The neurobiology of rewards and values in social decision making (original) (raw)

References

  1. Kishida, K. T., King-Casas, B. & Montague, P. R. Neuroeconomic approaches to mental disorders. Neuron 67, 543–554 (2010).
    Article CAS PubMed PubMed Central Google Scholar
  2. Damasio, A. R., Tranel, D. & Damasio, H. Individuals with sociopathic behavior caused by frontal damage fail to respond autonomically to social stimuli. Behav. Brain Res. 41, 81–94 (1990).
    Article CAS PubMed Google Scholar
  3. Rangel, A., Camerer, C. & Montague, P. R. A framework for studying the neurobiology of value-based decision making. Nature Rev. Neurosci. 9, 545–556 (2008).
    Article CAS Google Scholar
  4. Kable, J. W. & Glimcher, P. W. The neurobiology of decision: consensus and controversy. Neuron 63, 733–745 (2009).
    Article CAS PubMed PubMed Central Google Scholar
  5. Chib, V. S., Rangel, A., Shimojo, S. & O'Doherty, J. P. Evidence for a common representation of decision values for dissimilar goods in human ventromedial prefrontal cortex. J. Neurosci. 29, 12315–12320 (2009).
    Article CAS PubMed PubMed Central Google Scholar
  6. Lebreton, M., Jorge, S., Michel, V., Thirion, B. & Pessiglione, M. An automatic valuation system in the human brain: evidence from functional neuroimaging. Neuron 64, 431–439 (2009).
    Article CAS PubMed Google Scholar
  7. Dunbar, R. I. M. & Shultz, S. Evolution in the social brain. Science 317, 1344–1347 (2007).
    Article CAS PubMed Google Scholar
  8. Peelen, M. V. & Downing, P. E. The neural basis of visual body perception. Nature Rev. Neurosci. 8, 636–648 (2007).
    Article CAS Google Scholar
  9. Amodio, D. M. & Frith, C. D. Meeting of minds: the medial frontal cortex and social cognition. Nature Rev. Neurosci. 7, 268–277 (2006).
    Article CAS Google Scholar
  10. Saxe, R. Uniquely human social cognition. Curr. Opin. Neurobiol. 16, 235–239 (2006).
    Article CAS PubMed Google Scholar
  11. Carter, M. C., Bowling, D. L., Reeck, C. & Huettel, S. A. A distinct role of the temporo-parietal junction in predicting socially guided decisions. Science 337, 109–111 (2012).
    Article CAS PubMed PubMed Central Google Scholar
  12. Adolphs, R. Conceptual challenges and directions for social neuroscience. Neuron 65, 752–767 (2010).
    Article CAS PubMed PubMed Central Google Scholar
  13. Aharon, I. et al. Beautiful faces have variable reward value: fMRI and behavioral evidence. Neuron 32, 537–551 (2001).
    Article CAS PubMed Google Scholar
  14. O'Doherty, J. P. et al. Beauty in a smile: the role of medial orbitofrontal cortex in facial attractiveness. Neuropsychologia 41, 147–155 (2003).
    Article CAS PubMed Google Scholar
  15. Kampe, K. K. W., Frith, C. D., Dolan, R. J. & Frith, U. Psychology: reward value of attractiveness and gaze. Nature 413, 589 (2001).
    Article CAS PubMed Google Scholar
  16. Winston, J. S., O'Doherty, J., Kilner, J. M., Perrett, D. I. & Dolan, R. J. Brain systems for assessing facial attractiveness. Neuropsychologia 45, 195–206 (2007).
    Article PubMed Google Scholar
  17. Todorov, A., Said, C. P., Oosterhof, N. N. & Engell, A. D. Task-invariant brain responses to the social value of faces. J. Cogn. Neurosci. 23, 2766–2781 (2011).
    Article PubMed Google Scholar
  18. Prévost, C., Pessiglione, M., Météreau, E., Cléry-Melin, M.-L. & Dreher, J.-C. Separate valuation subsystems for delay and effort decision costs. J. Neurosci. 30, 14080–14090 (2010).
    Article CAS PubMed PubMed Central Google Scholar
  19. Sescousse, G., Redouté, J. & Dreher, J.-C. The architecture of reward value coding in the human orbitofrontal cortex. J. Neurosci. 30, 13095–13104 (2010).
