The role of gamma interbrain synchrony in social coordination when humans face territorial threats

Social Cognitive and Affective Neuroscience, 2017, 1614–1623 doi: 10.1093/scan/nsx093 Advance Access Publication Date: 27 July 2017 Original article The role of gamma interbrain synchrony in social coordination when humans face territorial threats Yan Mu,1 Shihui Han,2 and Michele J. Gelfand1 1 Department of Psychology, University of Maryland, College Park, MD 20742, USA, and 2School of Psychological and Cognitive Sciences, PKU-IDG/McGovern Institute for Brain Research, Beijing Key Laboratory of Behavior and Mental Health, Peking University, Beijing, 100080, China Correspondence should be addressed to Michele J. Gelfand and Yan Mu, Department of Psychology, University of Maryland, College Park, MD 20742, USA. E-mail: ; Abstract Throughout history and into the modern era, human groups have been continually subjected to a wide range of societal threats, from natural disasters to pandemics to terrorism. Yet despite this fundamental aspect of human existence, there has been little research on how societal threat affects social coordination at both the neural and the behavioral level. Here, we show for the first time that individuals are better able to coordinate under high societal threat as compared to low or no threat (Experiment 1). Using a method of hyperscanning electroencephalography (EEG), which simultaneously measures brain activity among interacting subjects, we further illustrate that interbrain synchrony of gamma band oscillations is enhanced when people are under high threat, and increased gamma interbrain synchrony is associated with lower dyadic interpersonal time lag (i.e. higher coordination) (Experiment 2). To our knowledge, the current work provides some of the first empirical evidence that gamma interbrain synchrony is associated with social coordination when humans are under threat. Key words: threat; coordination; brain synchrony; EEG; hyperscanning; gamma Introduction In the course of our 200,000-year history, humans have been subjected to numerous threats to our survival, including ecological threats such as natural disasters, resource scarcity and pathogens, as well as human-made threats like territorial invasions. In the 21st century, threats to human groups, from climate change to pandemics to terrorism, continue unabated. Yet surprisingly, there has been little research on the behavioral or neural mechanisms through which humans coordinate under high societal threat. From an evolutionary point of view, the ability of humans to effectively synchronize their actions under threat would presumably confer an important survival advantage (Roos et al., 2015). To address this question, we combine state of the art hyperscanning techniques with exposure to real-world threat. Hyperscanning techniques, which record multiple brains’ neural activity simultaneously with great precision as humans interact over time (Montague, 2002; Dumas et al., 2011; Burgess, 2013), are perfectly situated to elucidate the interbrain mechanisms underlying social coordination under high societal threat. Accumulating hyperscanning eletroenthephalograph (EEG) studies have indeed shown that interbrain synchrony plays a critical role in various forms of human coordination, such as the ability to synchronize body movements (Dumas et al, 2010) and speech rhythms (Kawasaki et al., 2013) and to perform duets (Sänger et al., 2013). We complement previous research by examining the role interbrain synchrony plays in coordination when humans are under threat. Using a coordination game validated in previous research (Mu et al., 2016), in Experiment 1, we examined whether dyads exposed to ingroup threat (IGT) would exhibit greater coordination as compared to dyads exposed to outgroup threat (OGT) or no threat control conditions (IGC). Received: 31 December 2016; Revised: 29 June 2017; Accepted: 20 July 2017 C The Author (2017). Published by Oxford University Press. V This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/ licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact 1614 Y. Mu et al. In Experiment 2, we combined hyperscanning EEG with the same threat manipulation (i.e. IGT, OGT and IGC) and the same coordination game employed in Experiment 1 to investigate whether interbrain synchrony would help humans coordinate under conditions of high societal threat. Using a dual-EEG setup, we tested how societal threat influences interbrain synchrony while participants attempted to coordinate. Previous hyperscanning EEG studies have shown that alpha interbrain synchrony is activated in a variety of social coordination tasks, including interactional synchrony (Dumas et al., 2010), coordinated teamwork (Astolfi et al., 2012) and synchronized counting (Mu et al., 2016). Thus, we examined whether alpha interbrain synchrony would be recruited to support social coordination in an unexplored context, namely that of societal threat. We also examined other bands of interbrain synchrony which may be particularly relevant to social coordination under threat—most notably gamma band, a high frequency band (>28 Hz) that is a threat-sensitive neural marker. In particular, single brain analyses have shown that gamma band oscillations contribute to threat detection, reflecting the involvement of a quick subcortical route to the amygdala(Luo et al., 2007), which plays a central role in processing threat-related stimuli, such as fearful images (Adolphs et al., 1994; Coccaro et al., 2007) and threat-related words (Isenberg et al., 1999). Gamma activity is also higher in anxiety disorder patients who experience chronic fear (Oathes et al., 2008). Thus, if threat affects interpersonal coordination by modulating interbrain synchrony linked to threat processing, we would expect that gamma band synchrony may be associated with human coordination under threat. Experiment 1 Method Participants. Ninety graduate and undergraduate college students at a Chinese university (mean age ¼ 23.2 years, range: 18–31 years; 44 males) were recruited online for a laboratory study and were paid for their participation. Same-gender dyads were formed in the lab and were assigned to one of three threat conditions: ingroup threat, outgroup threat and ingroup control (15 dyads per condition, see below for more details on the threat manipulations). According to previous research (Mu et al., 2016), the sample size (N ¼ 90) was adequate for testing the effects of threat on social coordination. To control for individual differences, we assessed participants’ political ideology on a scale from 1 (Very Liberal) to 7 (Very Conservative). Subjective socioeconomic status was also assessed using McArthur’s SelfAnchoring Scale (Adler et al., 2000). No differences in age, political ideology, or socioeconomic status (...truncated)