Brain-to-Brain Synchrony Tracks Real-World Dynamic Group Interactions in the Classroom

The human brain has evolved for group living [1Dunbar I.R. The social brain hypothesis.in: Cacioppo J.T. Foundations in Social Neuroscience. MIT Press, 2002: 69-88Google Scholar]. Yet we know so little about how it supports dynamic group interactions that the study of real-world social exchanges has been dubbed the “dark matter of social neuroscience” [2Schilbach L. Timmermans B. Reddy V. Costall A. Bente G. Schlicht T. Vogeley K. Toward a second-person neuroscience.Behav. Brain Sci. 2013; 36: 393-414Crossref PubMed Scopus (890) Google Scholar]. Recently, various studies have begun to approach this question by comparing brain responses of multiple individuals during a variety of (semi-naturalistic) tasks [3Babiloni F. Astolfi L. Social neuroscience and hyperscanning techniques: past, present and future.Neurosci. Biobehav. Rev. 2014; 44: 76-93Crossref PubMed Scopus (289) Google Scholar, 4Dmochowski J.P. Bezdek M.A. Abelson B.P. Johnson J.S. Schumacher E.H. Parra L.C. Audience preferences are predicted by temporal reliability of neural processing.Nat. Commun. 2014; 5: 4567Crossref PubMed Scopus (164) Google Scholar, 5Dumas G. Nadel J. Soussignan R. Martinerie J. Garnero L. Inter-brain synchronization during social interaction.PLoS ONE. 2010; 5: e12166Crossref PubMed Scopus (495) Google Scholar, 6Hasson U. Ghazanfar A.A. Galantucci B. Garrod S. Keysers C. Brain-to-brain coupling: a mechanism for creating and sharing a social world.Trends Cogn. Sci. 2012; 16: 114-121Abstract Full Text Full Text PDF PubMed Scopus (545) Google Scholar, 7Hari R. Himberg T. Nummenmaa L. Hämäläinen M. Parkkonen L. Synchrony of brains and bodies during implicit interpersonal interaction.Trends Cogn. Sci. 2013; 17: 105-106Abstract Full Text Full Text PDF PubMed Scopus (67) Google Scholar, 8Jiang J. Chen C. Dai B. Shi G. Ding G. Liu L. Lu C. Leader emergence through interpersonal neural synchronization.Proc. Natl. Acad. Sci. USA. 2015; 112: 4274-4279Crossref PubMed Scopus (168) Google Scholar, 9Pfeiffer U.J. Timmermans B. Vogeley K. Frith C.D. Schilbach L. Towards a neuroscience of social interaction.Front. Hum. Neurosci. 2013; 7: 22Crossref PubMed Scopus (30) Google Scholar, 10Stephens G.J. Silbert L.J. Hasson U. Speaker-listener neural coupling underlies successful communication.Proc. Natl. Acad. Sci. USA. 2010; 107: 14425-14430Crossref PubMed Scopus (546) Google Scholar, 11Babiloni C. Buffo P. Vecchio F. Marzano N. Del Percio C. Spada D. Rossi S. Bruni I. Rossini P.M. Perani D. Brains “in concert”: frontal oscillatory alpha rhythms and empathy in professional musicians.Neuroimage. 2012; 60: 105-116Crossref PubMed Scopus (84) Google Scholar, 12Duan L. Dai R.N. Xiao X. Sun P.P. Li Z. Zhu C.Z. Cluster imaging of multi-brain networks (CIMBN): a general framework for hyperscanning and modeling a group of interacting brains.Front. Neurosci. 2015; 9: 267Crossref PubMed Scopus (28) Google Scholar, 13Hasson U. Nir Y. Levy I. Fuhrmann G. Malach R. Intersubject synchronization of cortical activity during natural vision.Science. 2004; 303: 1634-1640Crossref PubMed Scopus (1063) Google Scholar, 14Nummenmaa L. Glerean E. Viinikainen M. Jääskeläinen I.P. Hari R. Sams M. Emotions promote social interaction by synchronizing brain activity across individuals.Proc. Natl. Acad. Sci. USA. 2012; 109: 9599-9604Crossref PubMed Scopus (287) Google Scholar, 15Dikker S. Silbert L.J. Hasson U. Zevin J.D. On the same wavelength: predictable language enhances speaker-listener brain-to-brain synchrony in posterior superior temporal gyrus.J. Neurosci. 2014; 34: 6267-6272Crossref PubMed Scopus (71) Google Scholar]. These experiments reveal how stimulus properties [13Hasson U. Nir Y. Levy I. Fuhrmann G. Malach R. Intersubject synchronization of cortical activity during natural vision.Science. 2004; 303: 1634-1640Crossref PubMed Scopus (1063) Google Scholar], individual differences [14Nummenmaa L. Glerean E. Viinikainen M. Jääskeläinen I.P. Hari R. Sams M. Emotions promote social interaction by synchronizing brain activity across individuals.Proc. Natl. Acad. Sci. USA. 2012; 109: 9599-9604Crossref PubMed Scopus (287) Google Scholar], and contextual factors [15Dikker S. Silbert L.J. Hasson U. Zevin J.D. On the same wavelength: predictable language enhances speaker-listener brain-to-brain synchrony in posterior superior temporal gyrus.J. Neurosci. 2014; 34: 6267-6272Crossref PubMed Scopus (71) Google Scholar] may underpin similarities and differences in neural activity across people. However, most studies to date suffer from various limitations: they often lack direct face-to-face interaction between participants, are typically limited to dyads, do not investigate social dynamics across time, and, crucially, they rarely study social behavior under naturalistic circumstances. Here we extend such experimentation drastically, beyond dyads and beyond laboratory walls, to identify neural markers of group engagement during dynamic real-world group interactions. We used portable electroencephalogram (EEG) to simultaneously record brain activity from a class of 12 high school students over the course of a semester (11 classes) during regular classroom activities (Figures 1A–1C; Supplemental Experimental Procedures, section S1). A novel analysis technique to assess group-based neural coherence demonstrates that the extent to which brain activity is synchronized across students predicts both student class engagement and social dynamics. This suggests that brain-to-brain synchrony is a possible neural marker for dynamic social interactions, likely driven by shared attention mechanisms. This study validates a promising new method to investigate the neuroscience of group interactions in ecologically natural settings.

Brain-to-Brain Synchrony Tracks Real-World Dynamic Group Interactions in the Classroom | Litlas