    Article CAS PubMed PubMed Central Google Scholar
  20. Spreckelmeyer, K. N. et al. Anticipation of monetary and social reward differently activates mesolimbic brain structures in men and women. Soc. Cogn. Affect. Neurosci. 4, 158–165 (2009).
    Article PubMed PubMed Central Google Scholar
  21. Rademacher, L. et al. Dissociation of neural networks for anticipation and consumption of monetary and social rewards. Neuroimage 49, 3276–3285 (2010).
    Article PubMed Google Scholar
  22. Lin, A., Adolphs, R. & Rangel, A. Social and monetary reward learning engage overlapping neural substrates. Soc. Cogn. Affect. Neurosci. 7, 274–281 (2012).
    Article PubMed Google Scholar
  23. Kim, H., Adolphs, R., O'Doherty, J. P. & Shimojo, S. Temporal isolation of neural processes underlying face preference decisions. Proc. Natl Acad. Sci. USA 104, 18253–18258 (2007).
    Article PubMed PubMed Central Google Scholar
  24. Smith, D. V. et al. Distinct value signals in anterior and posterior ventromedial prefrontal cortex. J. Neurosci. 30, 2490–2495 (2010).
    Article CAS PubMed PubMed Central Google Scholar
  25. Hayden, B. Y., Parikh, P. C., Deaner, R. O. & Platt, M. L. Economic principles motivating social attention in humans. Proc. Biol. Sci. 274, 1751–1756 (2007).
    Article PubMed PubMed Central Google Scholar
  26. Izuma, K., Saito, D. N. & Sadato, N. Processing of social and monetary rewards in the human striatum. Neuron 58, 284–294 (2008). This study shows that monetary gains and observed social gestures elicit largely overlapping patterns of BOLD activity in the striatum, therefore suggesting that both types of outcomes trigger related value computations.
    Article CAS PubMed Google Scholar
  27. Davey, C. G., Allen, N. B., Harrison, B. J., Dwyer, D. B. & Yücel, M. Being liked activates primary reward and midline self-related brain regions. Hum. Brain Mapp. 31, 660–668 (2010).
    PubMed Google Scholar
  28. Gunther Moor, B., van Leijenhorst, L., Rombouts, S. A. R. B., Crone, E. A. & Van der Molen, M. W. Do you like me? Neural correlates of social evaluation and developmental trajectories. Soc. Neurosci. 5, 461–482 (2010).
    Article PubMed Google Scholar
  29. Powers, K. E., Somerville, L. H., Kelley, W. M. & Heatherton, T. F. Rejection sensitivity polarizes striatal-medial prefrontal activity when anticipating social feedback. J. Cogn. Neurosci. 25, 1887–1895 (2013).
    Article PubMed PubMed Central Google Scholar
  30. Meshi, D., Morawetz, C. & Heekeren, H. R. Nucleus accumbens response to gains in reputation for the self relative to gains for others predicts social media use. Front. Hum. Neurosci. 7, 439 (2013).
    Article PubMed PubMed Central Google Scholar
  31. Morelli, S. A., Torre, J. B. & Eisenberger, N. I. The neural bases of feeling understood and not understood. Soc. Cogn. Affect. Neurosci. http://dx.doi.org/10.1093/scan/nst191 (2014).
  32. Cooper, J. C., Dunne, S., Furey, T. & O'Doherty, J. P. The role of the posterior temporal and medial prefrontal cortices in mediating learning from romantic interest and rejection. Cereb. Cortex http://dx.doi.org/10.1093/cercor/bht102 (2013).
  33. Zink, C. F. et al. Know your place: neural processing of social hierarchy in humans. Neuron 58, 273–283 (2008).
    Article CAS PubMed PubMed Central Google Scholar
  34. Eisenberger, N. I., Lieberman, M. D. & Williams, K. D. Does rejection hurt? An fMRI study of social exclusion. Science 302, 290–292 (2003).
    Article CAS PubMed Google Scholar
  35. Slavich, G. M., Way, B. M., Eisenberger, N. I. & Taylor, S. E. Neural sensitivity to social rejection is associated with inflammatory responses to social stress. Proc. Natl Acad. Sci. USA 107, 14817–14822 (2010).
    Article PubMed PubMed Central Google Scholar
  36. Dewall, C. N. et al. Acetaminophen reduces social pain: behavioral and neural evidence. Psychol. Sci. 21, 931–937 (2010).
