In social interactions, each individual's brain drives an action that, in turn, elicits systematic neural responses in their partner that drive a reaction. Consequently, the brain responses of both interactants become temporally contingent upon one another through the actions they generate, and different interaction dynamics will be underpinned by distinct forms of between-brain coupling. In this study, we investigated this by "performing functional magnetic resonance imaging on two individuals simultaneously (dual-fMRI) while they competed or cooperated with one another in a turn-based or concurrent fashion." To assess whether distinct patterns of neural coupling were associated with these different interactions, we combined two data-driven, model-free analytical techniques: group-independent component analysis and inter-subject correlation. This revealed four distinct patterns of brain responses that were temporally aligned between interactants: one emerged during co-operative exchanges and encompassed brain regions involved in social cognitive processing, such as the temporo-parietal cortex. The other three were associated with competitive exchanges and comprised brain systems implicated in visuo-motor processing and social decision-making, including the cerebellum and anterior cingulate cortex. Interestingly, neural coupling was significantly stronger in concurrent relative to turn-based exchanges. These results demonstrate the utility of data-driven approaches applied to "dual-fMRI" data in elucidating the interpersonal neural processes that give rise to the two-in-one dynamic characterizing social interaction.

Behavioural and Social Neuroscience Research Group CEITEC Central European Institute of Technology Masaryk University Brno Czech Republic

Department of Neurology Faculty of Medicine Masaryk University Brno Czech Republic

Department of Psychology School of Life and Health Sciences Aston University Birmingham UK

Muiltomodal and Functional Neuroimaging Laboratory CEITEC Central European Institute of Technology Masaryk University Brno Czech Republic

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Abe, M. O. , Koike, T. , Okazaki, S. , Sugawara, S. K. , Takahashi, K. , Watanabe, K. , & Sadato, N. (2019). Neural correlates of online cooperation during joint force production. NeuroImage, 191, 150–161. 10.1016/j.neuroimage.2019.02.003 PubMed DOI

Ahn, S. , Cho, H. , Kwon, M. , Kim, K. , Kwon, H. , Kim, B. S. , … Jun, S. C. (2017). Interbrain phase synchronization during turn‐taking verbal interaction‐a hyperscanning study using simultaneous EEG/MEG. Human Brain Mapping, 39(1), 171–188. 10.1002/hbm.23834 PubMed DOI PMC

Babiloni, F. , & Astolfi, L. (2014). Social neuroscience and hyperscanning techniques: past, present and future. Neuroscience & Biobehavioral Reviews, 44, 76–93. PubMed PMC

Bardi, L. , Six, P. , & Brass, M. (2017). Repetitive TMS of the temporo‐parietal junction disrupts participant's expectations in a spontaneous theory of mind task. Social Cognitive and Affective Neuroscience, 12(11), 1775–1782. 10.1093/scan/nsx109 PubMed DOI PMC

Beckmann, C. F. , & Smith, S. M. (2004). Probabilistic independent component analysis for functional magnetic resonance imaging. IEEE Transactions on Medical Imaging , 23, 137–152. PubMed

Bhaganagarapu, K. , Jackson, G. D. , & Abbott, D. F. (2013). An automated method for identifying artifact in independent component analysis of resting‐state fMRI. Frontiers in Human Neuroscience , 7(7), 1–17. PubMed PMC

Bilek, E. , Ruf, M. , Schäfer, A. , Akdeniz, C. , Calhoun, V. D. , Schmahl, C. , … Meyer‐Lindenberg, A. (2015). Information flow between interacting human brains: Identification, validation, and relationship to social expertise. Proceedings of the National Academy of Sciences, 112(16), 5207–5212. 10.1073/pnas.1421831112 PubMed DOI PMC

Bilek, E. , Stößel, G. , Schäfer, A. , Clement, L. , Ruf, M. , Robnik, L. , … Meyer‐Lindenberg, A. (2017). State‐dependent cross‐brain information flow in borderline personality disorder. JAMA psychiatry, 74(9), 949–957. PubMed PMC

Calhoun, V. D. , Adali, T. , Pearlson, G. D. , & Pekar, J. J. (2001). A method for making group inferences from functional MRI data using independent component analysis. Human brain mapping, 14(3), 140–151. PubMed PMC

