Brain bases of real-time social interaction: A meta-analytic investigation of human neuroimaging studies

Abstract

INTRODUCTION: Social interactions play a central role in shaping brain function, but neuroscientific research on interactive social behavior has been limited by the restrictions of brain imaging environments. Although a growing body of neuroimaging research situates participants in real-time social interactive contexts, questions remain about the brain systems critical for understanding social interaction. This study addresses three primary questions: 1) Is there a common network of brain regions that underlies diverse forms of social interaction? 2) Are there dissociable brain systems that contribute to different aspects of social interactive behavior? 3) What are the brain networks and cognitive functions associated with the socially interactive brain? METHODS: We implemented a systematic search of the human neuroimaging literature to find studies involving social interaction – participants were socially engaged and interacted with perceived social partners in real-time – that contrasted against non-socially interactive control conditions. We used coordinate-based meta-analysis (CBMA) of 108 studies to elucidate common social interaction brain regions. We further analyzed subsets of studies to probe social engagement with a human (versus non-human) partner, interactive (versus non-interactive) social contexts, and reciprocal initiating (participant elicits a response from a partner) and responding (to partners actions). Finally, we used the Brainmap and Neurosynth databases to conduct meta-analytic coactivation modeling (MACM) and functional decoding to better characterize the neurocognitive systems associated with social interaction. RESULTS: The overarching CBMA uncovered significant convergence in ten brain areas that cut across different large-scale brain networks. Follow-up analyses suggest that regions of the reward system contribute to perceived social engagement, regions of the ventral attention network are associated with reciprocal interaction, and partially dissociable brain systems relate to initiating and responding behaviors. MACM and functional decoding results suggest that 3-4 overlapping neurocognitive systems underlie social interaction: default mode network (temporoparietal junction, medial prefrontal cortex, precuneus, and cerebellum); lateral frontoparietal regions associated with cognitive control processes; and intermediary midcingulo-insular areas that are associated with reward and emotion. DISCUSSION: The current study used a data-driven investigation of the neuroimaging literature to advance our understanding of the neural and cognitive systems critical for human social interaction. Our findings suggest that the myriad forms of social interaction may be subserved by a common network of brain areas that traverse multiple neurocognitive systems and adds support to emerging theories proposing the centrality of social interaction in human brain function.