    Article PubMed Google Scholar
  37. Kross, E., Berman, M. G., Mischel, W., Smith, E. E. & Wager, T. D. Social rejection shares somatosensory representations with physical pain. Proc. Natl Acad. Sci. USA 108, 6270–6275 (2011).
    Article PubMed PubMed Central Google Scholar
  38. Smith, D. V., Clithero, J. A., Boltuck, S. & Huettel, S. A. Functional connectivity with ventromedial prefrontal cortex reflects subjective value for social rewards. Soc. Cogn. Affect. Neurosci. http://dx.doi.org/10.1093/scan/nsu005 (2014).
  39. Izuma, K., Saito, D. N. & Sadato, N. Processing of the incentive for social approval in the ventral striatum during charitable donation. J. Cogn. Neurosci. 22, 621–631 (2010).
    Article PubMed Google Scholar
  40. Kohls, G. et al. The nucleus accumbens is involved in both the pursuit of social reward and the avoidance of social punishment. Neuropsychologia 51, 2062–2069 (2013).
    Article PubMed PubMed Central Google Scholar
  41. Chein, J., Albert, D., O'Brien, L., Uckert, K. & Steinberg, L. Peers increase adolescent risk taking by enhancing activity in the brain's reward circuitry. Dev. Sci. 14, F1–F10 (2011).
    Article PubMed PubMed Central Google Scholar
  42. Moll, J. et al. Human fronto–mesolimbic networks guide decisions about charitable donation. Proc. Natl Acad. Sci. USA 103, 15623–15628 (2006).
    Article CAS PubMed PubMed Central Google Scholar
  43. Harbaugh, W. T., Mayr, U. & Burghart, D. R. Neural responses to taxation and voluntary giving reveal motives for charitable donations. Science 316, 1622–1625 (2007).
    Article CAS PubMed Google Scholar
  44. Izuma, K., Saito, D. N. & Sadato, N. The roles of the medial prefrontal cortex and striatum in reputation processing. Soc. Neurosci. 5, 133–147 (2010).
    Article PubMed Google Scholar
  45. Hare, T. A., Camerer, C. F., Knoepfle, D. T. & Rangel, A. Value computations in ventral medial prefrontal cortex during charitable decision making incorporate input from regions involved in social cognition. J. Neurosci. 30, 583–590 (2010). This study shows that charitable donations involve increased functional connectivity between the vmPFC and TPJ, suggesting that the TPJ provides information for the vmPFC value computations.
    Article CAS PubMed PubMed Central Google Scholar
  46. Fareri, D. S., Niznikiewicz, M. A., Lee, V. K. & Delgado, M. R. Social network modulation of reward-related signals. J. Neurosci. 32, 9045–9052 (2012).
    Article CAS PubMed PubMed Central Google Scholar
  47. Delgado, M. R., Frank, R. H. & Phelps, E. A. Perceptions of moral character modulate the neural systems of reward during the trust game. Nature Neurosci. 8, 1611–1618 (2005).
    Article CAS PubMed Google Scholar
  48. King-Casas, B. et al. Getting to know you: reputation and trust in a two-person economic exchange. Science 308, 78–83 (2005). This study shows that repeated social interactions involve prediction-error computations in the striatum that resemble similar computations during non-social choices.
    Article CAS PubMed Google Scholar
  49. Baumgartner, T., Heinrichs, M., Vonlanthen, A., Fischbacher, U. & Fehr, E. Oxytocin shapes the neural circuitry of trust and trust adaptation in humans. Neuron 58, 639–650 (2008). This study demonstrates that oxytocin has specific influences on the behavioural and neural sensitivity to violations of trust during social interactions.
    Article CAS PubMed Google Scholar
  50. Phan, K. L., Sripada, C. S., Angstadt, M. & McCabe, K. Reputation for reciprocity engages the brain reward center. Proc. Natl Acad. Sci. USA 107, 13099–13104 (2010).
    Article PubMed PubMed Central Google Scholar
  51. Schultz, W. Multiple dopamine functions at different time courses. Annu. Rev. Neurosci. 30, 259–288 (2007).
    Article CAS PubMed Google Scholar
  52. Smith-Collins, A. P. R. et al. Specific neural correlates of successful learning and adaptation during social exchanges. Soc. Cogn. Affect. Neurosci. 8, 887–896 (2013).
