The primate amygdala in social perception – insights from electrophysiological recordings and stimulation

Abstract

The amygdala’s role in emotion and social perception has been intensively investigated primarily through studies using fMRI. Recently, this topic has been examined using single-unit recordings in both humans and monkeys, with a focus on face processing. The findings provide novel insights, including several surprises: amygdala neurons have very long response latencies, show highly nonlinear responses to whole faces, and can be exquisitely selective for very specific parts of faces such as the eyes. In humans, the responses of amygdala neurons correlate with internal states evoked by faces, rather than with their objective features. Current and future studies extend the investigations to psychiatric illnesses such as autism, in which atypical face processing is a hallmark of social dysfunction.

Fixations Gate Species-Specific Responses to Free Viewing of Faces in the Human and Macaque Amygdala

“…This view of the amygdala’s function fits with a long-standing debate about whether the amygdala mediates rapid automatic and relatively coarse detection of significant stimuli through a route of subcortical inputs (Cauchoix and Crouzet, 2013). These views challenge observations that human amygdala neurons show exceedingly long visual response latencies (Mormann et al, 2008; Rutishauser et al, 2015a), and that fMRI activation of the amygdala appears to require visual attention (Pessoa et al, 2002). In the absence of comparative studies using the same stimuli and the same paradigm in both species, it is nearly impossible to determine whether these are differences between the two species or rather different experimental conditions.…”

“…The finding that face-selective neural responses in the amygdala are strongly related to visual attention is ecologically important, because, in real social situations, directing one’s gaze towards or away from faces and parts thereof (in particular the eyes) is a crucial social signal and sets the affective tone of the social interaction (Emery, 2000). The amygdala is crucially involved in this process (Adolphs et al, 2005; Rutishauser et al, 2015a), and impairments in directing gaze to faces are a prominent deficit in autism that is thought to be partially due to amygdala dysfunction (Baron-Cohen et al, 2000; Rutishauser et al, 2013). While a preference for features, such as the eyes, can be explained by perceptual properties (Ohayon et al, 2012), the conspecific-preference we showed cannot be attributed to low-level stimulus properties.…”

Neural Basis for Economic Saving Strategies in Human Amygdala-Prefrontal Reward Circuits

“…Such cue reactivity is also a dominant theme in current views of human amygdala function [37, 38, 39, 40]. By contrast, recent neurophysiological investigations implicate the amygdala in more complex, sequential decision-making [15, 16].…”

Gutsy Moves: The Amygdala as a Critical Node in Microbiota to Brain Signaling

“…Amygdala lesions in humans and non-human primates seem to diminish social inhibition and limit social perception, increasing social interaction and interfering with adherence to social norms. [45,46] In ASD, enlarged amygdala volumes during infancy have been associated with the severity of social and communicative Figure 2. Overlapping timelines of sensitivity to environmental insult or intervention for the amygdala and gut microbiota across the lifespan.…”