Calhoun V. D., Kiehl, K. A. & Pearlson, G. D. (2008). Modulation of temporally coherent brain networks estimated using ICA at rest and during cognitive tasks. Human Brain Mapping, 29(7), 828–838. PubMed PMC

Carlson, S. M. , Koenig, M. A. , & Harms, M. B. (2013). Theory of mind. Wiley Interdisciplinary Reviews. Cognitive Science, 4(4), 391–402. 10.1002/wcs.1232 PubMed DOI

Cavanna, A. E. , & Trimble, M. R. (2006). The precuneus: a review of its functional anatomy and behavioural correlates. Brain, 129(3), 564–583. PubMed

Cheng, X. , Li, X. , & Hu, Y. (2015). Synchronous brain activity during cooperative exchange depends on gender of partner: A fNIRS‐based hyperscanning study. Human Brain Mapping, 36(6), 2039–2048. 10.1002/hbm.22754 PubMed DOI PMC

Culham, J. C. , Cavina‐Pratesi, C. , & Singhal, A. (2006). The role of parietal cortex in visuomotor control: What have we learned from neuroimaging? Neuropsychologia, 44(13), 2668–2684. 10.1016/j.neuropsychologia.2005.11.003 PubMed DOI

Decety, J. , Jackson, P. L. , Sommerville, J. A. , Chaminade, T. , & Meltzoff, A. N. (2004). Theneural bases of cooperation and competition: an fMRI investigation. NeuroImage, 23, 744–751. PubMed PMC

Dumas, G. , Martinerie, J. , Soussignan, R. , & Nadel, J. (2012). Does the brain know who is at the origin of what in an imitative interaction? Frontiers in Human Neuroscience, 6, 1–11. 10.3389/fnhum.2012.00128 PubMed DOI PMC

Dumas, G. , Nadel, J. , Soussignan, R. , Martinerie, J. , & Garnero, L. (2010). Inter‐brain synchronization during social interaction. PLoS One, 5(8), e12166 10.1371/journal.pone.0012166 PubMed DOI PMC

Dumontheil, I. , Küster, O. , Apperly, I. A. , & Blakemore, S. J. (2010). Taking perspective into account in a communicative task. Neuroimage, 52(4), 1574–1583. PubMed

Eddy, C. M. (2016). The junction between self and other? Temporo‐parietal dysfunction in neuropsychiatry. Neuropsychologia, 89, 465–477. 10.1016/j.neuropsychologia.2016.07.030 PubMed DOI

Frith, C. D. , & Frith, U. (2006). The neural basis of Mentalizing. Neuron, 50(4), 531–534. 10.1016/j.neuron.2006.05.001 PubMed DOI

Gallivan, J. P. , & Culham, J. C. (2015). Neural coding within human brain areas involved in actions. Current Opinion in Neurobiology, 33, 141–149. 10.1016/j.conb.2015.03.012 PubMed DOI

Ghaem, O. , Mellet, E. , Crivello, F. , Tzourio, N. , Mazoyer, B. , Berthoz, A. , & Denis, M. (1997). Mental navigation along memorized routes activates the hippocampus, precuneus, and insula. Neuroreport, 8(3), 739–744. PubMed

Grahn, J. A. , Parkinson, J. A. , & Owen, A. M. (2008). The cognitive functions of the caudate nucleus. Progress in Neurobiology, 86(3), 141–155. 10.1016/j.pneurobio.2008.09.004 PubMed DOI

Hampton, A. N. , Bossaerts, P. , & O'Doherty, J. P. (2008). Neural correlates of mentalizing‐related computations during strategic interactions in humans. Proceedings of the National Academy of Sciences, 105(18), 6741–6746. PubMed PMC

Hanakawa, T. , Honda, M. , Okada, T. , Fukuyama, H. , & Shibasaki, H. (2003). Neural correlates underlying mental calculation in abacus experts: a functional magnetic resonance imaging study. Neuroimage, 19(2), 296–307. PubMed

Hari, R. , Himberg, T. , Nummenmaa, L. , Hämäläinen, M. , & Parkkonen, L. (2013). Synchrony of brains and bodies during implicit interpersonal interaction. Trends in Cognitive Sciences, 17(3), 105–106. 10.1016/j.tics.2013.01.003 PubMed DOI

