What makes eye contact special? Neural substrates of on-line mutual eye-gaze: a hyperscanning fMRI study

Abstract

Automatic mimicry is a critical element of social interaction. A salient type of automatic mimicry is eye contact characterized by sharing of affective and mental states among individuals. We conducted a hyperscanning functional magnetic resonance imaging (fMRI) study involving online (LIVE) and delayed off-line (REPLAY) conditions to test our hypothesis that recurrent interaction through eye contact activates the limbic mirror system, including the anterior cingulate cortex (ACC) and anterior insula (AIC), both of which are critical for self-awareness. Sixteen pairs of human adults participated in the experiment. Given that an eye-blink represents an individual’s attentional window toward the partner, we analyzed pairwise time-series data for eye-blinks. We used multivariate autoregression analysis to calculate the noise contribution ratio (NCR) as an index of how a participant’s directional attention was influenced by that of their partner. NCR was greater in the LIVE than in the REPLAY condition, indicating mutual perceptual–motor interaction during real-time eye contact. Relative to the REPLAY condition, the LIVE condition was associated with greater activation in the left cerebellar hemisphere, vermis, and ACC, accompanied by enhanced functional connectivity between ACC and right AIC. Given the roles of the cerebellum in sensorimotor prediction and ACC in movement initiation, ACC–cerebellar activation may represent their involvement in modulating visual input related to the partner’s movement, which may, in turn, involve the limbic mirror system. Our findings indicate that mutual interaction during eye contact is mediated by the cerebellum and limbic mirror system.

Significance Statement Eye contact is a key element that connects humans during social communication. We focused on a previously unaddressed characteristic of eye contact: real-time mutual interaction as a form of automatic mimicry. Our results indicate that real-time interaction during eye contact is mediated by the cerebellum and limbic mirror system. These findings underscore the importance of the mirror system and cerebellum in real-time unconscious social interaction.