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Front. Hum. Neurosci. | doi: 10.3389/fnhum.2017.00571

Distributed neural activity patterns during human-to-human competition

  • 1Interdepartmental Neuroscience Program, Yale University, United States
  • 2Department of Psychiatry, Yale School of Medicine, Yale University, United States
  • 3Department of Psychology, Yale University, United States
  • 4Department of Neuroscience, Yale School of Medicine, Yale University, United States
  • 5Department of Comparative Medicine, Yale School of Medicine, Yale University, United States
  • 6Department of Medical Physics and Biochemistry, University College London, United Kingdom

Interpersonal interaction is the essence of human social behavior. However, conventional neuroimaging techniques have tended to focus on social cognition in single individuals rather than on dyads or groups. As a result, relatively little is understood about the neural events that underlie face-to-face interaction. We resolved some of the technical obstacles inherent in studying interaction using a novel imaging modality and aimed to identify neural mechanisms engaged both within and across brains in an ecologically valid instance of interpersonal competition. Functional near-infrared spectroscopy was utilized to simultaneously measure hemodynamic signals representing neural activity in pairs of subjects playing poker against each other (human-human condition) or against computer opponents (human-computer condition). Previous fMRI findings concerning single subjects confirm that neural areas recruited during social cognition paradigms are individually sensitive to human-human and human-computer conditions. However, it is not known whether face-to-face interactions between opponents can extend these findings. We hypothesize distributed effects due to live processing and specific variations in across-brain coherence not observable in single-subject paradigms. Angular gyrus (AG), a component of the temporal-parietal junction (TPJ) previously found to be sensitive to socially relevant cues, was selected as a seed to measure within-brain functional connectivity. Increased connectivity was confirmed between AG and bilateral dorsolateral prefrontal cortex (dlPFC) as well as a complex including the left subcentral area (SCA) and somatosensory cortex (SS) during interaction with a human opponent. These distributed findings were supported by contrast measures that indicated increased activity at the left dlPFC and frontopolar area (FA) that partially overlapped with the region showing increased functional connectivity with AG. Across-brain analyses of neural coherence between the players revealed synchrony between dlPFC and supramarginal gyrus (SMG) and SS in addition to synchrony between AG and the fusiform gyrus (FG) and SMG. These findings present the first evidence of a frontal-parietal neural complex including the TPJ, dlPFC, SCA, SS, and FG that is more active during human-to-human social cognition both within brains (functional connectivity) and across brains (across-brain coherence), supporting a model of functional integration of socially and strategically relevant information during live face-to-face competitive behaviors.

Keywords: social interaction, temporal-parietal junction, functional near-infrared spectroscopy, hyperscanning, connectivity, coherence

Received: 19 Jul 2017; Accepted: 10 Nov 2017.

Edited by:

Mark A. Williams, Macquarie University, Australia

Reviewed by:

Iku Nemoto, Tokyo Denki University, Japan
Matthew S. Shane, University of Ontario Institute of Technology, Canada  

Copyright: © 2017 Piva, Zhang, Noah, Chang and Hirsch. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

* Correspondence: Dr. Joy Hirsch, Yale School of Medicine, Yale University, Department of Psychiatry, New Haven, United States, joy.hirsch@yale.edu