    Article PubMed Google Scholar
  53. Baron, S. G., Gobbini, M. I., Engell, A. D. & Todorov, A. Amygdala and dorsomedial prefrontal cortex responses to appearance-based and behavior-based person impressions. Soc. Cogn. Affect. Neurosci. 6, 572–581 (2011).
    Article PubMed Google Scholar
  54. Fouragnan, E. et al. Reputational priors magnify striatal responses to violations of trust. J. Neurosci. 33, 3602–3611 (2013).
    Article CAS PubMed PubMed Central Google Scholar
  55. Jones, R. M. et al. Behavioral and neural properties of social reinforcement learning. J. Neurosci. 31, 13039–13045 (2011). This study demonstrates, with various behavioural and neural measures, that social gestures have similar reinforcing properties to those of non-social rewards.
    Article CAS PubMed PubMed Central Google Scholar
  56. Kosfeld, M., Heinrichs, M., Zak, P. J., Fischbacher, U. & Fehr, E. Oxytocin increases trust in humans. Nature 435, 673–676 (2005).
    Article CAS PubMed Google Scholar
  57. Behrens, T. E. J., Hunt, L. T., Woolrich, M. W. & Rushworth, M. F. S. Associative learning of social value. Nature 456, 245–249 (2008). This study shows that social and non-social information relevant for value-based choices is encoded by similar types of neural computations but that these computations are implemented in different neural structures.
    Article CAS PubMed PubMed Central Google Scholar
  58. Hampton, A. N., Bossaerts, P. & O'Doherty, J. P. Neural correlates of mentalizing-related computations during strategic interactions in humans. Proc. Natl Acad. Sci. USA 105, 6741–6746 (2008).
    Article PubMed PubMed Central Google Scholar
  59. Mobbs, D. et al. Key role for similarity in vicarious reward. Science 324, 900 (2009). This study shows that neural responses in value-related areas can be triggered vicariously when observing a positive outcome for another person and that these responses are modulated by the perceived similarity between the observer and the observee.
    Article CAS PubMed PubMed Central Google Scholar
  60. Braams, B. R. et al. Reward-related neural responses are dependent on the beneficiary. Soc. Cogn. Affect. Neurosci. http://dx.doi.org/10.1093/scan/nst077 (2013).
  61. Singer, T. et al. Empathy for pain involves the affective but not sensory components of pain. Science 303, 1157–1162 (2004).
    Article CAS PubMed Google Scholar
  62. Wicker, B. et al. Both of us disgusted in my insula: the common neural basis of seeing and feeling disgust. Neuron 40, 655–664 (2003).
    Article CAS PubMed Google Scholar
  63. Krach, S. et al. Your flaws are my pain: linking empathy to vicarious embarrassment. PLoS ONE 6, e18675 (2011).
    Article CAS PubMed PubMed Central Google Scholar
  64. Hein, G., Silani, G., Preuschoff, K., Batson, C. D. & Singer, T. Neural responses to ingroup and outgroup members' suffering predict individual differences in costly helping. Neuron 68, 149–160 (2010).
    Article CAS PubMed Google Scholar
  65. Singer, T. et al. Empathic neural responses are modulated by the perceived fairness of others. Nature 439, 466–469 (2006).
    Article CAS PubMed PubMed Central Google Scholar
  66. Burke, C. J., Tobler, P. N., Schultz, W. & Baddeley, M. Striatal BOLD response reflects the impact of herd information on financial decisions. Front. Hum. Neurosci. 4, 48 (2010).
    PubMed PubMed Central Google Scholar
  67. De Martino, B., O'Doherty, J. P., Ray, D., Bossaerts, P. & Camerer, C. In the mind of the market: theory of mind biases value computation during financial bubbles. Neuron 79, 1222–1231 (2013).
    Article CAS PubMed PubMed Central Google Scholar
  68. Cooper, J. C., Kreps, T. A., Wiebe, T., Pirkl, T. & Knutson, B. When giving is good: ventromedial prefrontal cortex activation for others' intentions. Neuron 67, 511–521 (2010).
    Article CAS PubMed PubMed Central Google Scholar
  69. Janowski, V., Camerer, C. & Rangel, A. Empathic choice involves vmPFC value signals that are modulated by social processing implemented in IPL. Soc. Cogn. Affect. Neurosci. 8, 201–208 (2012).
