During social interactions, decision-making involves mutual reciprocity-each individual's choices are simultaneously a consequence of, and antecedent to those of their interaction partner. Neuroeconomic research has begun to unveil the brain networks underpinning social decision-making, but we know little about the patterns of neural connectivity within them that give rise to reciprocal choices. To investigate this, the present study measured the behaviour and brain function of pairs of individuals (N = 66) whilst they played multiple rounds of economic exchange comprising an iterated ultimatum game. During these exchanges, both players could attempt to maximise their overall monetary gain by reciprocating their opponent's prior behaviour-they could promote generosity by rewarding it, and/or discourage unfair play through retaliation. By adapting a model of reciprocity from experimental economics, we show that players' choices on each exchange are captured accurately by estimating their expected utility (EU) as a reciprocal reaction to their opponent's prior behaviour. We then demonstrate neural responses that map onto these reciprocal choices in two brain regions implicated in social decision-making: right anterior insula (AI) and anterior/anterior-mid cingulate cortex (aMCC). Finally, with behavioural Dynamic Causal Modelling, we identified player-specific patterns of effective connectivity between these brain regions with which we estimated each player's choices with over 70% accuracy; namely, bidirectional connections between AI and aMCC that are modulated differentially by estimates of EU from our reciprocity model. This input-state-output modelling procedure therefore reveals systematic brain-behaviour relationships associated with the reciprocal choices characterising interactive social decision-making.

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

Department of Economics Faculty of Economics and Administration Masaryk University Brno Czech Republic

Department of Psychology School of Life and Health Sciences Aston University Birmingham United Kingdom

Department of Public Economics Faculty of Economics and Administration Masaryk University Brno Czech Republic

Multimodal and Functional Imaging Laboratory CEITEC Central European Institute of Technology Masaryk University Brno Czech Republic

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Allman, J. M. , Tetreault, N. A. , Hakeem, A. Y. , Manaye, K. F. , Semendeferi, K. , Erwin, J. M. , … Hof, P. R. (2011). The von Economo neurons in the frontoinsular and anterior cingulate cortex. Annals of the New York Academy of Sciences, 1225(1), 59–71. 10.1111/j.1749-6632.2011.06011.x PubMed DOI PMC

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, 251 10.3389/fnins.2013.00251 PubMed DOI 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(4), 692–707. 10.1016/j.neuron.2016.04.018 PubMed DOI PMC

Augustine, J. R. (1996). Circuitry and functional aspects of the insular lobe in primates including humans. Brain Research Reviews, 22(3), 229–244. 10.1016/S0165-0173(96)00011-2 PubMed DOI

Avrahami, J. , Güth, W. , Hertwig, R. , Kareev, Y. , & Otsubo, H. (2013). Learning (not) to yield: An experimental study of evolving ultimatum game behavior. Journal of Socio‐Economics, 47, 47–54. 10.1016/j.socec.2013.08.009 DOI

Barbas, H. , Ghashghaei, H. , Dombrowski, S. M. , & Rempel‐Clower, N. L. (1999). Medial prefrontal cortices are unified by common connections with superior temporal cortices and distinguished by input from memory‐related areas in the rhesus monkey. Journal of Comparative Neurology, 410(3), 343–367. 10.1002/(SICI)1096-9861(19990802)410:3<343::AID-CNE1>3.0.CO;2-1 PubMed DOI

Bernhardt, B. C. , & Singer, T. (2012). The neural basis of empathy. Annual Review of Neuroscience, 35(1), 1–23. 10.1146/annurev-neuro-062111-150536 PubMed DOI

Billeke, P. , Zamorano, F. , Cosmelli, D. , & Aboitiz, F. (2013). Oscillatory brain activity correlates with risk perception and predicts social decisions. Cerebral Cortex (New York, N.Y. : 1991), 23(12), 2872–2883. 10.1093/cercor/bhs269 PubMed DOI

Billeke, P. , Zamorano, F. , López, T. , Rodriguez, C. , Cosmelli, D. , & Aboitiz, F. (2014). Someone has to give in: Theta oscillations correlate with adaptive behavior in social bargaining. Social Cognitive and Affective Neuroscience, 9(12), 2041–2048. 10.1093/scan/nsu012 PubMed DOI PMC

