Neuroanatomy of Social Behaviour

An Evolutionary and Psychoanalytic Perspective

Ralf-Peter Behrendt

• Publisher: Routledge
• Year: 2018
• Print ISBN: 9780367322762
• eBook ISBN: 9780429916533
• Topic: Psychology
• Subtopic: History & Theory in Psychology
• Index: Psychology

This book is for readers who are knowledgeable about the neurosciences and curious about brain mechanisms that produce normal and pathological social behaviour. It is a reference work that presents and reviews facts and recent findings that need to be accounted for within a coherent neuroanatomy and neurophysiology of social behaviour.

Chapter One
Introduction

Attempts to relate social behaviour and psychopathology to neuroscience, and on a more fundamental level to unify the social and psychological sciences with the physical sciences, are plagued by seemingly insurmountable conceptual problems attributable, in part, to the continuing dominance of cognitivist views. Insights provided by a rich tradition of psychoanalytic theory will prove critical in bridging the existing gap between psychology and sociology, on the one hand, and the neurosciences, on the other. Psychoanalysis, along with philosophical phenomenology, may help us to construct an evolutionarily sound understanding of social phenomena onto which the accumulating body of evidence from neurophysiology, behavioural neuroscience, and biological psychiatry can be mapped parsimoniously. The contention is that a conceptual framework founded on psychoanalysis, philosophical phenomenology, and evolutionary theory can elucidate the otherwise incomprehensible complexity of the brain. In fact, adoption of a psychoanalytically informed framework may be unavoidable if we want to succeed in understanding how the brain has evolved for, and subserves, complex social behaviours and psychological phenomena, both in adaptive social functioning and mental illness. The role envisaged for psychoanalysis goes beyond the well-known emphasis on the primacy of the unconscious. Firstly, psychological phenomena that arise in an interpersonal context are, of course, nothing but manifestations of unconscious drives and defence mechanisms, yet we have to apply this principle without compromising to all conscious phenomena. A position that leaves any room for a conscious agency, or does not fully discard the idea that conscious phenomena are causal to behaviour, is philosophically untenable. Secondly, psychoanalysis provides a wealth of clinical findings and internally consistent ideas that allow us to relate psychological and psychopathological phenomena to an interplay of primitive behaviour modes that are deeply rooted in the evolution of reward seeking and defensive behaviours of vertebrates. Psychopathology, as captured by descriptive phenomenology and conceptualized by psychoanalysis, is a rich source of information, highlighting more clearly the primitive motivational processes that drive all social behaviour and give rise to the interpersonal, social, and cultural fabric that surrounds us—primitive motivational processes that, unless they present themselves under extreme conditions, we are well versed to ignore or rationalize away within a worldview that centres on our notion of the self as the rational agent of all our actions.

Thus, in seeking to understand the way in which the brain subserves, and has evolved for, social behaviour, we face two interlinking tasks. Firstly, the basic structure of social behaviour needs to be understood in a way that is evolutionarily and ontogenetically sensible. Insights gained by psychoanalytic theory are critical in guiding attempts to elucidate the interplay of primitive motivational process in the generation of complex social behaviours. Secondly, we need to discern principles of brain function from a body of neurobiological data that is methodologically heterogeneous, still remains poorly conceptualized, systematized, and integrated, and only penetrates the surface of an immense complexity of brain function and brain-behaviour relationships. Neuroscientific research into mental illness usefully correlates extremes of the motivational interplay underpinning social behaviour with selected aspects of brain function, yet we still need a conceptual framework within which to integrate these data. Again, psychoanalysis cannot be ignored if we want to find a way in which brain function can be mapped onto a robust understanding of the structure of social behaviour. A proper understanding of the consciousness-brain relationship is an important step in the conceptual advance that is required. We will only be able to elucidate principles of brain function related to social functioning and mental illness if we can ascertain in how far our conscious awareness of aspects of our behaviour is relevant to the actual working of the brain and the way in which the brain actually produces behaviour. It is proposed here that by reducing consciousness to a mnemonic process subserved by certain arrangements in the hippocampus, we avoid the temptation of prematurely embedding principles of behaviour that we discern through introspection within structures and mechanisms of the brain (agreeing here with a principle of behaviourism). In particular, conceptualizing the self or conscious emotions as factors that are causally related to behaviour, as common sense would suggest, only serves to confuse efforts of understanding the relationship between brain and motivated social behaviour.

