Frequency-specific gaze modulation of emotional face processing in the human amygdala

Determining the social significance of emotional face expression is of major importance for adaptive behavior, and gaze direction provides critical information in this process. The amygdala is implicated in both emotion and gaze processing, but how and when it integrates expression and gaze cues remains unresolved. We tackled this question using intracranial electroencephalography in epileptic patients to assess both amygdala (n = 12) and orbitofrontal cortex (OFC; n = 11) time-frequency evoked responses to faces with different emotional expressions and different gaze directions. As predicted, self-relevant threat signals (averted fearful and directed angry faces) elicited stronger amygdala activity than self-irrelevant threat (directed fearful and averted angry faces). Fear effects started at early latencies in both amygdala and OFC (~110 and 160 ms, respectively), while gaze direction effects and their interaction with emotion occurred at later latencies. Critically, the amygdala showed differential gamma band increases to fearful averted gaze (starting ~550 ms) and to angry directed gaze (~470 ms). Moreover, when comparing the 2 self-relevant threat conditions among them, we found higher gamma amygdala activity for averted fearful faces and higher beta OFC activity for angry directed faces. Together, these results reveal for the first time frequency-specific effects of emotion and gaze on amygdala and OFC neural activity.