Amygdala damage impairs eye contact during conversations with real people

Abstract

The role of the human amygdala in real social interactions remains essentially unknown, although studies in nonhuman primates and studies using photographs and video in humans have shown it to be critical for emotional processing and suggest its importance for social cognition. We show here that complete amygdala lesions result in a severe reduction in direct eye contact during conversations with real people, together with an abnormal increase in gaze to the mouth. These novel findings from real social interactions are consistent with an hypothesized role for the amygdala in autism and the approach taken here opens up new directions for quantifying social behavior in humans.

Figure 1.

Experimental setup. a, In the face-to-face paradigm, the actor (left) is shown seated across from the participant (right), who is wearing the eye tracker. b, In the live video setup, the actor (on screen) is shown over one-way live video so that the participant can see and hear the actor, although the actor can only hear, but not see, the participant.

Figure 2.

Fixations made during naturalistic social interaction. a–d, Color encodes the normalized number of fixations (see bar at bottom right). The number of fixations S.M. (a, c) and five controls (b, d) made to regions of the face during face-to-face conversations with the actor (N.A.), either face-to-face (a, b) or over live video (c, d), is shown. e, Proportion of time spent fixating facial features in the face-to-face (F) and live video (V) conditions, as well as during face-to-face interaction with a familiar person (one of the experimenters, R.A.). Values for the eyes (middle) and mouth (right) were normalized with respect to overall gaze to the face (left). Red circles, S.M.; green circles, five matched controls; filled black circles, comparison group of 21 younger participants (means and SDs). Across all conditions and compared with all subject groups, S.M. made an abnormally large number of fixations on the mouth and an abnormally small number of fixations on the eyes.