Brain evidence of allostatic and interoceptive dysfunction in psychopathy

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Abstract

The search for brain mechanisms of psychopathy has diverse potential starting points. In this review, we propose taking an approach that begins with the question: why do we need a brain? Adopting this starting point requires examining evolutionary evidence, which indicates that brains evolved to anticipate and meet the needs of the body before they arise (i.e., allostasis), and that brains, in service of this aim, continually model and sense the internal conditions of the body (i.e., interoception). These fundamental functions of the nervous system are carried out in part by the allostatic-interoceptive system, which spans brainstem nuclei, subcortical structures, and large-scale cortical networks (i.e., default mode, salience, and somatomotor networks). Psychopathy is related to alterations of the brain’s allostatic-interoceptive system, particularly the cortical extent, in terms of its myeloarchitecture, task-based neural activity, and functional connectivity. Synthesizing evidence of these alterations, we propose that psychopathy is marked by an impaired integrative capacity of the allostatic-interoceptive cortices, resulting in visceromotor signals that lack rich contextual details and that regulate the viscera in a relatively context-insensitive manner. Impoverished visceromotor signals may also hinder the allocation of attention to signals that are relevant to allostasis. However, the extant neuroimaging evidence supporting these hypotheses is highly heterogeneous. We consider two proposals for resolving this heterogeneity, grounded in neuroanatomy and organizing principles of biological systems. Uncovering the brain bases of psychopathy and aggression will likely require moving toward a science of individual brains regulating individual bodies in the context of an ever-changing environment.

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