THE NEW NEUROSCIENCE OF “TWO”: COMMUNICATING EYE-TO-EYE.

Human brains are primarily adapted for social interaction and communication. However, the underlying neural processes associated with social interaction and communication are not well-understood. This knowledge gap reflects both conventional limitations in neuroimaging methods that are restricted to single individuals and not conducive to investigations of naturally occurring human interactions, and also a limited theoretical framework for understanding human interpersonal interactions. Both are addressed by recent developments that include: 1) a novel hyperscanning technology (functional near-infrared spectroscopy, fNIRS) that acquires hemodynamic signals simultaneously between two naturally interacting partners using a spectral absorbance technique that detects changes in hemodynamic signals acquired by surface-mounted optodes, and 2) a recently proposed Interactive Brain Hypothesis that establishes a broad theoretical framework for two-person social neuroscience. This hypothesis is based on the assumptions that two-way communications elicit specific neural processes some of which will synchronize across interacting brains. Here I present evidence for these assumptions based on two social behaviors, eye-to-eye contact and verbal dialogue. Hemodynamic signals associated with eye-to-eye contact between partners (interactive condition) were compared with signals associated with mutual gaze at eyes in a picture of a face (non-interactive condition). Similar signals for picture naming and description in a dialogue (interactive) condition were compared with picture-naming and description in a monologue (non-interactive) condition. Consistent with the Interactive Brain Hypothesis, both eye-to-eye contact effects and dialogue effects were observed in a left frontal and temporal-parietal complex including the canonical language system. Further, cross-brain synchrony observed by wavelet analysis in the interactive conditions was observed for the temporal-parietal complex. These findings are consistent with the Interactive Brain Hypothesis and suggest a model of neural specializations for communication that links eye-to-eye contact and language systems via frontal, central, and temporal-parietal networks.