    Article PubMed PubMed Central Google Scholar
  70. Nicolle, A. et al. An agent independent axis for executed and modeled choice in medial prefrontal cortex. Neuron 75, 1114–1121 (2012). This study shows that neural value signals in the vmPFC (versus those in the dmPFC) do not generically encode outcomes for oneself (versus another person) but rather represent values for choices that the agent executes him- or herself (versus only simulates cognitively).
    Article CAS PubMed PubMed Central Google Scholar
  71. Olsson, A. & Phelps, E. A. Social learning of fear. Nature Neurosci. 10, 1095–1102 (2007).
    Article CAS PubMed Google Scholar
  72. Kuss, K. et al. A reward prediction error for charitable donations reveals outcome orientation of donators. Soc. Cogn. Affect. Neurosci. 8, 216–223 (2011).
    Article PubMed PubMed Central Google Scholar
  73. Cooper, J. C., Dunne, S., Furey, T. & O'Doherty, J. P. Human dorsal striatum encodes prediction errors during observational learning of instrumental actions. J. Cogn. Neurosci. 24, 106–118 (2012).
    Article PubMed Google Scholar
  74. Burke, C. J., Tobler, P. N., Baddeley, M. & Schultz, W. Neural mechanisms of observational learning. Proc. Natl Acad. Sci. USA 107, 14431–14436 (2010). This study shows that learning by observing another person involves two distinct types of signals in the dlPFC and vmPFC that relate to predictions errors about the other person's actions and outcomes, respectively.
    Article PubMed PubMed Central Google Scholar
  75. Suzuki, S. et al. Learning to simulate others' decisions. Neuron 74, 1125–1137 (2012).
    Article CAS PubMed Google Scholar
  76. Fehr, E. & Fischbacher, U. The nature of human altruism. Nature 425, 785–791 (2003).
    Article CAS PubMed Google Scholar
  77. Fliessbach, K. et al. Social comparison affects reward-related brain activity in the human ventral striatum. Science 318, 1305–1308 (2007).
    Article CAS PubMed Google Scholar
  78. Bault, N., Joffily, M., Rustichini, A. & Coricelli, G. Medial prefrontal cortex and striatum mediate the influence of social comparison on the decision process. Proc. Natl Acad. Sci. USA 108, 16044–16049 (2011).
    Article PubMed PubMed Central Google Scholar
  79. Fehr, E. & Schmidt, K. M. A theory of fairness, competition, and cooperation. Q. J. Econ. 114, 817–868 (1999).
    Article Google Scholar
  80. Tricomi, E., Rangel, A., Camerer, C. F. & O'Doherty, J. P. Neural evidence for inequality-averse social preferences. Nature 463, 1089–1091 (2010). This study demonstrates that social preferences for equitable outcomes are evident in neural value signals in the striatum and vmPFC.
    Article CAS PubMed Google Scholar
  81. Haruno, M. & Frith, C. D. Activity in the amygdala elicited by unfair divisions predicts social value orientation. Nature Neurosci. 13, 160–161 (2010).
    Article CAS PubMed Google Scholar
  82. Boyce, C. J., Brown, G. D. & Moore, S. C. Money and happiness: rank of income, not income, affects life satisfaction. Psychol. Sci. 21, 471–475 (2010).
    Article PubMed Google Scholar
  83. Pennisi, E. On the origin of cooperation. Science 325, 1196–1199 (2009).
    Article CAS PubMed Google Scholar
  84. Rilling, J. K. et al. Neural basis for social cooperation. Neuron 35, 395–405 (2002).
    Article CAS PubMed Google Scholar
  85. Decety, J., Jackson, P. L., Sommerville, J. A., Chaminade, T. & Meltzoff, A. N. The neural bases of cooperation and competition: an fMRI investigation. Neuroimage 23, 744–751 (2004).
    Article PubMed Google Scholar
  86. Yoshida, W., Seymour, B., Friston, K. J. & Dolan, R. J. Neural mechanisms of belief inference during cooperative games. J. Neurosci. 30, 10744–10751 (2010).
    Article CAS PubMed PubMed Central Google Scholar
  87. Krill, A. L. & Platek, S. M. Working together may be better: activation of reward centers during a cooperative maze task. PLoS ONE 7, e30613 (2012).
