Distributed Neural Activity Patterns during Human-to-Human Competition

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.

Real-Time Eye-to-Eye Contact Is Associated With Cross-Brain Neural Coupling in Angular Gyrus

“…Functional NIRS signal acquisition, optode localization, and signal processing, including global mean removal, were similar to methods described previously (Noah et al, 2015(Noah et al, , 2017Zhang et al, 2016Zhang et al, , 2017Piva et al, 2017;Dravida et al, 2018;Hirsch et al, 2018) and are summarized below. To assure that all participants provided recordable hemodynamic signals using fNIRS prior to participation in this experiment, subjects who demonstrated a significant fNIRS signal (p < 0.05) in the left motor cortex for both OxyHb and deOxyHb signals were eligible to participate in the present study.…”

“…Evidence for coherence between neural circuits across partners has been observed during coordinated button pressing (Funane et al, 2011;Dikker et al, 2014); coordinated singing and humming (Osaka et al, 2014(Osaka et al, , 2015; gestural communication (Schippers et al, 2010); cooperative memory tasks (Dommer et al, 2012); and face-to-face unstructured dialogue (Jiang et al, 2012). Cross-brain coherence has also been previously shown to increase during live face-to-face interactions between dyads engaged in poker competitions in contrast to human-to-computer partners (Piva et al, 2017) in which crossbrain coherence specific to the human-to-human condition was observed between the angular gyrus (AG; a part of the TPJ) and occipito-temporal area, including the lateral aspect of the occipital and temporal lobes. This finding suggests a functional role for AG and face processing areas in coherent social interaction associated with face and eye processing and motivates the current investigation.…”

Optimization of wavelet coherence analysis as a measure of neural synchrony during hyperscanning using functional near-infrared spectroscopy

“…1,34 Observations of neural coupling during interactive tasks have become a cornerstone for an emerging theoretical framework of dynamic cross-brain neural processes. 2,[10][11][12]25,[35][36][37][38][39][40] Although the evidence for the association of cross-brain signal coherence and behavioral synchrony is abundant, the underlying mechanisms for interpersonal behavioral attunement are topics of active investigation. The dyadic frame of reference provides a computational platform for hypothesis testing related to models of behavioral synchrony.…”

“…3(b)]. In this paper, as well as in previous publications, [10][11][12] coherence data were averaged along the time domain to obtain a measure of average coherence:…”

“…As such, wavelets have been proposed for revealing coupled neural processes between interacting dyads where shared social signals are transient and spontaneous. In particular, cross-brain neural synchrony measured with wavelet coherence analysis has been applied to investigate interactive behaviors, such as cooperative and competitive gameplay, 2-4 synchronized finger tapping, 5 unstructured conversation, 6 dyadic singing and humming, 7 button-pressing, 8 creative problem solving, 9 face-to-face interaction, 10 structured talking and listening, 11 playing poker against a human or computer opponent, 12 judging intentions and fairness in economic exchanges, 13 and following and leading. 14,15 Although the wavelet coherence computations have been applied previously in these and other applications, the computational factors that affect the power of the analysis have not been explored for fNIRS signals.…”