The Human Dynamic Clamp reveals the fronto-parietal network linking real-time social coordination and cognition

Abstract

How does the brain allow us to interact with others, and above all how does it handle situations when the goals of the interactors overlap (i.e. cooperation) or differ (i.e. competition)? Social neuroscience has already provided some answers to these questions but has tended to treat high-level, cognitive interpretations of social behavior separately from the sensorimotor mechanisms upon which they rely. The goal here is to identify the underlying neural processes and mechanisms linking sensorimotor coordination and intention attribution. We combine the Human Dynamic Clamp (HDC), a novel paradigm for studying realistic social behavior between self and other in well-controlled laboratory conditions, with high resolution electroencephalography (EEG). The collection of humanness and intention attribution reports, kinematics and neural data affords an opportunity to relate brain activity to the behavior of the HDC as well as to what the human is doing. Behavioral results demonstrate that sensorimotor coordination influences judgements of cooperativeness and humanness. Analysis of brain dynamics reveals two distinct networks related to integration of visuo-motor information from self and other. The two networks overlap over the right parietal region, an area known to be important for interpersonal motor interactions. Furthermore, connectivity analysis highlights how the judgement of humanness and cooperation of others modulate the connection between the right parietal hub and prefrontal cortex. These results reveal how distributed neural dynamics integrates information from low-level sensorimotor mechanisms and high-level social cognition to support the realistic social behaviors that play out in real time during interactive scenarios.\n\nSignificance StatementDaily social interactions require us to coordinate with others and to reflect on their potential motives. This study investigates the brain and behavioral dynamics of these two key aspects of social cognition. Combining high-density electroencephalography and the Human Dynamic Clamp (a Virtual Partner endowed with human-based coordination dynamics), we show first, that several features of sensorimotor coordination influence attribution of intention and judgement of humanness; second, that the right parietal lobe is a key integration hub between information related to self- and other-behavior; and third, that the posterior online social hub is functionally coupled to anterior offline brain structures to support mentalizing about others. Our results stress the complementary nature of low-level and high-level mechanisms that underlie social cognition.