Although a large proportion of our lives are spent participating in social interactions, the investigation of the neural mechanisms supporting these interactions has largely been restricted to situations of social observation — that is, situations in which an individual observes a social stimulus without opportunity for interaction. In recent years, efforts have been made to develop a truly social, or ‘second-person’, neuroscientific approach to these investigations in which neural processes are examined within the context of a real-time reciprocal social interaction. These developments have helped to elucidate the behavioural and neural mechanisms of social interactions; however, further theoretical and methodological innovations are still needed. Findings to date suggest that the neural mechanisms supporting social interaction differ from those involved in social observation and highlight a role of the so-called ‘mentalizing network’ as important in this distinction. Taking social interaction seriously may also be particularly important for the advancement of the neuroscientific study of different psychiatric conditions.
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Schurz, M. et al. Fractionating theory of mind: a meta-analysis of functional brain imaging studies. Neurosci. Biobehav. Rev. 42, 9–34 (2014).
Schilbach, L. et al. Toward a second-person neuroscience. Behav. Brain 36, 393–414 (2013).
Schippers, M. B. et al. Mapping the information flow from one brain to another during gestural communication. Proc. Natl Acad. Sci. USA 107, 9388–9393 (2010).
Anders, S. et al. Flow of affective information between communicating brains. Neuroimage 54, 439–446 (2011).
Montague, P. R. et al. Hyperscanning: simultaneous fMRI during linked social interactions. Neuroimage 1164, 1159–1164 (2002).
King-Casas, B. et al. Getting to know you: reputation and trust in a two-person economic exchange. Science 308, 78–83 (2005).
Chiu, P. H. et al. Self responses along cingulate cortex reveal quantitative neural phenotype for high-functioning autism. Neuron 57, 463–473 (2008).
King-Casas, B. et al. The rupture and repair in borderline personality disorder. Science 321, 806–811 (2008).
Hirsch, J. et al. Frontal temporal and parietal systems synchronize within and across brains during live eye-to-eye contact. Neuroimage 157, 314–330 (2017).
Kinreich, S. et al. Brain-to-brain synchrony during naturalistic social interactions. Sci. Rep. 7, 1–12 (2017).
Bilek, E. et al. Information flow between interacting human brains: Identification, validation, and relationship to social expertise. Proc. Natl Acad. Sci. USA 112, 5207–5212 (2015).
Saito, D. N. et al. ‘Stay tuned’: inter-individual neural synchronization during mutual gaze and joint attention. Front. Integr. Neurosci. 4, 127 (2010).
Yun, K., Watanabe, K. & Shimojo, S. Interpersonal body and neural synchronization as a marker of implicit social interaction. Sci. Rep. 2, 1–8 (2012).
Schilbach, L. et al. Being with virtual others: neural correlates of social interaction. Neuropsychologia 44, 718–730 (2006).
Kampe, K. K. W., Frith, C. D. & Frith, U. ‘Hey John’: signals conveying communicative intention toward the self activate brain regions associated with ‘mentalizing,’ regardless of modality. J. Neurosci. 23, 5258–5263 (2003).
Redcay, E., Velnoskey, K. R. & Rowe, M. L. Perceived communicative intent in gesture and language modulates the superior temporal sulcus. Hum. Brain Mapp. 37, 3444–3461 (2016).
Redcay, E. & Carlson, T. A. Rapid neural discrimination of communicative gestures. Soc. Cogn. Affect. Neurosci. 10, 545–551 (2013).
Ferrari, P. F. et al. Mirror neurons responding to the observation of ingestive and communicative mouth actions in the monkey ventral premotor cortex. Eur. J. Neurosci. 17, 1703–1714 (2003).
Tylén, K. et al. Interaction versus observation: distinctive modes of social cognition in human brain and behavior? A combined fMRI and eye-tracking study. Front. Hum. Neurosci. 6, 331 (2012).
Ciaramidaro, A. et al. Do you mean me? Communicative intentions recruit the mirror and the mentalizing system. Soc. Cogn. Affect. Neurosci. 9, 909–916 (2014).
Nagels, A. et al. Feeling addressed! The role of body orientation and co-speech gesture in social communication. Hum. Brain Mapp. 36, 1925–1936 (2015).
Rice, K. & Redcay, E. Interaction matters: a perceived social partner alters the neural response to human speech. Neuroimage 129, 480–488 (2016).
Redcay, E. et al. Communicative signals promote object recognition memory and modulate the posterior superior temporal sulcus. J. Cogn. Neurosci. 28, 8–19 (2016).
von dem Hagen, E. A. H. et al. Direct gaze elicits atypical activation of the theory-of-mind network in autism spectrum conditions. Cereb. Cortex 24, 1485–1492 (2014).
