Fear and happiness in the eyes: An intra-cerebral event-related potential study from the human amygdala

We present the response pattern of intracranial event-related potentials (ERPs) recorded from depth-electrodes in the human amygdala (four patients) to faces or face parts encoding fearful, happy or neutral expressions. The amygdala showed increased amplitude ERPs (from 200 to 400 ms post-stimulus) in response to the eye region of the face compared to whole faces and to the mouth region. In particular, a strong emotional valence effect was observed, both at group and at single-subject level, with a preferential response to fearful eyes respect to every other stimulus category from 200 to 400 ms after stimulus presentation. A preferential response to smiling eyes compared to happy faces and smiling mouths was also observed at group level from 300 to 400 ms post-stimulus presentation. A complementary time–frequency analysis was performed showing that an increase in the theta frequency band (4–7 Hz) accounted for the main event-related band power (ERBP) change during the 200–500 ms post stimulus interval. The analysis of the ERBPs changes according to their emotional valence showed a strong increase in theta ERBP to fearful eyes, which was higher respect to any other facial stimulus. Moreover, theta ERBP increase to “smiling eyes” was larger respect with that evoked by smiling mouths and whole happy faces. Minimal post-stimulus ERBPs changes were evoked by neutral stimuli. These data are consistent with a special role of the amygdala in processing facial signals, both with negative and positive valence, conveyed by the eye region of the face.

► Amygdala presents a preferential response to eyes expressing fear and joy.
► Preferential response to fearful eyes respect to every other stimulus category was observed from 200 to 400 ms after stimulus presentation.
► Increase in the theta band accounts for the main changes in amygdala field potentials.
► Data support a special role of the amygdala in processing emotions conveyed by the eye region of the face.