavior in mammals, including humans. Social behavior, broadly defined, comprises those behaviors that are exhibited by conspecifics as they interact and includes both affiliative (prosocial) and antagonistic (antisocial) interactions. The social behaviors and processes that will be examined include aggression and competition, sexual behaviors, parental behaviors, the formation of social attachments, cooperation, and altruism. Each of these social behaviors will be analyzed across the different levels of investigation that have been used to study the behavior, from molecular neurobiology to neural circuits to functional magnetic resonance imaging (fMRI) data. The first two chapters of the book provide the necessary background in functional neuroanatomy (Chapter 1) and molecular biology and genetics (Chapter 2) that will serve as a foundation for a full appreciation of the neurobiology of social behavior that will be presented in the subsequent chapters.

One important aspect of this book is to uncover the neural mechanisms that determine whether social stimuli are assigned either a positive or a negative valence by the perceiver, with positive social stimuli activating neural pathways that cause contact seeking behaviors, acceptance, caregiving, and other prosocial behaviors, while negative social stimuli activate neural pathways that cause avoidance, rejection, competition, or even attack (antisocial behaviors). In other words, it may be valuable to view social behaviors as being influenced by two elementary neural networks: social stimuli can be processed by either an aversion/rejection network or an attraction/acceptance network, with such differential neural processing leading to different social outcomes [698]. Further, social stimuli may be automatically (innately) routed over either attraction or aversion networks, or such valence properties may be acquired through learning mechanisms. These core neural processes may then set the foundation for more complex social interactions. But what are the neural systems that regulate core approach and avoidance processes, processes that are embedded within and influence more complex social interactions? In what follows, an overview will be presented of functional neuroanatomy with an aim to explain such approach and avoidance systems in mammals. Animals approach or avoid a broad range of stimuli, not just social stimuli. Research findings will be presented from both social and nonsocial contexts with the understanding, which will be borne out in subsequent chapters, that there is overlap in the neural systems influencing social and nonsocial motivational processes (see [82]).

1.2. A Schematic Overview of the Mammalian Brain

Based on the neuroanatomy in Swanson [951], Figure 1.1 depicts the general organization of the mammalian brain. Moving from rostral to caudal, the brain is broken down into two great divisions: the cerebral hemispheres (telencephalon) and the brainstem. Caudal to the brainstem lies the spinal cord. The cerebral hemispheres are divided into the cerebral cortex and the underlying, and therefore subcortical, cerebral nuclei. The cerebral cortex can be divided into isocortex (neocortex) and allocortex, with the former containing six well-defined cellular layers, while the latter contains less than six well-differentiated layers [951]. Isocortex makes up most of the occipital, parietal, temporal, and lateral prefrontal parts of the cortex. Examples of allocortex include the olfactory (piriform) cortex, parts of the amygdala, the hippocampal formation, and parts of the medial and orbital prefrontal cortex. Some important subcortical cerebral nuclei include the caudate nucleus (dorsal striatum), nucleus accumbens (ventral striatum), globus pallidus (dorsal pallidum), ventral pallidum, septal area, and some nuclei within the amygdala. The brainstem, upon which sits the cerebral hemispheres, is composed of the thalamus and hypothalamus (diencephalon), and the lower brainstem, which includes the midbrain, pons, cerebellum, and medulla. Some of the lower brainstem nuclei that will be shown to play important roles in social behavior are the midbrain periaqueductal gray (PAG), dopamine neurons within the ventral tegmental area of the midbrain, and the serotonin neurons of the raphe nuclei located in the midbrain and pons. The term brainstem motor area (BSMA) will be used to refer to a group of nuclei in the lower brainstem with indirect and direct connections to cranial and spinal motor neurons. Most relevant with respect to the BSMA, the PAG and the midbrain locomotor region (located lateral to the PAG) both project to the medullary reticular formation, whose axons project to cranial and spinal motor neurons [361,420,1069]. As will become important, the descending projection of the midbrain PAG to the medullary reticular formation is an important route through which PAG output affects the display of reflex-like defensive and aggressive responses, such as behavioral immobility, escape responses, or biting, and reflexive responses related to sexual and parental behaviors.

