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Social behavior from a comparative neuroanatomical perspective : the amygdala in human evolution

  • Author(s): Barger, Nicole L.
  • et al.
Abstract

Anatomically, the amygdala and its 13 component nuclei integrate higher order perceptual information from the neocortex with subcortical neuroendocrine and autonomic centers. Functionally, it is a central constituent in the neural circuits subserving social and emotional behavior. An increasingly influential hypothesis posits that primate intelligence has arisen in response to challenges in the social milieu. However, structures associated with emotion processing, i.e., "limbic" structures, have been historically construed as primitive. Given these competing claims, this dissertation seeks to assess the amygdala's role in human brain evolution by quantifying and comparing volumes and neuron counts for the amygdala and four of its major nuclei (the lateral, basal, accessory basal, and central nuclei) in a large sample comprising humans and all ape genera. Analyses revealed three core findings. First, human amygdala volume has tripled in size, but neuron numbers have been maintained in great ape ranges, suggesting that changes in neuron number and volume may be decoupled in human amygdala evolution. Second, the intrinsic organization of the human amygdala is unique compared with ape amygdala. Specifically, the human lateral nucleus is 37% larger and contains 59% more neurons than expected, departing from the organization of ape amygdala which emphasize the basal nucleus. Conversely, the central nucleus was three times smaller in the human amygdala than expected. As the lateral nucleus is the major recipient of neocortical, especially temporal lobe, input and the central nucleus is the major source of autonomic output, human amygdala reorganization may reflect the expansion and conservation of these interconnected anatomical regions, respectively. Third, the human lateral nucleus is one of the most expansive structures in the human limbic system, second only to the hippocampus. Volumetric increases in the lateral nucleus and amygdala also outpace expansion in the dorsal frontal cortex, a region associated both with executive and motor, but not emotional, function, indicating that emotion processing is not uniquely or especially de-emphasized in human brain evolution. Overall, it may be speculated that increases in the human lateral nucleus arose in response to a heightened need to process the emotional salience of stimuli in the complex human social environment

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