Hasson, U. , & Frith, C. D. (2016). Mirroring and beyond: Coupled dynamics as a generalized framework for modelling social interactions. Philosophical Transactions of the Royal Society B: Biological Sciences, 371(1693), 20150366 10.1098/rstb.2015.0366 PubMed DOI PMC

Hasson, U. , & Honey, C. J. (2012). Future trends in neuroimaging: Neural processes as expressed within real‐life contexts. NeuroImage, 62(2), 1272–1278. 10.1016/j.neuroimage.2012.02.004 PubMed DOI PMC

Hasson, U. , Nir, Y. , Levy, I. , Fuhrmann, G. , & Malach, R. (2004). Intersubject synchronization of cortical activity during natural vision. Science (New York, NY), 303(2004), 1634–1640. 10.1126/science.1089506 PubMed DOI

Himberg, J. , Hyvärinen, A. , & Esposito, F. (2004). Validating the independent components of neuroimaging time series via clustering and visualization. NeuroImage, 22(3), 1214–1222. 10.1016/j.neuroimage.2004.03.027 PubMed DOI

Hirsch, J. , Zhang, X. , Noah, J. A. , & Ono, Y. (2017). Frontal temporal and parietal systems synchronize within and across brains during live eye‐to‐eye contact. NeuroImage, 157, 314–330. 10.1016/j.neuroimage.2017.06.018 PubMed DOI PMC

Holmes, C. J. , Hoge, R. , Collins, L. , Woods, R. , Toga, A. W. , & Evans, A. C. (1998). Enhancement of MR images using registration for signal averaging. Journal of Computer Assisted Tomography, 22, 324–333. 10.1097/00004728-199803000-00032 PubMed DOI

Jahng, J. , Kralik, J. D. , Hwang, D. U. , & Jeong, J. (2017). Neural dynamics of two players when using nonverbal cues to gauge intentions to cooperate during the Prisoner's dilemma game. NeuroImage, 157, 263–274. 10.1016/j.neuroimage.2017.06.024 PubMed DOI

Jara‐Ettinger, J. , Baker, C. , & Tenenbaum, J. (2012). Learning what is where from social observations. Proceedings of the Annual Meeting of the Cognitive Science Society, 34(34), 515–520.

Jenkinson, M. , Bannister, P. R. , Brady, J. M. & Smith, S. M. (2002). Improved optimisation for the robust and accurate linear registration and motion correction of brain images. NeuroImage, 17(2), 825–841. PubMed

Jenkinson, M. , Beckmann, C. F. , Behrens, T. E. J. , Woolrich, M. W. , & Smith, S. M. (2012). FSL. NeuroImage, 62(2), 782–790. PubMed

Kasai, K. , Fukuda, M. , Yahata, N. , Morita, K. , & Fujii, N. (2015). The future of real‐world neuroscience: Imaging techniques to assess active brains in social environments. Neuroscience Research, 90, 65–71. 10.1016/j.neures.2014.11.007 PubMed DOI

Kestemont, J. , Ma, N. , Baetens, K. , Clément, N. , Van Overwalle, F. , & Vandekerckhove, M. (2015). Neural correlates of attributing causes to the self, another person and the situation. Social Cognitive and Affective Neuroscience, 10(1), 114–121. 10.1093/scan/nsu030 PubMed DOI PMC

Kestemont, J. , Vandekerckhove, M. , Ma, N. , Van Hoeck, N. , & Van Overwalle, F. (2013). Situation and person attributions under spontaneous and intentional instructions: An fMRI study. Social Cognitive and Affective Neuroscience, 8(5), 481–493. 10.1093/scan/nss022 PubMed DOI PMC

Kinreich, S. , Djalovski, A. , Kraus, L. , Louzoun, Y. , & Feldman, R. (2017). Brain‐to‐brain synchrony during naturalistic social interactions. Scientific Reports, 7(1), 17060 10.1038/s41598-017-17339-5 PubMed DOI PMC

Koike, T. , Tanabe, H. C. , & Sadato, N. (2015). Hyperscanning neuroimaging technique to reveal the “two‐in‐one” system in social interactions. Neuroscience Research, 90, 25–32. 10.1016/j.neures.2014.11.006 PubMed DOI