Morris, J. P., Pelphrey, K. A. & McCarthy, G. Regional brain activation evoked when approaching a virtual human on a virtual walk. J. Cogn. Neurosci. 17, 1744–1752 (2005).
Saggar, M. et al. Revealing the neural networks associated with processing of natural social interaction and the related effects of actor-orientation and face-visibility. Neuroimage 84, 656–648 (2014).
Pfeiffer, U. J. et al. Why we interact: on the functional role of the striatum in the subjective experience of social interaction. Neuroimage 101, 124–137 (2014).
Alkire, D. et al. Social interaction recruits mentalizing and reward systems in middle childhood. Hum. Brain Mapp. 39, 3928–3942 (2018).
Kuhlen, A. K. et al. Brains in dialogue: decoding neural preparation of speaking to a conversational partner. Soc. Cogn. Affect. Neurosci. 12, 871–880 (2017).
Redcay, E. et al. Live face-to-face interaction during fMRI: a new tool for social cognitive neuroscience. Neuroimage 50, 1639–1647 (2010).
Rice, K., Moraczewski, D. & Redcay, E. Perceived live interaction modulates the developing social brain. Soc. Cogn. Affect. Neurosci. 11, 1354–1362 (2016).
Schuwerk, T. et al. The rTPJ’s overarching cognitive function in networks for attention and theory of mind. Soc. Cogn. Affect. Neurosci. 12, 157–168 (2017).
Pönkänen, L. M. et al. Does it make a difference if I have an eye contact with you or with your picture? An ERP study. Soc. Cogn. Affect. Neurosci. 6, 486–494 (2011).
Wykowska, A. et al. Beliefs about the minds of others influence how we process sensory information. PLOS ONE 9, e94339 (2014).
Cavallo, A. et al. When gaze opens the channel for communication: integrative role of IFG and MPFC. Neuroimage 119, 63–69 (2015).
Coan, J. A., Schaefer, H. S. & Davidson, R. J. Lending a hand: social regulation of the neural response to threat. Psychol. Sci. 17, 1032–1039 (2006).
Kokal, I., Gazzola, V. & Keysers, C. Acting together in and beyond the mirror neuron system. Neuroimage 47, 2046–2056 (2009).
Koike, T., Tanabe, H. C. & Sadato, N. Hyperscanning neuroimaging technique to reveal the “two-in-one” system in social interactions. Neurosci. Res. 90, 25–32 (2015).
Dumas, G. et al. Inter-brain synchronization during social interaction. PLOS ONE 5, e12166 (2010).
Jiang, J. et al. Leader emergence through interpersonal neural synchronization. Proc. Natl Acad. Sci. USA 112, 4274–4279 (2015).
Koike, T. et al. Neural substrates of shared attention as social memory: a hyperscanning functional magnetic resonance imaging study. Neuroimage 125, 401–412 (2016).
Bruner, J. Child’s Talk: Learning to Use Language (Norton, 1983).
Verga, L. & Kotz, S. A. How relevant is social interaction in second language learning? Front. Hum. Neurosci. 7, 550 (2013).
Brennan, S. E. & Hanna, J. E. Partner-specific adaptation in dialog. Top. Cogn. Sci. 1, 274–291 (2009).
Giles, H., Coupland, N. & Coupland, J. in Contexts of Accommodation (eds Giles, H., Coupland, J. & Coupland, N.) 1–68 (Cambridge Univ. Press, 1992).
Schockley, K., Santana, M. & Fowler, C. A. Mutual interpersonal postural constraints are involved in cooperative conversation. J. Exp. Psychol. Hum. Percept. Perform. 29, 326–332 (2003).
Niedenthal, P. et al. The simulation of smiles (SIMS) model: embodied simulation and the meaning of facial expression. Behav. Brain Sci. 33, 417–433 (2010).
Richardson, D. C., Dale, R. & Kirkham, N. Z. The art of conversation is coordination. Psychol. Sci. 18, 407–413 (2007).
Leander, N. P., Chartrand, T. L. & Wood, W. Mind your mannerisms: behavioral mimicry elicits stereotype conformity. J. Exp. Soc. Psychol. 47, 195–201 (2011).
Bolis, D. et al. Beyond autism: introducing the dialectical misattunement hypothesis and a Bayesian account of intersubjectivity. Psychopathology 50, 355–372 (2018).
Campbell-Meiklejohn, D. K. et al. How the opinion of others affects our valuation of objects. Curr. Biol. 20, 1165–1170 (2010).
