The Human Dynamic Clamp Reveals the Fronto-Parietal Network Linking Real-Time Social Coordination and Cognition.

J A S Kelso,E Tognoli,Q Moreau,G Dumas

doi:10.1093/cercor/bhz308

Abstract

How does the brain allow us to interact with others? 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, a novel paradigm for studyingrealistic social behavior, with high-resolution electroencephalography. The collection of humanness and intention attribution reports, kinematics, and neural data affords an opportunity to relate brain activity to the ongoing social behavior. Behavioral results demonstrate that sensorimotor coordination influences the judgments of cooperativeness and humanness. Analysis of brain dynamics reveals two distinct networks related to the integration of visuo-motor information from self and other which overlap over the right parietal region. Furthermore, judgment of humanness and cooperation of others modulate the functional connectivity between this right parietal hub and the 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.

Highlights

Much of our social life consists of interactions with others
How does the brain allow us to interact with others? 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 present study used the human dynamic clamp (HDC) to investigate the neural underpinnings of social interaction and in particular how the brain integrates its own behavior with that of others to support the attribution of humanness and intention

Summary

Introduction

Much of our social life consists of interactions with others. Despite their essential role, social interactions still remain the “dark matter” of social neuroscience: the field is in urgent need of studies that embrace the reciprocal and real-time nature of social coordination (Hari and Kujala 2009; Dumas 2011; Hasson et al 2012; Konvalinka and Roepstorff 2012; Schilbach et al 2013; Hari et al 2015). Overcoming the methodological challenge of bringing a true interactive context into the laboratory, some innovations have allowed behavioral tracking, brain recording, and stimulation of multiple participants in interaction (Montague et al 2002; Babiloni et al 2006; Tognoli et al 2007; Dumas et al 2010; Funane et al 2011; Moreau et al 2016; Chen et al 2017; Dikker et al 2017; Hirsch et al 2017; Novembre et al 2017; Era et al 2018b). A nonexclusive list includes visual cortices such as lateral occipito-temporal cortex (Lingnau and Downing 2015) and superior temporal sulcus (STS; Chauvigné et al 2018), the parietal lobe including the intra parietal sulcus and the temporo-parietal junction (TPJ; Chauvigné et al 2018), and frontal motor areas comprising the primary motor cortex (M1; Kilner et al 2007), the premotor cortex, and the supplementary motor area, and the anterior cingulate cortex (Apps et al 2016) and the prefrontal cortex (Shaw et al 2018; cf., Fig. 1)

Methods

Discussion

Conclusion