Konvalinka, I. , & Roepstorff, A. (2012). The two‐brain approach: How can mutually interacting brains teach us something about social interaction? Frontiers in Human Neuroscience, 6, 1–10. 10.3389/fnhum.2012.00215 PubMed DOI PMC

Lamm, C. , Bukowski, H. , & Silani, G. (2016). From shared to distinct self‐other representations in empathy: Evidence from neurotypical function and socio‐cognitive disorders. Philosophical Transactions of the Royal Society B: Biological Sciences, 371(1686), 20150083 10.1098/rstb.2015.0083 PubMed DOI PMC

Langlois, D. , Chartier, S. , & Gosselin, D. (2010). An introduction to independent component analysis: InfoMax and FastICA algorithms. Tutorials in Quantitative Methods for Psychology, 6(1), 31–38. 10.20982/tqmp.06.1.p031 DOI

Leggio, M. , & Molinari, M. (2015). Cerebellar sequencing: A trick for predicting the future. The Cerebellum, 14(1), 35–38. 10.1007/s12311-014-0616-x PubMed DOI

Lindquist, M. A. , Geuter, S. , Wager, T. D. , & Caffo, B. S. (2019). Modular preprocessing pipelines can reintroduce artifacts into fMRI data. Human brain mapping, 40(8), 2358–2376. PubMed PMC

Liu, T. , & Pelowski, M. (2014). Clarifying the interaction types in two‐person neuroscience research. Frontiers in Human Neuroscience, 8, 276 10.3389/fnhum.2014.00276 PubMed DOI PMC

Mazzarella, E. , Ramsey, R. , Conson, M. , & Hamilton, A. (2013). Brain systems for visual perspective taking and action perception. Social neuroscience, 8(3), 248–267. PubMed

Nastase, S. A. , Gazzola, V. , & Keysers, C. (2019). Measuring shared responses across subjects using intersubject correlation. Social Cognitive and Affective Neuroscience, 14(6), 667–685. 10.1101/600114 PubMed DOI PMC

Nixon, P. D. (2003). The role of the cerebellum in preparing responses to predictable sensory events. Cerebellum, 2(2), 114–122. 10.1080/14734220310011353 PubMed DOI

Pérez, A. , Carreiras, M. , & Duñabeitia, J. A. (2017). Brain‐to‐brain entrainment: EEG interbrain synchronization while speaking and listening. Scientific Reports, 7(1), 1–12. 10.1038/s41598-017-04464-4 PubMed DOI PMC

Pérez, A. , Dumas, G. , Karadag, M. , & Duñabeitia, J. A. (2019). Differential brain‐to‐brain entrainment while speaking and listening in native and foreign languages. Cortex, 111, 303–315. PubMed

Redcay, E. , & Schilbach, L. (2019). Using second‐person neuroscience to elucidate the mechanisms of social interaction. Nature Reviews Neuroscience., 20, 495–505. 10.1038/s41583-019-0179-4 PubMed DOI PMC

Rojiani, R. , Zhang, X. , Noah, A. , & Hirsch, J. (2018). Communication of emotion via drumming: Dual‐brain imaging with functional near‐infrared spectroscopy. Social Cognitive and Affective Neuroscience, 13(10), 1047–1057. 10.1093/scan/nsy076 PubMed DOI PMC

Sammut, C. , & Webb, G. I. (2016). In Sammut C. & Webb G. I. (Eds.), Encyclopedia of machine learning and data mining. Boston, MA: Springer US; 10.1007/978-1-4899-7502-7 DOI

Sänger, J. , Müller, V. , & Lindenberger, U. (2012). Intra‐ and interbrain synchronization and network properties when playing guitar in duets. Frontiers in Human Neuroscience, 6, 312 10.3389/fnhum.2012.00312 PubMed DOI PMC

Schilbach, L. , Bzdok, D. , Timmermans, B. , Fox, P. T. , Laird, A. R. , Vogeley, K. , & Eickhoff, S. B. (2012). Introspective minds: Using ALE meta‐analyses to study commonalities in the neural correlates of emotional processing, social & unconstrained cognition. PLoS One, 7(2), e30920 10.1371/journal.pone.0030920 PubMed DOI PMC

