Abstract
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 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.
Highlights
The dyadic neuroimaging literature far has established that cooperative and communicative behaviors are associated with across-brain coherence using a neuroimaging strategy called hyperscanning, which involves the imaging of two interacting individuals simultaneously (Montague et al, 2002)
The impact of an opponent’s previous decision on a given player’s current decision as determined using an N-1 analysis indicated that z-scores of the cross-correlation coefficients in the human– human condition (r = 0.19) and the human–computer condition (r = 0.07) varied [Figure 2A; cross-correlation coefficients calculated between an opponent’s immediately previous decision and a player’s current decision shown for the human–human and human–computer conditions on the y-axis; t(38) = 2.1, P = 3E-02, paired-sample t-test]. This demonstrated that subjects were more influenced by an opponent’s previous decision when playing against human rather than computer opponents and indicated a difference in the influence of a human opponent on a given player’s decision
Neural differences in patterns of activity and functional connectivity within brains as well as coherence across two interacting brains could represent the neural correlates of the specific difference in the influence of immediate choice history observed between the human–human and human–computer conditions
Summary
The dyadic neuroimaging literature far has established that cooperative and communicative behaviors are associated with across-brain coherence using a neuroimaging strategy called hyperscanning, which involves the imaging of two interacting individuals simultaneously (Montague et al, 2002). Increased coherence in the neural activity between partners was found in the superior frontal cortex only during cooperation (Cui et al, 2012) These findings were independently replicated in a study that found divergent activity between female–female, male–male, and female–male pairs that seemed to correlate with differences in task performance (Cheng et al, 2015). This paradigm has more recently been used to show increased coherence in superior frontal cortex between lovers compared to between pairs of friends or strangers (Pan et al, 2017). Other similar paradigms have shown increased synchrony between the dorsomedial prefrontal cortices of interacting partners during cooperation (Liu et al, 2016)
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