Frontal temporal and parietal systems synchronize within and across brains during live eye-to-eye contact

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Abstract

Human eye-to-eye contact is a primary source of social cues and communication. In spite of the biological significance of this interpersonal interaction, the underlying neural processes are not well-understood. This knowledge gap, in part, reflects limitations of conventional neuroimaging methods, including solitary confinement in the bore of a scanner and minimal tolerance of head movement that constrain investigations of natural, two-person interactions. However, these limitations are substantially resolved by recent technical developments in functional near-infrared spectroscopy (fNIRS), a non-invasive spectral absorbance technique that detects changes in blood oxygen levels in the brain by using surface-mounted optical sensors. Functional NIRS is tolerant of limited head motion and enables simultaneous acquisitions of neural signals from two interacting partners in natural conditions. We employ fNIRS to advance a data-driven theoretical framework for two-person neuroscience motivated by the Interactive Brain Hypothesis which proposes that interpersonal interaction between individuals evokes neural mechanisms not engaged during solo, non-interactive, behaviors. Within this context, two specific hypotheses related to eye-to-eye contact, functional specificity and functional synchrony, were tested. The functional specificity hypothesis proposes that eye-to-eye contact engages specialized, within-brain, neural systems; and the functional synchrony hypothesis proposes that eye-to-eye contact engages specialized, across-brain, neural processors that are synchronized between dyads. Signals acquired during eye-to-eye contact between partners (interactive condition) were compared to signals acquired during mutual gaze at the eyes of a picture-face (non-interactive condition). In accordance with the specificity hypothesis, responses during eye-to-eye contact were greater than eye-to-picture gaze for a left frontal cluster that included pars opercularis (associated with canonical language production functions known as Broca's region), pre- and supplementary motor cortices (associated with articulatory systems), as well as the subcentral area. This frontal cluster was also functionally connected to a cluster located in the left superior temporal gyrus (associated with canonical language receptive functions known as Wernicke's region), primary somatosensory cortex, and the subcentral area. In accordance with the functional synchrony hypothesis, cross-brain coherence during eye-to-eye contact relative to eye-to-picture gaze increased for signals originating within left superior temporal, middle temporal, and supramarginal gyri as well as the pre- and supplementary motor cortices of both interacting brains. These synchronous cross-brain regions are also associated with known language functions, and were partner-specific (i.e., disappeared with randomly assigned partners). Together, both within and across-brain neural correlates of eye-to-eye contact included components of previously established productive and receptive language systems. These findings reveal a left frontal, temporal, and parietal long-range network that mediates neural responses during eye-to-eye contact between dyads, and advance insight into elemental mechanisms of social and interpersonal interactions.

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