What Makes Eye Contact Special? Neural Substrates of On-Line Mutual Eye-Gaze

A Hyperscanning fMRI Study

Takahiko Koike, Motofumi Sumiya, Eri Nakagawa, Shuntaro Okazaki, Norihiro Sadato

    Research output: Contribution to journalArticle

    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 study involving on-line (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 insular cortex (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.

    Original languageEnglish
    JournaleNeuro
    Volume6
    Issue number1
    DOIs
    Publication statusPublished - 2019 Jan 1

    Fingerprint

    Gyrus Cinguli
    Magnetic Resonance Imaging
    Limbic System
    Cerebral Cortex
    Cerebellum
    Noise
    Interpersonal Relations
    Multivariate Analysis

    Keywords

    • automatic mimicry
    • eye contact
    • fMRI
    • mirror neurons
    • shared attention

    ASJC Scopus subject areas

    • Neuroscience(all)

    Cite this

    What Makes Eye Contact Special? Neural Substrates of On-Line Mutual Eye-Gaze : A Hyperscanning fMRI Study. / Koike, Takahiko; Sumiya, Motofumi; Nakagawa, Eri; Okazaki, Shuntaro; Sadato, Norihiro.

    In: eNeuro, Vol. 6, No. 1, 01.01.2019.

    Research output: Contribution to journalArticle

    Koike, Takahiko ; Sumiya, Motofumi ; Nakagawa, Eri ; Okazaki, Shuntaro ; Sadato, Norihiro. / What Makes Eye Contact Special? Neural Substrates of On-Line Mutual Eye-Gaze : A Hyperscanning fMRI Study. In: eNeuro. 2019 ; Vol. 6, No. 1.
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