From the present vantage point it appears that the terminology of cognitive psychology, cognitive neuroscience, and sociology has obstructed the path towards a unification of psychology and sociology with the physical sciences. Insights offered by psychoanalytic theory and philosophical phenomenology rapidly advancing in the first half of the 20th century have not been seized upon by behavioural neuroscience. On the other hand, conceptual difficulties are often related to the practical functions which language evolved to serve. The interpretation of data emanating from neuroscience experiments designed to reveal mechanisms involved in “reward”, “attention”, or “memory”, “must depend on our concepts of cognitive processing, which might ultimately prove to be poor descriptions of the signals used by the brain” (Maunsell, 2004, p. 261). Discussing the concept of “reward” in neuroscience, Ikemoto and Panksepp (1999) were concerned that “existing conceptual frameworks constrain the way in which empirical findings are interpreted”. The term “reward”, for instance, has connotations of “pleasure”; it suggests misleadingly that reinforcers have emotional or hedonic effects (Salamone, Correa, Farrar & Mingote, 2007). Similarly, reviewing the history of research into hippocampal θ oscillations, Buzsáki (2005) concluded:

… that our behavioral-cognitive terms are simply working hypothetical constructs that do not necessarily correspond to any given brain mechanism. Although the true goal of neuroscience research is to reveal how the brain generates behavior …, most behavioral-cognitive research, to date, seems to work in the opposite direction. We take a man-created word or concept … and search for brain mechanisms that may be responsible for the generation of this conceived behavior. (Buzsáki, 2005, p. 828)

It is difficult not to be misled by common sense and fall into the trap of teleological thinking when discussing “goal”-directed behaviour (such as the pursuit of “reward”) and its contribution to social behaviour. In line with advances in other fields of science, the challenge is to explain purposeful behaviour in terms of self-organization and deterministic chaos. Firstly, we have to accept that behaviour and mental processes are thoroughly deterministic: behavioural, psychopathological, and social phenomena are determined by physical causes. The concept of self-organization encourages us to view complex phenomena, attributable to any one level of a system’s organization, as emerging from competitive interaction between more elemental processes on a lower level of organization. Accordingly, each set of phenomena has its appropriate level of explanation. Psychological and social phenomena need to be explained without recourse to teleology and in such a way that the layering of levels of self-organization can be recognized. Secondly, the concept of chaos as applied to various levels of organization elucidates the variability of behavioural expression. On each level of self-organization, complex phenomena arise unpredictably but deterministically, whereby the marginal conditions under which self-organizing processes occur are regulated by evolved regulatory mechanisms. Like others, Schall (2001) recognized that “decisions originate in deterministic brain processes”, whereby “states of the brain, although deterministic, are not entirely predictable” (p. 40).

Certainly, to the extent that neurons will not discharge unless they are depolarized by other neurons, brain states can be determined naturally only by earlier brain states. However, does such apparently Laplacian determinism grant as much prediction and influence as the evidence seems to indicate? Perhaps not. Complex dynamic systems that are far from equilibrium are usually not predictable. The brain is without doubt such a dynamical system that produces behaviour with the signature of chaos … . Thus, the states of the brain, like the clouds in the sky, happen because of earlier states of the system. (Schall, 2001, p. 40)

An important level of self-organization concerns stimulus-response relationships. Primitive stimulus-response mappings would have evolved into perception-action transformations that are controlled not by discrete stimuli but by objects abstracted in the process of hierarchical sensory processing. Object representations would be necessary for gating access to approach or instrumental behaviour modes, although detailed stimulus representations remain essential for the implementation of instances of these behaviours. Thus, the environment would be neurally represented, on one level, in terms of the meaning of objects (that is, the ability of objects to provide access to higher-level behaviour modes) and, on another level, in terms of cues specifying orienting reactions as well as motor responses that implement object-guided behaviour. Importantly, object and cue representations activated by dynamically evolving patterns of sensory input tend to give rise to response dispositions that suppress each other in a competitive fashion. Perception-action transformations are controlled by thresholds (Mazurek, Roitman, Ditterich & Shadlen, 2003), which not only allow for competition between cue or object representations but also enables their cooperation towards the formation of increasingly differentiated and sophisticated perception-action transformations. Apart form cues and objects, the external world is represented in terms of situations that constrain the selection of sensorimotor transformations or more complex perception-action transformation. Behavioural responding to some but not other cues or objects is adaptive within a particular motivational and situational context. Situations, which can refer to spatial locations or recurring social constellations, are encoded within spatial and temporal frames of reference. Ongoing characterization of situations may enable orien tation to, and behavioural navigation across, space and time and, ultimately, may be responsible for our experience of space and time.