Bolton, B. G. E. , & Ockenfels, A. (2000). ERC: A theory of equity, reciprocity, and competition, The American Economic Review, American Economic Association, Vol. 90(1), 166–193. 10.1007/sl DOI

Cáceda, R. , James, G. A. , Gutman, D. A. , & Kilts, C. D. (2015). Organization of intrinsic functional brain connectivity predicts decisions to reciprocate social behavior. Behavioural Brain Research, 292, 478–483. 10.1016/j.bbr.2015.07.008 PubMed DOI

Cáceda, R. , Prendes‐Alvarez, S. , Hsu, J. J. , Tripathi, S. P. , Kilts, C. D. , & James, G. A. (2017). The neural correlates of reciprocity are sensitive to prior experience of reciprocity. Behavioural Brain Research, 332, 136–144. 10.1016/j.bbr.2017.05.030 PubMed DOI

Chang, S. W. , Gariépy, J. F. , & Platt, M. L. (2013). Neuronal reference frames for social decisions in primate frontal cortex. Nature Neuroscience, 16(2), 243–250. 10.1038/nn.3287.Neuronal PubMed DOI PMC

Charness, G. , & Rabin, M. (2002). Understanding social preferences with simple tests. Quarterly Journal of Economics, 117(3), 817–869.

Cox, J. C. , Friedman, D. , & Gjerstad, S. (2007). A tractable model of reciprocity and fairness. Games and Economic Behavior, 59(1), 17–45. 10.1016/j.geb.2006.05.001 DOI

Craig, A. D. (2009). How do you feel‐‐now? The anterior insula and human awareness. Nature Reviews. Neuroscience, 10(1), 59–70. 10.1038/nrn2555 PubMed DOI

Daunizeau, J. , Adam, V. , & Rigoux, L. (2014). VBA: A probabilistic treatment of nonlinear models for neurobiological and behavioural data. PLoS Computational Biology, 10(1), e1003441 10.1371/journal.pcbi.1003441 PubMed DOI PMC

Davis, M. H. (1983). Measuring individual differences in empathy: Evidence for a multidimensional approach. Journal of Personality and Social Psychology, 44(1), 113–126.

Erev, B. I. , & Roth, A. E. (1998). Predicting how people play games: Reinforcement learning in experimental games with unique, mixed strategy equilibria. The American Economic Review, 88(4), 848–881.

Falk, A. , & Fischbacher, U. (2006). A theory of reciprocity. Games and Economic Behavior, 54(2), 293–315.

Fehr, E. , & Schmidt, K. M. (1999). A theory of fairness, competition, and cooperation. Quarterly Journal of Economics, 114(3), 817–868.

Feng, C. , Deshpande, G. , Liu, C. , Gu, R. , Luo, Y. J. , & Krueger, F. (2016). Diffusion of responsibility attenuates altruistic punishment: A functional magnetic resonance imaging effective connectivity study. Human Brain Mapping, 37(2), 663–677. 10.1002/hbm.23057 PubMed DOI PMC

Feng, C. , Feng, X. , Wang, L. , Wang, L. , Gu, R. , Ni, A. , … Luo, Y. J. (2018). The neural signatures of egocentric bias in normative decision‐making. Brain Imaging and Behavior, 10.1007/s11682-018-9893-1 PubMed DOI

Feng, C. , Luo, Y. J. , & Krueger, F. (2015). Neural signatures of fairness‐related normative decision‐making in the ultimatum game: A coordinate‐based meta‐analysis. Human Brain Mapping, 36(2), 591–602. 10.1002/hbm.22649 PubMed DOI PMC

Friston, K. J. , Harrison, L. , & Penny, W. (2003). Dynamic causal modelling. NeuroImage, 19(4), 1273–1302. 10.1016/S1053-8119(03)00202-7 PubMed DOI

Gabay, A. S. , Radua, J. , Kempton, M. J. , & Mehta, M. A. (2014). The ultimatum game and the brain: A meta‐analysis of neuroimaging studies. Neuroscience and Biobehavioral Reviews, 47, 549–558. 10.1016/j.neubiorev.2014.10.014 PubMed DOI