FIGURE 1.1 A schematic overview of the mammalian brain. The telencephalon (cerebral hemispheres) is composed of outer cortical layers and underlying cerebral nuclei. Caudal to the telencephalon is the brainstem, containing the diencephalon, midbrain, pons, cerebellum, and medulla. The spinal cord lies caudal to the medulla. Each section of the brainstem lists certain structures that are emphasized in this book. This listing is not meant to represent the exact anatomical location of the labeled structures but simply indicates their general location. For example, within the diencephalon, the thalamus is dorsal, not anterior, to the hypothalamus. Abbreviations: CB = cerebellum; DR = dorsal raphe nucleus; MR = median raphe nucleus; MRF = medullary reticular formation; PAG = periaqueductal gray; SN = substantia nigra; VTA = ventral tegmental area.

1.3. Functional Neuroanatomy

1.3.1. The Hypothalamus

1.3.1.1. Introduction

The three major functions of the hypothalamus are its regulatory influences over the autonomic nervous system and the pituitary gland, and its involvement in the control of a variety of motivated behaviors, including social behaviors [716,813,950]. Figure 1.2 shows a horizontal section through the hypothalamus, displaying its rostral-to-caudal and medial-to-lateral organization. With respect to its organization from medial to lateral, the hypothalamus contains a periventricular zone (which surrounds the third ventricle) and a medial and lateral zone. The periventricular zone contains those neurons primarily involved in neuroendocrine and autonomic regulation, while it is the nuclei of the medial and lateral zones that play dominant roles in the control of motivated behaviors, which involve influences over the somatic motor mechanisms that control both the reflexive and voluntary aspects of these behaviors. The social behaviors influenced by the hypothalamus include reproductive behaviors (sexual and parental) and aggressive and defensive behaviors. As will be seen, it is likely that separate and distinct neuronal populations within the hypothalamus regulate different social behaviors.

FIGURE 1.2 Horizontal section through the hypothalamus. The third ventricle is shown as a thick black line down the midline. Moving from medial to lateral, the hypothalamus contains a periventricular zone (PVZ), a medial zone, and a lateral zone. Other abbreviations: AHN = anterior hypothalamic nucleus; LH = lateral hypothalamus; LPOA = lateral preoptic area; MPOA = medial preoptic area; PH = posterior hypothalamus; PVN = paraventricular nucleus; VMN = ventromedial nucleus.

Given the involvement of the hypothalamus in social and other motivated behaviors, one would expect that it would be a recipient of significant sensory inputs, and indeed this is the case [759,813]. The hypothalamus receives olfactory inputs from the amygdala and other olfactory areas. Afferents from the brainstem carry tactile and pain inputs, and the hypothalamus receives multimodal sensory inputs from the prefrontal cortex and from the hippocampus, the latter arriving either directly or indirectly via the septal area. Finally, an organism’s internal state importantly influences its social behavior, and primary among these internal factors are hormones. Neurons in the hypothalamus contain receptors for prolactin, estradiol, testosterone, progesterone, and adrenal corticosteroids [813,950]. A simple view is that hormones and other internal physiological stimuli bias how various sensory inputs are processed by the hypothalamus, which in turn affects the hypothalamic efferent pathways that are activated. With respect to social behavior, such effects would allow an organism to respond in one way or another to particular social stimuli, depending on the current hormonal milieu that is affecting the operation of specific neural circuits.

1.3.1.2. Motivation: Appetitive, Avoidance/Rejection, and Consummatory Behaviors

Several definitions of motivation exist [90,716,764,1021]. In its simplest definition, motivation is an internal process that modifies an organism’s responsiveness to a constant stimulus. That is, if an organism shows a change in the way it responds to a constant stimulus, some internal alteration must be mediating the behavioral change. As examples, food deprivation increases an organism’s responsiveness to food-related cues, the hormonal events associated with pregnancy termination increase a female’s responsiveness to infant stimuli, and gonadal steroids influence the occurrence of male and female sexual responses to sexual stimuli. Another definition of motivation refers to those internal processes that arouse and direct behavior toward a particular goal, giving rise to the term goal-directed behavior. Two major typ...