The social situation, as it is presently faced by an individual, automatically translates into competing dispositions towards attention-seeking, aggressive, and submissive (normative) behaviours. At the very least, social behaviour is characterized by a conflict between the need to be seen and the need not to be seen (Laing, 1960). Withdrawal or escape from unconditionally aversive locations and fear-conditioned contexts, in which there may be an increased risk of encountering predators or other harmful events, may have evolved into behaviours soliciting inclusion into social formations. We may find that, in animals with a tendency to congregate into social formations, separation from the group or the experience of being rejected by, or detached from, members of the group (social unrelatedness) is evolutionarily related to the aversiveness of locations that expose to harm or the risk of harm. We may expect that navigation to, or active creation of, situations of safety (unlikely exposure to harm) is intertwined with an equally important tendency to navigate to, or actively create, situations in which affiliative reward (including other’s positive regard) is available. The contribution of aggression to complex social behaviours has to be recognized, too. Occupying a social position that securely provides access to affiliative reward, we hold on to this position through territorial (offensive) aggression directed against competitors (who unwittingly challenge our position through their lack of submission or “respect”). Cues that signify others’ social position in a hierarchy, and hence their capacity to express offensive aggression and inflict social punishment, are woven into the experience of, and memory for, social situations. Active avoidance behaviours elicited by conditioned fear stimuli or contexts may have evolved into social submission and conformity, that is, behaviours designed to avert the possibility of social punishment by actively inhibiting others’ potential for territorial (offensive) aggression. Thus, social stimuli are represented and perceived according to an imperative to “hide” from the group and not to become a target for others’ aggression, while, on the other hand, cues are represented and perceived insofar as they guide our drive to attract social attention. Social networks within which we actively, if not aggressively, move towards, or seek to maintain, a secure and resourceful position dynamically self-organize, producing a wealth of social and cultural phenomena (Lorenz, 1963).

Chapter Two
Conceptual framework

The evolution of behaviour started with simple stimulus-response relationships. Elementary sensorimotor modules link discrete sensory stimuli with discrete motor patterns that modify the external environment or change the position of the organism within the environment. Higher-order sensorimotor modules link regularities or patterns in sensory information with complex motor programs. Activation of sensorimotor modules, particularly those on higher levels of the sensorimotor hierarchy, needs to unfold gradually over time in order to enable the integration of changes over time in patterns of external sensory information. The temporal integration of sensory evidence over time “may be a fundamental computation underlying higher cognitive functions that are dissociated from immediate sensory inputs or motor outputs” (Huk & Shadlen, 2005). For such integration to occur, motor output from sensorimotor modules has to be regulated by a threshold. Cortical sensorimotor modules require matching sensory information for suprathreshold activation and generation of motor output. Sensory signals, which can be “construed as evidence for versus against a proposition”, must be “integrated to a threshold level”, the crossing of which “signals a commitment to a proposition or behavioral response” (Mazurek et al., 2003, p. 1268). Only a certain constellation of sensory inputs ascertained, over time, from the external environment would be able to activate a sensorimotor module above threshold. Sensory input reflecting the organism’s present environment is inherently ambiguous and may not contain a pattern that would in itself unambiguously activate above threshold one particular sensorimotor module. Under these circumstances, several sensorimotor modules would compete with each other for access to motor output structures. There has to be a process that resolves this competition: “perceptual decision making”.