Klucharev, V. et al. Reinforcement learning signal predicts social conformity. Neuron 61, 140–151 (2009).
Liu, D. et al. Interactive brain activity: review and progress on EEG-based hyperscanning in social interactions. Front. Psychol. 9, 1–11 (2018).
Szymanski, C. et al. Teams on the same wavelength perform better: inter-brain phase synchronization constitutes a neural substrate for social facilitation. Neuroimage 152, 425–436 (2017).
Dikker, S. et al. Brain-to-brain synchrony tracks real-world dynamic group interactions in the classroom. Curr. Biol. 27, 1375–1380 (2017).
Tognoli, E. et al. The phi complex as a neuromarker of human social coordination. Proc. Natl Acad. Sci. USA 104, 8190–8195 (2007).
Konvalinka, I. et al. Frontal alpha oscillations distinguish leaders from followers: multivariate decoding of mutually interacting brains. Neuroimage 94, 79–88 (2014).
Redcay, E. & Saxe, R. in Agency and Joint Attention (eds Terrace, H. S. & Metacalfe, J.) (Oxford Univ. Press, 2013).
Caruana, N., Brock, J. & Woolgar, A. A frontotemporoparietal network common to initiating and responding to joint attention bids. Neuroimage 108, 34–46 (2015).
Gordon, I. et al. Social, reward, and attention brain networks are involved when online bids for joint attention are met with congruent versus incongruent responses. Soc. Neurosci. 8, 544–554 (2013).
Oberwelland, E. et al. Look into my eyes: investigating joint attention using interactive eye-tracking and fMRI in a developmental sample. Neuroimage 130, 248–260 (2016).
Redcay, E., Kleiner, M. & Saxe, R. Look at this: the neural correlates of initiating and responding to bids for joint attention. Front. Hum. Neurosci. 6, 1–14 (2012).
Schilbach, L. et al. Minds made for sharing: initiating joint attention recruits reward-related neurocircuitry. J. Cogn. Neurosci. 22, 2702–2715 (2010).
Wagner, U. et al. Beautiful friendship: social sharing of emotions improves subjective feelings and activates the neural reward circuitry. Soc. Cogn. Affect. Neurosci. 10, 80–808 (2015).
Mundy, P. A review of joint attention and social-cognitive brain systems in typical development and autism spectrum disorder. Eur. J. Neurosci. 47, 497–514 (2018).
Garrod, S. & Pickering, M. J. Why is conversation so easy? Trends Cogn. Sci. 8, 8–11 (2004).
Pickering, M. J. & Garrod, S. An integrated theory of language production and comprehension. Behav. Brain Sci. 36, 329–347 (2013).
Rilling, J. K. et al. The neural correlates of theory of mind within interpersonal interactions. Neuroimage 22, 1694–1703 (2004).
Kircher, T. et al. Online mentalising investigated with functional MRI. Neurosci. Lett. 454, 176–181 (2009).
Gallagher, H. L. et al. Imaging the intentional stance in a competitive game. Neuroimage 16, 814–821 (2002).
Carter, R. M. et al. A distinct role of the temporal-parietal junction in predicting socially guided decisions. Science 336, 109–111 (2012).
Hill, C. A. et al. A causal account of the brain network computations underlying strategic social behavior. Nat. Neurosci. 20, 1142–1149 (2017).
Tang, H. et al. Interpersonal brain synchronization in the right temporo-parietal junction during face-to-face economic exchange. Soc. Cogn. Affect. Neurosci. 11, 23–32 (2015).
Takahashi, H. et al. Different impressions of other agents obtained through social interaction uniquely modulate dorsal and ventral pathway activities in the social human brain. Cortex 58, 289–300 (2014).
Bellucci, G. et al. Neural signatures of trust in reciprocity: a coordinate-based meta-analysis. Hum. Brain Mapp. 38, 1233–1248 (2017).
Xiang, T. et al. Computational phenotyping of two-person interactions reveals differential neural response to depth-of-thought. PLOS Comput. Biol. 8, 0–8 (2012).
Yoshida, W. et al. Cooperation and heterogeneity of the autistic mind. J. Neurosci. 30, 8815–8818 (2010).
Koshelev, M. et al. Biosensor approach to psychopathology classification. PLOS Comput. Biol. 6, e1000966 (2010).
De Vico Fallani, F. et al. Defecting or not defecting: how to ‘read’ human behavior during cooperative games by EEG measurements. PLOS ONE 5, e14187 (2010).
