Neuroanatomy of Social Behaviour: An Evolutionary and Psychoanalytic Perspective

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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.

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CHAPTER ONE Introduction

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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 cognitiv-ist 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 neurophys-iology, 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 psychoanalyti-cally 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.

 

CHAPTER TWO Conceptual framework

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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 sensori-motor modules has to be regulated by a threshold. Cortical sensorimotor modules require matching sensory information for suprathresh-old 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 senso-rimotor 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 sensorimo-tor 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”.

 

CHAPTER THREE Hypthalamo-periaqueductal system

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Neurons at multiple levels of the central nervous system generate specific patterns of sympathetic response that may also contain parasympathetic, endocrine, and somatomotor components. Pattern generators “at different levels of the neuraxis are organized in a hierarchical manner that allows individual response patterns to become parts of larger responses” (Saper, 2002, p. 458). Populations of neurons in the hypothalamus, periaqueductal grey matter, rostral medullary raphe (in the rostral ventromedial medulla), and the ventrolateral medullary reticular formation generate patterned autonomic responses involving multiple tissues. The hypothalamus contains highly integrated pattern generators for sympathetic responses in reproductive and fight-or-flight situations. Single hypothalamic neurons contact a wide range of sympathetic preganglionic neurons jointly concerned with producing an integrated response. Response patterns coordinated by hypothalamic nuclei “involve autonomic, endocrine, and behavioral components that are played out on a temporal and spatial sequence as a combination of more limited patterned responses, organized at other levels of the basal forebrain, brainstem, and spinal cord” (Saper, 2002, p. 460). The hypothalamus can be divided into three longitudinal zones: lateral, periventricular, and medial. Swanson’s (2000) model of basic hypothalamic organization maintains that interconnected medial hypotha-lamic nuclei concerned with ingestive, reproductive, and defensive behaviours (rostral segment of the “behaviour control column” located within the medial hypothalamic zone) project to a medially adjacent “visceromotor pattern generator network”. The “visceromotor pattern generator network”, located in the periventricular hypoth-alamic zone, receives a “triple descending input” from the cerebral hemispheres (cortical excitatory, striatal inhibitory, and pallidal disinhibitory) and projects massively to the “neuroendocrine motor zone” (also located in the periventricular hypoth-alamic zone), which is responsible for generating patterns of hormone secretion from the anterior and posterior lobes of the pituitary (Swanson, 2000).

 

CHAPTER FOUR Basolateral and extended amygdala

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Hippocampus and amygdala are located in the ventromedial portion of the temporal lobe and form part of the limbic system. All sensory information from multimo-dal and association neocortical areas converges on hippocampus and amygdala. The basolateral complex of the amygdala is a cortical-like structure. Like other nonisocortical structures, such as the hippocampus and piriform cortex, it projects prominently to the ventral striatum (mainly the nucleus accumbens) and the extended amygdala (Heimer, 2003). The central amygdala, medial amygdala, and bed nucleus of stria termina-lis are embryologically related and jointly form the “extended amygdala”. The extended amygdala does not, therefore, include the basolateral complex of the amygdala (“lateral basal cortical amygdala”) (Heimer, 2003). The extended amygdala receives cortical input primarily from the “greater limbic lobe” (encompassing allocortex, mesocortex, and basolateral amygdala). In this respect, the extended amygdala is similar to the basal nucleus of Meynert and the precommissural septum, which also receive primarily nonisocor-tical input. With regard to output, the “central division” of the extended amygdala, consisting of the central nucleus of the amygdala and lateral bed nucleus of stria terminalis, projects predominantly to autonomic and somatomotor centres in the lateral hypothalamus and brainstem. The “medial division”, consisting of the medial nucleus of the amygdala and medial bed nucleus of stria terminalis, has prominent projections to endocrine centres in the medial hypothalamus (reviewed in Heimer, 2003). Thus, the extended amygdala is an important output channel for activities in the greater limbic lobe (Figure 4-1), as is the ventral striatal-pallidal system. The extended amygdala is related to, and may even include, the shell of the nucleus accumbens (discussed in Di Chiara, 2002). It may appear that the central nucleus of the amygdala and bed nucleus of stria terminalis associate discriminative environmental stimuli (conditioned stimuli) with unconditioned somatomotor and autonomic responses coordinated by the hypothalamus, much as the shell of the nucleus accumbens links discriminative stimuli, according to Di Chiara (2002), with a state of “incentive arousal”.