Higher-order perception-action transformations may involve the activation of representations of “objects” that gate access to general-purpose behaviours or behavioural response modes. Cortical representations of objects or meaningful cues link abstractions derived from sensory input (in a manner that is independent from the particular environmental situation in which the animal finds itself) with mechanisms controlling behaviours that interact with aspects of the external physical world that correspond to these object representations. Objects and meaningful cues are represented in terms of the type of action mode that they engender, such as approach, grasping, or reaching. Several object representations may compete with each other within the same motivational and environmental context by accruing supportive sensory information from among sensory input that is continuously updated by orienting reactions. Ongoing orienting reactions may help to negotiate the balance between dispositions towards competing object-guided (or cue-guided) behaviours. Once a choice has been made, object-representing cortical networks may implement object-guided behaviour indirectly, via brainstem neurotransmitter centres that control global brain states specialized for a certain class of subordinate sensorimotor transformations. Thus, perception can be viewed as an unconscious process that entails the dynamic accumulation, under attentional constraints, of sensory evidence in cortical representations of cues, objects, and concepts that can be subjected to decision making. We will find that processes of unconscious object perception work in parallel with unconscious processes that link the animal’s appreciation and perception of its current situation with behaviours and behaviour modes.

A tendency for external resources to become sparse in a competitive environment is likely to provide an impetus for the gradual sophistication of stimulus-response transformations that bring the animal into contact with rewards that meet internal physiological needs. Stimulus-response mechanisms that serve defensive purposes are subjected to evolutionary pressures, too. Unconditioned pain stimuli and, perhaps secondarily in evolution, unconditioned aversive contexts elicit withdrawal reactions and vocalizations. Impulsive withdrawal inherent to pain responding may have evolved as a defensive strategy against stationary environmental dangers and more placid predators. Having evolved an ability to locate and approach prey, predators evolved to become more vigorous in their pursuit, that is, more aggressive, in order to prevent the prey from withdrawing or escaping once they were injured (Nell, 2006). Defensive aggression in response to aversive stimulation, rather than impulses to simply withdraw, may have evolved to meet the challenge posed by increasingly aggressive predators. Thus, flight and defensive aggression coevolved alongside chasing (vigorous pursuit) and stalking behaviours (the latter two being aspects of predatory aggression). Animals evolved the capacity to withdraw from unconditionally aversive contexts (and not just from aversive stimuli), minimizing exposure to environments or situations in which they can easily be detected and pursued by predators (such as bright, open places, or isolation from the herd). In species in which proximity to the mother or membership of a herd or social group serves the protection against predators, social isolation is aversive and elicits withdrawal behaviour (which is expressed in more or less abstract form). As a further example of predator-prey coevolution, prey freeze in response to stimuli predictive of a predator, such as sudden movement or noise, in order to avoid detection. Some predators may have capitalized on the tendency of prey to freeze by employing vigorous gestures and vocalizations in the vicinity of the prey and thereby preventing the prey from fleeing. Distress vocalizations by prey that have been injured may serve to attract assistance from the herd or social group, similarly to how the aversive state of separation from the mother is linked with separation calls that attract the mother. Predators are often prey to other species of predators. Primates, too, were having to perfect both sets of behaviour: predatory and defensive.

Mechanisms underlying predatory (instrumental) and defensive aggression can be implicated in the evolution of social behaviour. Territorial aggression, which may be evolutionarily related to instrumental aggression or defensive aggression or both, is another important contributor to social evolution. Territorial aggression (also known as offensive aggression) enables animals to actively maintain access to limited resources in competition with conspecifics. The evolution of territorial aggression necessitated, and was paralleled by, the evolution of species-specific submissive behaviours, which serve to inhibit territorial aggression in the territory’s resident or prevent such aggression from escalating. Due to evolutionary pressures exerted by predators, animals started to congregate in herds. In predatory species that are prey to other species (such as primates vis-à-vis large carnivores), defensive congregation in herds may have acted as a juncture at which strictly territorial aggression evolved into intraspecific offensive aggression that serves to defend an individual’s social rank, that is, the individual’s “social territory”. Primates and other highly social mammals have a tendency to attack those conspecifics who, in search for affiliative or other rewards, intrude into their “social terr...

Table of contents

• Cover
• Half Title
• Title
• Copyright
• Dedication
• Contents
• ABOUT THE AUTHOR
• CHAPTER ONE Introduction
• CHAPTER TWO Conceptual framework
• CHAPTER THREE Hypthalamo-periaqueductal system
• CHAPTER FOUR Basolateral and extended amygdala
• CHAPTER FIVE Septohippocampal system
• CHAPTER SIX Lateral frontoparietal networks
• CHAPTER SEVEN Prefrontal cortex (medial and orbital)
• CHAPTER EIGHT Basal ganglia
• CHAPTER NINE Syntheses
• REFERENCES
• INDEX