Gajdoš, M. , Mikl, M. , & Mareček, R. (2016). Mask_explorer: A tool for exploring brain masks in fMRI group analysis. Computer Methods and Programs in Biomedicine, 134, 155–163. 10.1016/j.cmpb.2016.07.015 PubMed DOI

Güth, W. , Schmittberger, R. , & Schwarze, B. (1982). An experimental analysis of ultimatum bargaining. Journal of Economic Behavior and Organization, 3(4), 367–388. 10.1016/0167-2681(82)90011-7 DOI

Haroush, K. , & Williams, Z. M. (2015). Neuronal prediction of opponent's behavior during cooperative social interchange in primates. Cell, 160(6), 1233–1245. 10.1016/j.cell.2015.01.045 PubMed DOI PMC

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

Henrich, J. , Ensminger, J. , Bowles, S. , Gil‐white, F. , Fehr, E. , Marlowe, F. W. , & Patton, J. Q. (2005). Economic man in cross‐cultural perspective: Behavioral experiments in 15 small‐scale societies. Behavioral and Brain Sciences, 28, 795–855. PubMed

Holroyd, C. B. , & Yeung, N. (2012). Motivation of extended behaviors by anterior cingulate cortex. Trends in Cognitive Sciences, 16(2), 122–128. 10.1016/j.tics.2011.12.008 PubMed DOI

Johnson, E. J. , Camerer, C. , & Rymon, T. (2002). Detecting Failures of Backward Induction: Monitoring Information Search in Sequential Bargaining 1. Journal of Economic Theory, 104, 16–47. 10.1006/jeth.2001.2850 DOI

Kelly, C. , Toro, R. , Di Martino, A. , Cox, C. L. , Bellec, P. , Castellanos, F. X. , & Milham, M. P. (2012). A convergent functional architecture of the insula emerges across imaging modalities. NeuroImage, 61(4), 1129–1142. 10.1016/j.neuroimage.2012.03.021 PubMed DOI PMC

Kolling, N. , Wittmann, M. K. , Behrens, T. E. J. , Boorman, E. D. , Mars, R. B. , & Rushworth, M. F. S. (2016). Value, search, persistence and model updating in anterior cingulate cortex. Nature Neuroscience, 19(10), 1280–1285. 10.1038/nn.4382 PubMed DOI PMC

Krueger, F. , Grafman, J. , & McCabe, K. (2008). Neural correlates of economic game playing. Philosophical Transactions of the Royal Society B: Biological Sciences, 363(1511), 3859–3874. 10.1098/rstb.2008.0165 PubMed DOI PMC

Kuhl, J. (1994). Action versus state orientation: Psychometric properties of the Action Control Scale (ACS‐90) In Kuhl J. & Beckmann J. (Eds.), Volition and personality: Action versus state orientation (pp. 47–56). Seattle, WA: Hogrefe Huber.

Kurth, F. , Zilles, K. , Fox, P. T. , Laird, A. R. , & Eickhoff, S. B. (2010). A link between the systems: Functional differentiation and integration within the human insula revealed by meta‐analysis. Brain Structure and Function, 214(5–6), 519–534. 10.1007/s00429-010-0255-z PubMed DOI PMC

Mailath, G. J. , & Samuelson, L. (2006). Repeated games and reputations: Long‐run relationships. New York, NY: Oxford University Press.

Medford, N. , & Critchley, H. D. (2010). Conjoint activity of anterior insular and anterior cingulate cortex: Awareness and response. Brain Structure and Function, 214(5–6), 535–549. 10.1007/s00429-010-0265-x PubMed DOI PMC

Mesulam, M. M. , & Mufson, E. J. (1982a). Insula of the old world monkey. III: Efferent cortical output and comments on function. Journal of Comparative Neurology, 212(1), 38–52. 10.1002/cne.902120104 PubMed DOI

Mesulam, M. M. , & Mufson, E. J. (1982b). Insula of the old world monkey. Architectonics in the insulo‐orbito‐temporal component of the paralimbic brain. The Journal of Comparative Neurology, 22(1), 1–22. PubMed