 

CHAPTER FIVE Septohippocampal system

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All sensory information from multimodal and association neocortical areas converges on hippocampus and amygdala, which are in located the ventromedial portion of the temporal lobe. The hippocampus can be divided into two subregions: the dorsal half, starting at the septal pole, and the ventral half, starting at the temporal pole of the hippocampus. The “dorsal hippocampus” (called “posterior hippocampus” in primates) is involved in spatial learning (spatial reference memory acquisition) in appetitive tasks (food retrieval in T-maze or radial maze tasks) or aversely motivated tasks (escape from water in water-maze tasks) (reviewed in Bannerman et al., 2004). The “ventral hippocampus” (called “anterior hippocampus” in primates) is located in close apposition to the amygdala and makes an important contribution to the control of behaviour in anxiogenic situations. Anxiety, as a tonic response to an aversive situation or a diffuse aversive cue, depends on the ventral hippocampus, whereas fear, as a phasic response to an explicit aversive cue, depends on the amygdala. Anxiety-related phenomena, such as reduced food intake, reduced social interaction and increased readiness to generate startle reflexes in anxiogenic environments (e.g., novel or bright and open places), are sensitive to lesions of the ventral hippocampus, but not amygdala lesions (reviewed in Bannerman et al., 2004). The hippocampus also supports conditioned freezing. The environmental context within which an aversive event, such as footshock, is encountered does not stand in any clear temporal relationship to the aversive event and will therefore not predict the punisher with any precision. While fear conditioning to elemental cues that temporally precede an aversive event and come to predict the reoccurrence of the pun-isher with some precision (such as in fear conditioning to a short tone) critically depends on the amygdala, assembly of various stimuli in the environment towards a coherent representation of context and association of the environmental context with aversive events are functions subserved by the hippocampus (Sanders et al., 2003). Bannerman et al. (2004) called for a “truly unifying theory of hippocampal function” to explain both episodic-like memory function and the role of the hippocampus in anxiety “by reference to a consistent physiological algorithm performed by the intra-hippocampal circuitry” (p. 279). At this juncture it appears that the dorsal hippocampus encodes and processes unique representations of the spatial environment that can be associated with biologically meaningful events, while the ventral hippocampus may supply an emotional dimension of the present situation that takes into account nonspatial characteristics of the environment and the internal physiological state.

 

CHAPTER SIX Lateral frontoparietal networks

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Within the visual cortex, stimuli compete for neural representation. Simultaneously presented visual stimuli suppress each other ‘s neuronal representation in striate and extrastriate visual areas (including V1, V2, V3, V4, temporal-occipital area, and middle temporal area). Stimuli that survive the competition for neural representation are in a position to impact on memory and motor systems. Attention modulates this competitive interaction among stimuli. The initial stimulus-related response in the primary visual cortex (V1) takes place about 60–90 ms after stimulus onset. It is the longer-latency activity in the primary visual cortex, taking place in the range of 150–250 ms, that is strongly modulated by attention. Attentional control areas enhance the processing of visual information for attended compared with unattended information. Spatially directed attention to one of simultaneously presented visual stimuli counteracts the suppressive effect of competing visual stimuli, particularly in V4 and the temporal-occipital area (reviewed in Pessoa, Kastner & Ungerleider, 2003). Thus, “directed attention enhances information processing of stimuli at the attended location by counteracting suppression induced by nearby stimuli”, with the consequence that “irrelevant distracting information is effectively filtered out” (Pessoa et al., 2003, p. 3992).

 

CHAPTER SEVEN Prefrontal cortex (medial and orbital)

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Patterns of activity in the prefrontal cortex represent goals and rules required to perform tasks. “Executive control” involves the sustained activation of representations that correspond to the goal of a behaviour and the rules for achieving it. Evidence suggests that prefrontal activity representing rules and other task-relevant information is maintained robustly, in the face of interference by distracters, until a goal is achieved (reviewed in Miller & Cohen, 2001). The prefrontal cortex is directly connected with association cortices where stimuli are represented in a behaviourally relevant manner. Stimulus representations coding for response dispositions compete for expression in behaviour. Representations of goals and rules in the prefron-tal cortex act as biasing signals that resolve the competition between stimulus representations in other parts of the brain. Thus, prefrontal representations of goals and rules guide stimulus-response mappings in accordance with current task demands and in a contextually appropriate manner (Miller & Cohen, 2001). Goals and rules represented in the prefrontal cortex favour the processing of task-relevant sensory input and the retrieval of task-relevant memories. The ability of goal and rule representations to bias the competition between conflicting representations in favour of task-relevant information (away from task-irrelevant information) can be conceptualized as “attention” and “behavioural inhibition”. Insofar as they act to favour task-relevant information, goals and rules represented in the lateral prefrontal cortex can be regarded as “attentional templates”. Miller and Cohen (2001) suggested that the prefrontal cortex exerts its biasing influence over behaviour not only in the form of directed attention but also through response selection and inhibitory control in the motor system. To this effect, the prefrontal cortex has extensive connections with premotor cortices (which in turn send projections to the primary motor cortex).

