Amygdala processing of social cues from faces: an intracrebral EEG study

Abstract

The amygdala is a key structure for monitoring the relevance of environmental stimuli. Yet, little is known about the dynamics of its response to primary social cues such as gaze and emotion. Here, we examined evoked amygdala responses to gaze and facial emotion changes in five epileptic patients with intracerebral electrodes. Patients first viewed a neutral face that would then convey social cues: it turned either happy or fearful with or without gaze aversion. This social cue was followed by a laterally presented target, the detection of which was faster if it appeared in a location congruent with the averted gaze direction. First, we observed pronounced evoked amygdala potentials to the initial neutral face. Second, analysis of the evoked responses to the cue showed an early effect of gaze starting at 123 ms in the right amygdala. Differential effects of fearful vs happy valence were individually present but more variable in time and therefore not observed at group-level. Our study is the first to demonstrate such an early effect of gaze in the amygdala, in line with its particular behavioral relevance in the spatial attention task.

Keywords: amygdala; emotion; facial expression; gaze; intracranial EEG.

© The Author (2015). Published by Oxford University Press. For Permissions, please email: journals.permissions@oup.com.

Figures

Fig. 1.

Experimental paradigm. A trial consisted of a central fixation cross followed by a neutral face with direct gaze. After a variable time interval of 400–600 ms, the same face would turn happy or fearful, with or without gaze aversion. Then, after a variable cue-to-target interval (SOA: 300–450 ms), a black and white checkerboard target appeared either on the left or on the right side of the screen.

Fig. 2.

Evoked potentials to the presentation of the neutral face. All patients generated discernable ERPs to the onset of the neutral face, equivalent to an N200. The shaded trace represents the standard error of the mean ERP. The normalized post-implantation MRI scan of each patient is shown, illustrating the exact localization of the first and second amygdala contacts. The ERPs of the innermost contact are shown in the upper panel (solid black arrows), the ERPs of the second contact in the lower panel (dotted black arrow). Note that for the first patient recorded (upper left panel), the SOA between the neutral face and the emotional face gaze cue was fixed at 500 ms. For this patient, a clearly discernable second ERP was observed in response to the emotional face (indicated by the ‘*’). All other patients were recorded with a randomly varying SOA of 400–600 ms. In the lower left part of the figure, the inset shows the grand mean of the ERPs to the neutral face, obtained by averaging all good trials across patients, on the inner and outer contacts respectively (pooling together the right and left contacts). This allows visualizing very clearly the selective neural response to the face observed around 200 ms on the inner contacts as compared with the outer ones.

Fig. 3

Amygdala responses to emotional expression and gaze changes. Illustration of group amygdala responses to the presentation of the social cue, i.e. to the emotional expression change with or without gaze aversion. The four main conditions are given in red and blue, solid or dashed lines as indicated in the legend. The effect of gaze is represented by the horizontal green bars below the neural time course. Only the right amygdala cluster resisted the cluster-based permutation that allowed correcting for multiple comparisons.