During social interactions, each individual's actions are simultaneously a consequence of and an antecedent to their interaction partner's behavior. Capturing online the brain processes underlying such mutual dependency requires simultaneous measurements of all interactants' brains during real-world exchange ('hyperscanning'). This demands a precise characterization of the type of interaction under investigation, however, and analytical techniques capable of capturing interpersonal dependencies. We adapted an interactive task capable of dissociating between two dimensions of interdependent social exchange: goal structure (cooperation vs competition) and interaction structure [concurrent (CN) vs turn-based]. Performing dual-functional magnetic resonance imaging hyperscanning on pairs of individuals interacting on this task, and modeling brain responses in both interactants as systematic reactions to their partner's behavior, we investigated interpersonal brain-behavior dependencies (iBBDs) during each dimension. This revealed patterns of iBBDs that differentiated among exchanges; in players supporting the actions of another, greater brain responses to the co-player's actions were expressed in regions implicated in social cognition, such as the medial prefrontal cortex, precuneus and temporal cortices. Stronger iBBD during CN competitive exchanges was observed in brain systems involved in movement planning and updating, however, such as the supplementary motor area. This demonstrates the potential for hyperscanning to elucidate neural processes underlying different forms of social exchange.

Behavioural and Social Neuroscience Research Group Central European Institute of Technology Masaryk University Kamenice 5 Brno Czech Republic

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

Faculty of Medicine Masaryk University Kamenice 5 Brno Czech Republic

See more in PubMed

Apps M.A.J., Lockwood P.L., Balsters J.H. (2013). The role of the midcingulate cortex in monitoring others decisions. Frontiers in Neuroscience, 7, 1–7. PubMed PMC

Apps M.A.J., Rushworth M.F.S., Chang S.W.C. (2016). The anterior cingulate gyrus and social cognition: tracking the motivation of others. Neuron, 90, 692–707. PubMed PMC

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

Babiloni F., Cincotti F., Mattia D., et al. (2007). High resolution EEG hyperscanning during a card game. Conference Proceedings of the IEEE Engineering in Medicine and Biology Society, 2007, 4957–4960. PubMed

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

Bickart K.C., Dickerson B.C., Feldman Barrett L. (2014). The amygdala as a hub in brain networks that support social life. Neuropsychologia, 63, 235–248. PubMed PMC

Brass M., Ruby P., Spengler S. (2009). Inhibition of imitative behaviour and social cognition. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 364, 2359–2367. PubMed PMC

Burgess A.P. (2013). On the interpretation of synchronization in EEG hyperscanning studies: a cautionary note. Frontiers in Human Neuroscience, 7, 881. PubMed PMC

Cabanis M., Pyka M., Mehl S., et al. (2013). The precuneus and the insula in self-attributional processes. Cognitive, Affective & Behavioral Neuroscience, 13, 330–345. PubMed

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

Chaminade T., Marchant J.L., Kilner J., Frith C.D. (2012). An fMRI study of joint action—varying levels of cooperation correlates with activity in control networks. Frontiers in Human Neuroscience, 6, 179. PubMed PMC

Cona G., Semenza C. (2017). Supplementary motor area as key structure for domain-general sequence processing: a unified account. Neuroscience and Biobehavioral Reviews, 72, 28–42. PubMed

Cui X., Bryant D.M., Reiss A.L. (2012). NIRS-based hyperscanning reveals increased interpersonal coherence in superior frontal cortex during cooperation. NeuroImage, 59, 2430–2437. PubMed PMC

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

Eklund A., Nichols T.E., Knutsson H. (2016). Cluster failure: why fMRI inferences for spatial extent have inflated false-positive rates. Proceedings of the National Academy of Sciences of the United States of America, 113, 7900–7905. PubMed PMC

Frith C.D., Frith U. (2006). The neural basis of mentalizing. Neuron, 50, 531–534. PubMed

Funane T., Kiguchi M., Atsumori H., Sato H., Kubota K., Koizumi H. (2011). Synchronous activity of two people’s prefrontal cortices during a cooperative task measured by simultaneous near-infrared spectroscopy. Journal of Biomedical Optics, 16, 077011. PubMed