 

CHAPTER EIGHT Basal ganglia

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Swanson (2000) proposed a minimal circuit model wherein the cortex sends an excitatory projection to the brainstem motor system, with an excitatory collateral projection to the striatum. The striatum, in turn, sends an inhibitory projection to the brainstem motor system, with an inhibitory collateral to the pallidum. Finally, the pallidum sends an inhibitory projection to the brainstem motor system, with an inhibitory collateral to the thalamus. Thalamic input arises “as collaterals of thicker descending parent axons to the brainstem” (p. 154). Thus, there is a “triple cascading projection” from the cerebral hemispheres (telencephalon) to the brainstem motor system. For instance, the sub-stantia nigra and ventral tegmental area, which form part of the caudal segment of the “behaviour control column”, receive such “triple descending cerebral input” (Swanson, 2000). Firstly, there is a topographically organized GABAergic projection from the caudate-putamen (dorsal striatum) to the substantia nigra, with collaterals to the globus pallidus. The caudate-putamen, in turn, receives a topographically organized projection from the motor cortex. By comparison, the ventral striatum, which distributes GABAergic fibres to the ventral tegmental area, receives cortical inputs from the entorhinal area of the hippocampal formation, the perirhinal area of the inferior temporal association cortex, the medial prefrontal cortex, and the caudally adjacent agranular insular region. Secondly, there is a dense GABAergic projection form the globus pallidus (dorsal pallidum) to the substantia nigra. The ventral pallidum, on the other hand, is known for its inhibitory projections to the ventral tegmental area. Thirdly, there is a cortical projection to the substantia nigra, emanating from the somatosensory cortex. By comparison, the ventral tegmental area receives cortical input from the medial prefrontal cortex. Importantly, embryological data suggest that “striatum” and “pallidum” need to be conceived more broadly as fundamental divisions of the telencephalon (Swanson, 2000). The striatum should not only include caudate-putamen and nucleus accumbens (dorsal and ventral striatum, respectively), and the pallidum needs to be seen as extending beyond globus pallidus and substantia innominata (dorsal and ventral pallidum, respectively). Striatum and pallidum, when conceived more broadly, include parts of the extended amygdala and septal nuclei (which can be allocated to “medial” and “caudorostral” divisions of the striatum and pallidum). Each of the different regions of the pallidum (globus pallidus, substantia innomi-nata, bed nucleus of stria terminalis, medial septal complex) is known to provide a double projection to the diencephalic and brainstem motor system as well as the ventral and dorsal thalamus (reviewed in Swanson, 2000).

 

CHAPTER NINE Syntheses

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Perception (primarily an unconscious process) and action are closely linked. Activation of a sensorimotor module by external sensory information can automatically produce a motor response, as illustrated by stimulus-bound phenomena. Partial activation of a sensorimotor module would not implement the link between stimulus and response but enhance the probability of responding, that is, create an action disposition. By activating stimulus-response representations (sensorimotor transformations) without bringing them above threshold, external stimuli can be said to prime these representations. The pattern of sensory input reflective of the present external environment activates several sensorimotor modules probabilistically, so that sensory input concurrently produces several action dispositions. Action dispositions, which may suppress each other or accumulate over time towards the activation of more abstract representations, are gated by an abstract appreciation of the present environmental situation and internal motivational state. The environmental context and motivational factors (reflecting hormonal or homeostatic alterations or exposure to unconditioned stimuli) enhance the probability of object-directed or cue-triggered action if representations of these objects or cues are supported by evolving patterns of sensory input. In other words, attentional sets, which constrain the competition between stimulus-response transformations or more complex object- or cue-guided actions, are instated in a manner that depends on the organism’s physiological needs as well as spatiotemporal characteristics of the environmental situation. Place and situation representations formed by the hippocampus are responsible for our orientation and behavioural relatedness to the environmental context and social situation.

 

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