Mufson, E. J. , & Mesulam, M. (1982). Insula of the old world monkey. II: Afferent cortical input and comments on the claustrum. Journal of Comparative Neurology, 212(1), 23–37. PubMed

Namkung, H. , Kim, S. H. , & Sawa, A. (2017). The insula: An underestimated brain area in clinical neuroscience, psychiatry, and neurology. Trends in Neurosciences, 40(4), 200–207. 10.1016/j.tins.2017.02.002 PubMed DOI PMC

Penny, W. D. , Stephan, K. E. , Mechelli, A. , & Friston, K. J. (2004). Comparing dynamic causal models. NeuroImage, 22(3), 1157–1172. 10.1016/j.neuroimage.2004.03.026 PubMed DOI

Rigoux, L. , & Daunizeau, J. (2015). NeuroImage dynamic causal modelling of brain – Behaviour relationships. NeuroImage, 117, 202–221. 10.1016/j.neuroimage.2015.05.041 PubMed DOI

Rigoux, L. , Stephan, K. E. , Friston, K. J. , & Daunizeau, J. (2014). Bayesian model selection for group studies ‐ Revisited. NeuroImage, 84, 971–985. 10.1016/j.neuroimage.2013.08.065 PubMed DOI

Rilling, J. K. , & Sanfey, A. G. (2011). The neuroscience of social decision‐making. Current Opinion in Neurobiology, 62, 23–48. 10.1016/j.conb.2008.06.003 PubMed DOI

Seltzer, B. , & Pandya, D. N. (1989). Frontal lobe connections of the superior temporal sulcus in the rhesus monkey. Journal of Comparative Neurology, 281(1), 97–113. PubMed

Stephan, K. E. , Harrison, L. M. , Kiebel, S. J. , David, O. , Penny, W. D. , & Friston, K. J. (2007). Dynamic causal models of neural system dynamics: Current state and future extensions. Journal of Biosciences, 32(1), 129–144. 10.1007/s12038-007-0012-5 PubMed DOI PMC

Stephan, K. E. , Penny, W. D. , Daunizeau, J. , Moran, R. J. , & Friston, K. J. (2009). Bayesian model selection for group studies. NeuroImage, 46(4), 1004–1017. 10.1016/j.neuroimage.2009.03.025 PubMed DOI PMC

Uddin, L. Q. (2015). Salience processing and insular cortical function and dysfunction. Nature Reviews Neuroscience, 16(1), 55–61. 10.1038/nrn3857 PubMed DOI

van Damme, E. , Binmore, K. G. , Roth, A. E. , Samuelson, L. , Winter, E. , Bolton, G. E. , … Azar, O. H. (2014). How Werner Güth's ultimatum game shaped our understanding of social behavior. Journal of Economic Behavior and Organization, 108, 292–318. 10.1016/j.jebo.2014.10.014 DOI

Vogt, B. A. , Pandya, D. N. , & Rosene, D. L. (1987). Cingulate cortex of the rhesus monkey: I. Cortical afferents. The Journal of Comparative Neurology, 262(2), 271–289. 10.1002/cne.902620208 PubMed DOI

Wager, T. D. , & Nichols, T. E. (2003). Optimization of experimental design in fMRI: A general framework using a genetic algorithm. NeuroImage, 18(2), 293–309. 10.1016/S1053-8119(02)00046-0 PubMed DOI

Wang, G. , Li, J. , Li, Z. , Wei, M. , & Li, S. (2016). Medial frontal negativity reflects advantageous inequality aversion of proposers in the ultimatum game: An ERP study. Brain Research, 1639, 38–46. 10.1016/j.brainres.2016.02.040 PubMed DOI

Zheng, Y. , Cheng, X. , Xu, J. , Zheng, L. , Li, L. , Yang, G. , & Guo, X. (2017). Proposers' economic status affects behavioral and neural responses to unfairness. Frontiers in Psychology, 8, 1–8. 10.3389/fpsyg.2017.00847 PubMed DOI PMC

Dissecting social interaction: dual-fMRI reveals patterns of interpersonal brain-behavior relationships that dissociate among dimensions of social exchange