Haber S.N., Knutson B. (2010). The reward circuit: linking primate anatomy and human imaging. Neuropsychopharmacology, 35, 4–26. PubMed PMC

Hari R., Henriksson L., Malinen S., et al. (2015). Centrality of social interaction in human brain function. Neuron, 88, 181–193. 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, 105–106. PubMed

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 of London. Series B, Biological Sciences, 371, 20150366. PubMed 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(2), 324–333. PubMed

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

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

Jiang J., Dai B., Peng D., Zhu C., Liu L., Lu C. (2012). Neural synchronization during face-to-face communication. The Journal of Neuroscience, 32, 16064–16069. PubMed PMC

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. PubMed

King-Casas B., Tomlin D., Anen C., Camerer C.F., Quartz S.R., Montague P.R. (2005). Getting to know you: reputation and trust in a two-person economic exchange. Science (New York, N.Y.), 308, 78–83. PubMed

Koike T., Tanabe H.C., Okazaki S., et al. (2016). Neural substrates of shared attention as social memory: a hyperscanning functional magnetic resonance imaging study. NeuroImage, 125, 401–412. PubMed

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. PubMed

Konvalinka I., Bauer M., Stahlhut C., Hansen L.K., Roepstorff A., Frith C.D. (2014). Frontal alpha oscillations distinguish leaders from followers: multivariate decoding of mutually interacting brains. NeuroImage, 94, 79–88. PubMed

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, 215. PubMed PMC

Krill A.L., Platek S.M. (2012). Working together may be better: activation of reward centers during a cooperative maze task. PLoS One, 7, 1–7. PubMed PMC

Kurzban R., Burton-Chellew M.N., West S.A. (2015). The evolution of altruism in humans. Annual Review of Psychology, 66, 575–599. PubMed

Lindenberger U., Li S.C., Gruber W., Müller V. (2009). Brains swinging in concert: cortical phase synchronization while playing guitar. BMC Neuroscience, 10, 22. PubMed PMC

Liu N., Mok C., Witt E., Pradhan A.H., Chen J.E., Reiss A.L. (2016). NIRS-based hyperscanning reveals inter-brain neural synchronization during cooperative Jenga game with face-to-face communication. Frontiers in Human Neuroscience, 10, 1–11. PubMed PMC

Liu T., Pelowski M. (2014). Clarifying the interaction types in two-person neuroscience research. Frontiers in Human Neuroscience, 8, 276. PubMed PMC

Liu T., Saito H., Oi M. (2015). Role of the right inferior frontal gyrus in turn-based cooperation and competition: a near-infrared spectroscopy study. Brain and Cognition, 99, 17–23. PubMed

MATLAB and Statistics Toolbox (2016) The MathWorks, Inc., Natick, Massachusetts, United States.

Morelli S.A., Rameson L.T., Lieberman M.D. (2014). The neural components of empathy: predicting daily prosocial behavior. Social Cognitive and Affective Neuroscience, 9, 39–47. PubMed PMC

Nachev P., Kennard C., Husain M. (2008). Functional role of the supplementary and pre-supplementary motor areas. Nature Reviews Neuroscience, 9, 856–869. PubMed

Naeem M., Prasad G., Watson D.R., Kelso J.A. (2012). Functional dissociation of brain rhythms in social coordination. Clinical Neurophysiology, 123, 1789–1797. PubMed

Nozawa T., Sasaki Y., Sakaki K., Yokoyama R., Kawashima R. (2016). Interpersonal frontopolar neural synchronization in group communication: an exploration toward fNIRS hyperscanning of natural interactions. NeuroImage, 133, 484–497. PubMed

Osaka N., Minamoto T., Yaoi K., Azuma M., Osaka M. (2014). Neural synchronization during cooperated humming: a hyperscanning study using fNIRS. Procedia, Social and Behavioral Sciences, 126, 241–243.