Diaconescu, A. O. et al. Inferring on the intentions of others by hierarchical Bayesian learning. PLOS Comput. Biol. 10, e1003810 (2014).
Wang, H., Braun, C. & Enck, P. How the brain reacts to social stress (exclusion) — a scoping review. Neurosci. Biobehav. Rev. 80, 80–88 (2017).
Müller-Pinzler, L. et al. Neural pathways of embarrassment and their modulation by social anxiety. Neuroimage 119, 252–261 (2015).
Schmalzle, R. et al. Brain connectivity dynamics during social interaction reflect social network structure. Proc. Natl Acad. Sci. USA 114, 5153–5158 (2017).
Preller, K. H. et al. Functional changes of the reward system underlie blunted response to social gaze in cocaine users. Proc. Natl Acad. Sci. USA 111, 2842–2847 (2014).
Parkinson, C., Kleinbaum, A. M. & Wheatley, T. Similar neural responses predict friendship. Nat. Commun. 9, 1–13 (2018).
Gallese, V. & Goldman, A. Mirror neurons and the simulation theory of mind-reading. Trends Cogn. Sci. 2, 493–501 (1998).
Thioux, M., Gazzola, V. & Keysers, C. Action understanding: how, what, and why. Curr. Biol. 18, 431–434 (2008).
de Lange, F. P. et al. Complementary systems for understanding action intentions. Curr. Biol. 18, 454–457 (2008).
Spunt, R. P., Satpute, A. B. & Lieberman, M. D. Identifying the what, why, and how of an observed action: an fMRI study of mentalizing and mechanizing during action observation. J. Cogn. Neurosci. 23, 63–74 (2011).
Frith, U. & Frith, C. The biological basis of social interaction. Curr. Dir. Psychol. Sci. 10, 151–155 (2001).
Grossmann, T. The development of social brain functions in infancy. Psychol. Bull. 141, 1266–1287 (2015).
Redcay, E. & Warnell, K. R. in Advances in Child Development and Behavior Vol. 54 (ed. Benson, J. B.) 1–44 (Elsevier, 2018).
Sliwa, J. & Freiwald, W. A. A dedicated network for social interaction processing in the primate brain. Science 749, 745–749 (2017).
Tomasello, M. How children come to understand false beliefs: a shared intentionality account. Proc. Natl Acad. Sci. USA 115, 8491–8498 (2018).
Schippers, M. B. et al. Playing charades in the fMRI: are mirror and/or mentalizing areas involved in gestural communication? PLOS ONE 4, e6801 (2009).
Zaki, J. & Ochsner, K. The need for a cognitive neuroscience of naturalistic social cognition. Ann. NY Acad. Sci. 1167, 16–30 (2009).
Sperduti, M. et al. Mirror neuron system and mentalizing system connect during online social interaction. Cogn. Process. 15, 307–316 (2014).
Spengler, S., Von Cramon, D. Y. & Brass, M. Control of shared representations relies on key processes involved in mental state attribution. Hum. Brain Mapp. 30, 3704–3718 (2009).
Wang, Y., Ramsey, R. & Hamilton, A. F. The control mimicry eye contact is mediated medial prefrontal cortex. J. Neurosci. 31, 12001–10 (2011).
Warnell, K. R., Sadikova, E. & Redcay, E. Let’s chat: developmental neural bases of social motivation during real-time peer interaction. Dev. Sci. 21, e12581 (2018).
Konvalinka, I. & Roepstorff, A. The two-brain approach: how can mutually interacting brains teach us something about social interaction? Front. Hum. Neurosci. 6, 215 (2012).
Hasson, U. & Frith, C. D. Mirroring and beyond: coupled dynamics as a generalized framework for modelling social interactions. Phil. Trans. R. Soc. B 371, 20150366 (2016).
Sänger, J., Müller, V. & Lindenberger, U. Intra- and interbrain synchronization and network properties when playing guitar in duets. Front. Hum. Neurosci. 6, 312 (2012).
Montague, P. R. et al. Computational psychiatry. Trends Cogn. Sci. 16, 72–80 (2012).
Jasmin, K. et al. Overt social interaction and resting state in young adult males with autism: core and contextual neural features. Brain 142, 808–822 (2019).
Murray, L. & Trevarthen, C. in Social Perception in Infancy (eds Field, T. M. & Fox, N. A.) 177–198 (ABlex, 1985).
Feldman, R. Parent-infant synchrony: a biobehavioral model of mutual influences in the formation of affiliative bonds. Monogr. Soc. Res. Child Dev. 77, 42–51 (2012).