Schilbach, L. , Timmermans, B. , Reddy, V. , Costall, A. , Bente, G. , Schlicht, T. , & Vogeley, K. (2013). Toward a second‐person neuroscience. Behavioral and Brain Sciences, 36(04), 393–414. 10.1017/S0140525X12000660 PubMed DOI

Scholkmann, F. , Holper, L. , Wolf, U. , & Wolf, M. (2013). A new methodical approach in neuroscience: assessing inter‐personal brain coupling using functional near‐infrared imaging (fNIRI) hyperscanning. Frontiers in human neuroscience, 7, 813. PubMed PMC

Sebanz, N. , Bekkering, H. , & Knoblich, G. (2006). Joint action: Bodies and minds moving together. Trends in Cognitive Sciences, 10, 70–76. 10.1016/j.tics.2005.12.009 PubMed DOI

Shaw, D. J. , Czekóová, K. , Staněk, R. , Mareček, R. , Urbánek, T. , Špalek, J. , … Brázdil, M. (2018). A dual‐fMRI investigation of the iterated ultimatum game reveals that reciprocal behaviour is associated with neural alignment. Scientific Reports, 8(1), 10896 10.1038/s41598-018-29233-9 PubMed DOI PMC

Špiláková, B. , Shaw, D. J. , Czekóová, K. , & Brázdil, M. (2019). Dissecting social interaction: Dual‐fMRI reveals patterns of interpersonal brain‐behavior relationships that dissociate among dimensions of social exchange. Social Cognitive and Affective Neuroscience, 14(2), 225–235. 10.1093/scan/nsz004 PubMed DOI PMC

Tang, H. , Mai, X. , Wang, S. , Zhu, C. , Krueger, F. , & Liu, C. (2016). Interpersonal brain synchronization in the right temporo‐parietal junction during face‐to‐face economic exchange. Social Cognitive and Affective Neuroscience, 11(1), 23–32. 10.1093/scan/nsv092 PubMed DOI PMC

Toppi, J. , Borghini, G. , Petti, M. , He, E. J. , De Giusti, V. , … Babiloni, F. (2016). Investigating cooperative behavior in ecological settings: An EEG Hyperscanning study. PLOS One, 11(4), e0154236 10.1371/journal.pone.0154236 PubMed DOI PMC

Uddin, L. Q. , Molnar‐Szakacs, I. , Zaidel, E. , & Iacoboni, M. (2006). rTMS to the right inferior parietal lobule disrupts self‐other discrimination. Social Cognitive and Affective Neuroscience, 1(1), 65–71. 10.1093/scan/nsl003 PubMed DOI PMC

van den Heuvel, M. P. , & Sporns, O. (2011). Rich‐Club Organization of the Human Connectome. Journal of Neuroscience, 31(44), 15775–15786. 10.1523/JNEUROSCI.3539-11.2011 PubMed DOI PMC

Wan, X. , Nakatani, H. , Ueno, K. , Asamizuya, T. , Cheng, K. , & Tanaka, K. (2011). The neural basis of intuitive best next‐move generation in board game experts. Science, 331(6015), 341–346. 10.1126/science.1194732 PubMed DOI

Wilson, S. M. , Molnar‐Szakacs, I. , & Iacoboni, M. (2008). Beyond superior temporal cortex: Intersubject correlations in narrative speech comprehension. Cerebral Cortex, 18, 230–242. 10.1093/cercor/bhm049 PubMed DOI

Wolf, I. , Dziobek, I. , & Heekeren, H. R. (2010). Neural correlates of social cognition in naturalistic settings: A model‐free analysis approach. NeuroImage, 49(1), 894–904. 10.1016/j.neuroimage.2009.08.060 PubMed DOI

Zaki, J. , Bolger, N. , & Ochsner, K. (2008). The Interpersonal Nature of Empathic Accuracy. Psychological Science, 19(4), 399–404. PubMed

Zhang, M. , Liu, T. , Pelowski, M. , Jia, H. , & Yu, D. (2017). Social risky decision‐making reveals gender differences in the TPJ: A hyperscanning study using functional near‐infrared spectroscopy. Brain and Cognition, 119, 54–63. 10.1016/j.bandc.2017.08.008 PubMed DOI

A neuroscientific evaluation of driver rehabilitation: Functional neuroimaging demonstrates the effectiveness of empathy induction in altering brain responses during social information processing