Face processing in human and macaque amygdala

In an inter-species study, we show that human and non-human primates prioritize faces of conspecifics during free-viewing. Neural activity recorded from individual amygdala cells in both species shows that faces of conspecifics are preferentially processed.

Summary

Neurons in the primate amygdala respond prominently to faces. This implicates the amygdala in the processing of socially significant stimuli, yet its contribution to social perception remains poorly understood. We evaluated the representation of faces in the primate amygdala during naturalistic conditions by recording from both human and macaque amygdala neurons during free viewing of identical arrays of images with concurrent eye tracking. Neurons responded to faces only when they were fixated, suggesting that neuronal activity was gated by visual attention. Further experiments in humans utilizing covert attention confirmed this hypothesis. In both species, the majority of face-selective neurons preferred faces of conspecifics, a bias also seen behaviorally in first fixation preferences. Response latencies, relative to fixation onset, were shortest for conspecific-selective neurons and were ∼100 ms shorter in monkeys compared to humans. This argues that attention to faces gates amygdala responses, which in turn prioritize species-typical information for further processing.

Humans (left) and macaques (right) viewed an array of images sampled from four different categories as we monitored their eye movements concurrently with neural activity from amygdala cells. Face-selective cells were common in both species, and mostly tuned to faces of conspecifics. Cells tuned to faces of conspecifics responded faster than those tuned to faces of heterospecifics, further suggesting that amygdala cells preferentially process socially-relevant stimuli.