Kuhl, P. K., Tsao, F.-M. & Liu, H.-M. Foreign-language experience in infancy: effects of short-term exposure and social interaction on phonetic learning. Proc. Natl Acad. Sci. USA 100, 9096–9101 (2003).
Lytle, S. R., Garcia-Sierra, A. & Kuhl, P. K. Two are better than one: infant language learning from video improves in the presence of peers. Proc. Natl Acad. Sci. USA 115, 9859–9866 (2018).
Kirschner, S. & Tomasello, M. Joint drumming: social context facilitates synchronization in preschool children. J. Exp. Child Psychol. 102, 299–314 (2009).
Leong, V. et al. Speaker gaze increases information coupling between infant and adult brains. Proc. Natl Acad. Sci. USA 114, 13290–13295 (2017).
Liao, Y. et al. EEG imaging of toddlers during dyadic turn-taking: Mu-rhythm modulation while producing or observing social actions. Neuroimage 112, 52–60 (2015).
Pan, Y. et al. Cooperation in lovers: Axiangn fNIRS-based hyperscanning study. Hum. Brain Mapp. 38, 831–841 (2017).
Goldstein, P. et al. Brain-to-brain coupling during handholding is associated with pain reduction. Proc. Natl Acad. Sci. USA 115, E2528–E2537 (2018).
Fareri, D. S. et al. Social network modulation of reward-related signals. J. Neurosci. 32, 9045–9052 (2012).
Clark, H. H., Schreuder, R. & Buttrick, S. Common ground and the understanding of demonstrative reference. J. Verbal Learning Verbal Behav. 22, 245–258 (1983).
Hasson, U. et al. Brain-to-brain coupling: a mechanism for creating and sharing a social world. Trends Cogn. Sci. 16, 113–120 (2012).
Yeshurun, Y. et al. Same story, different story: the neural representation of interpretive frameworks. Psychol. Sci. 28, 307–319 (2017).
Lahnakoski, J. M. et al. Synchronous brain activity across individuals underlies shared psychological perspectives. Neuroimage 100, 316–324 (2014).
Nummenmaa, L. et al. Emotions promote social interaction by synchronizing brain activity across individuals. Proc. Natl Acad. Sci. USA 109, 9599–9604 (2012).
Golland, Y. et al. Neural dynamics underlying emotional transmissions between individuals. Soc. Cogn. Affect. Neurosci. 12, 1249–1260 (2017).
Schilbach, L. et al. Minds at rest? Social cognition as the default mode of cognizing and its putative relationship to the ‘default system’ of the brain. Consci. Cogn. 17, 457–467 (2008).
Schilbach, L. Towards a second-person neuropsychiatry. Phil. Trans. R. Soc. B 371, 20150081 (2016).
Lu, J. et al. Single stimulus fMRI produces a neural individual difference measure for autism spectrum disorder. Clin. Psychol. Sci. 3, 422–432 (2016).
Komeda, H. et al. Autistic empathy toward autistic others. Soc. Cogn. Affect. Neurosci. 10, 145–152 (2015).
Edey, R. et al. Interaction takes two: typical adults exhibit mind-blindness towards those with autism spectrum disorder. J. Abnorm. Psychol. 125, 879–885 (2016).
Bolis, D. & Schilbach, L. Observing and participating in social interactions: action perception and action control across the autistic spectrum. Dev. Cogn. Neurosci. 29, 168–175 (2018).
Parpart, H. et al. Schematherapy-informed social interaction training: an intervention approach for adults with high-functioning autism [German]. Psychotherapeut 63, 235–242 (2018).
Kennedy, D. P. & Adolphs, R. The social brain in psychiatric and neurological disorders. Trends Cogn. Sci. 16, 559–572 (2012).
The authors thank D. Alkire, M.-L. Brandi, J. Lahnakoski, D. Moraczewski, K. Warnell and Y. Xiao for critical comments on the manuscript. The authors are also grateful to the referees for their valuable suggestions. E.R.’s contributions to this paper were supported in part by grants from the US National Institutes of Health (NIH; R01MH107441, R01MH112517 and P01 HD064653). L.S. was funded by a grant from the Max Planck Society for an Independent Max Planck Research Group. The content is solely the responsibility of the authors and does not necessarily represent the official views of the NIH or the Max Planck Society.
Nature Reviews Neuroscience thanks C. Frith, R. Montague and N. Sadato for their contribution to the peer review of this work.
The authors declare no competing interests.
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Redcay, E., Schilbach, L. Using second-person neuroscience to elucidate the mechanisms of social interaction. Nat Rev Neurosci 20, 495–505 (2019). https://doi.org/10.1038/s41583-019-0179-4
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