Reniers R.L.E.P., Völlm B.A., Elliott R., Corcoran R. (2014). Empathy, ToM, and self-other differentiation: an fMRI study of internal states. Social Neuroscience, 9, 50–62. PubMed

Rilling J.K., Gutman D.A., Zeh T.R., Pagnoni G., Berns G., Kilts C. (2002). A neural basis for social cooperation. Neuron, 35, 395–405. PubMed

Rizzolatti G., Craighero L. (2004). The mirror-neuron system. Annual Review of Neuroscience, 27, 169–192. PubMed

Schilbach L. (2014). On the relationship of online and offline social cognition. Frontiers in Human Neuroscience, 8, 278. PubMed PMC

Schilbach L., Timmermans B., Reddy V., et al. (2013). Toward a second-person neuroscience. The Behavioral and Brain Sciences, 36, 393–414. PubMed

Schilbach L., Wilms M., Eickhoff S.B., et al. (2010). Minds made for sharing: initiating joint attention recruits reward-related neurocircuitry. Journal of Cognitive Neuroscience, 22, 2702–2715. PubMed

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

Shaw D., Czekóová K., Gajdoš M., Staněk R., Špalek J., Brázdil M. (2019). Social decision making in the brain: input-state-output modelling reveals patterns of effective connectivity underlying reciprocal choices. Human Brain Mapping. doi:10.1002/hbm.24446. PubMed DOI PMC

Shaw D.J., Czekóová K., Staněk R., et al. (2018). A dual-fMRI investigation of the iterated ultimatum game reveals that reciprocal behaviour is associated with neural alignment. Scientific Reports, 8, 10896. PubMed PMC

Smith S.M., Nichols T.E. (2009). Threshold-free cluster enhancement: addressing problems of smoothing, threshold dependence and localisation in cluster inference. NeuroImage, 44, 83–98. PubMed

Spiegelhalder K., Ohlendorf S., Regen W., et al. (2014). Interindividual synchronization of brain activity during live verbal communication. Behavioural Brain Research, 258, 75–79. PubMed

Stolk A., Noordzij M.L., Verhagen L., et al. (2014). Cerebral coherence between communicators marks the emergence of meaning. Proceedings of the National Academy of Sciences of the United States of America, 201414886. PubMed PMC

Takahashi H., Izuma K., Matsumoto M., Matsumoto K., Omori T. (2015). The anterior insula tracks behavioral entropy during an interpersonal competitive game. PLoS One, 10, 1–17. PubMed 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, 23–32. PubMed PMC

Tognoli E., Lagarde J., DeGuzman G.C., Kelso J.A. (2007). The phi complex as a neuromarker of human social coordination. Proceedings of the National Academy of Sciences of the United States of America, 104, 8190–8195. PubMed PMC

Tomasello M., Vaish A. (2013). Origins of human cooperation and morality. Annual Review of Psychology, 64, 231–255. PubMed

Tomlin D., Kayali M.A., King-Casas B., et al. (2006). Agent-specific responses in the cingulate cortex during economic exchanges. Science (New York, N.Y.), 312, 1047–1050. PubMed

Toppi J., Borghini G., Petti M., et al. (2016). Investigating cooperative behavior in ecological settings: an EEG hyperscanning study. Yao D., editorPLoS One, 11(4), e0154236. PubMed PMC

Twining R.C., Vantrease J.E., Love S., Padival M., Rosenkranz J.A. (2017). An intra-amygdala circuit specifically regulates social fear learning. Nature Neuroscience, 20, 459–469. PubMed PMC

Van Overwalle F. (2009). Social cognition and the brain: a meta-analysis. Human Brain Mapping, 30, 829–858. PubMed PMC

Völlm B.A., Taylor A.N.W., Richardson P., et al. (2006). Neuronal correlates of theory of mind and empathy: a functional magnetic resonance imaging study in a nonverbal task. NeuroImage, 29, 90–98. PubMed

Walter H. (2012). Social cognitive neuroscience of empathy: concepts, circuits, and genes. Emotion Review, 4, 9–17.

Winkler A.M., Ridgway G.R., Webster M.A., Smith S.M., Nichols T.E. (2014). Permutation inference for the general linear model. NeuroImage, 92, 381–397. PubMed PMC

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

Getting into sync: Data-driven analyses reveal patterns of neural coupling that distinguish among different social exchanges