Electrophysiological Responses in the Human Amygdala Discriminate Emotion Categories of Complex Visual Stimuli

Abstract
The human amygdala has been shown to participate in processing emotionally salient stimuli related to threat, danger, and aversion, data that have come primarily from functional imaging and lesion studies. Recording intracranial field potentials from five amygdalas in four patients with chronically implanted depth electrodes, we analyzed responses in the gamma frequency range, a region of the power spectrum thought to reflect especially the contribution of neuronal activity to cognitive processes. Significant changes in the power amplitude of responses were obtained selectively to visual images judged to look aversive but not to those judged to look pleasant or neutral. Several possible confounds were addressed: all four patients had been carefully selected so that the amygdalas from which recordings were obtained were distal to epileptogenic foci, making it likely that we recorded from healthy tissue, and the observed responses could not be attributed to luminance or color differences between the stimuli. A further analysis of differences in power between the high and low gamma bands revealed an additional structure that discriminated those stimuli related to bodily injury from those related to disgust. Despite the increased power amplitude in the gamma range, there was no stimulus-locked phase coherence. The observed responses in the gamma frequency range may reflect the role of the amygdala in binding perceptual representations of the stimuli with memory, emotional response, and modulation of ongoing cognition, on the basis of the emotional significance of the stimuli.