    Article CAS PubMed PubMed Central Google Scholar
  88. de Quervain, D. J.-F. et al. The neural basis of altruistic punishment. Science 305, 1254–1258 (2004).
    Article CAS PubMed Google Scholar
  89. White, S. F., Brislin, S. J., Sinclair, S. & Blair, J. R. Punishing unfairness: rewarding or the organization of a reactively aggressive response? Hum. Brain Mapp. 35, 2137–2147 (2013).
    Article PubMed PubMed Central Google Scholar
  90. Sanfey, A. G., Rilling, J. K., Aronson, J. A., Nystrom, L. E. & Cohen, J. D. The neural basis of economic decision-making in the ultimatum game. Science 300, 1755–1758 (2003).
    Article CAS PubMed Google Scholar
  91. Tabibnia, G., Satpute, A. B. & Lieberman, M. D. The sunny side of fairness: preference for fairness activates reward circuitry (and disregarding unfairness activates self-control circuitry). Psychol. Sci. 19, 339–347 (2008).
    Article PubMed Google Scholar
  92. Guroglu, B., Bos, W. V. D., Rombouts, S. A. R. B. & Crone, E. A. Unfair? It depends: neural correlates of fairness in social context. Soc. Cogn. Affect. Neurosci. 5, 414–423 (2010).
    Article PubMed PubMed Central Google Scholar
  93. Wright, N. D., Symmonds, M., Fleming, S. M. & Dolan, R. J. Neural segregation of objective and contextual aspects of fairness. J. Neurosci. 31, 5244–5252 (2011).
    Article CAS PubMed PubMed Central Google Scholar
  94. Zaki, J. & Mitchell, J. P. Equitable decision making is associated with neural markers of intrinsic value. Proc. Natl Acad. Sci. USA 108, 19761–19766 (2011).
    Article PubMed PubMed Central Google Scholar
  95. Dawes, C. T. et al. Neural basis of egalitarian behavior. Proc. Natl Acad. Sci. USA 109, 6479–6483 (2012).
    Article PubMed PubMed Central Google Scholar
  96. Baumgartner, T., Götte, L., Gügler, R. & Fehr, E. The mentalizing network orchestrates the impact of parochial altruism on social norm enforcement. Hum. Brain Mapp. 33, 1452–1469 (2012).
    Article PubMed Google Scholar
  97. Hsu, M., Anen, C. & Quartz, S. R. The right and the good: distributive justice and neural encoding of equity and efficiency. Science 320, 1092–1095 (2008).
    Article CAS PubMed Google Scholar
  98. Shenhav, A. & Greene, J. D. Moral judgments recruit domain-general valuation mechanisms to integrate representations of probability and magnitude. Neuron 67, 667–677 (2010).
    Article CAS PubMed Google Scholar
  99. Preuschoff, K., Quartz, S. R. & Bossaerts, P. Human insula activation reflects risk prediction errors as well as risk. J. Neurosci. 28, 2745–2752 (2008).
    Article CAS PubMed PubMed Central Google Scholar
  100. Klucharev, V., Hytönen, K., Rijpkema, M., Smidts, A. & Fernández, G. Reinforcement learning signal predicts social conformity. Neuron 61, 140–151 (2009).
    Article CAS PubMed Google Scholar
  101. Campbell-Meiklejohn, D. K., Bach, D. R., Roepstorff, A., Dolan, R. J. & Frith, C. D. How the opinion of others affects our valuation of objects. Curr. Biol. 20, 1165–1170 (2010).
    Article CAS PubMed PubMed Central Google Scholar
  102. Zaki, J., Schirmer, J. & Mitchell, J. P. Social influence modulates the neural computation of value. Psychol. Sci. 22, 894–900 (2011).
    Article PubMed Google Scholar
  103. Logothetis, N. K. What we can do and what we cannot do with fMRI. Nature 453, 869–878 (2008).
    Article CAS PubMed Google Scholar
  104. Klein, J. T. & Platt, M. L. Social information signaling by neurons in primate striatum. Curr. Biol. 23, 691–696 (2013). This study shows that social versus non-social rewards are processed by distinct types of neurons in the striatum of the macaque.
    Article CAS PubMed PubMed Central Google Scholar
  105. Báez-Mendoza, R., Harris, C. J. & Schultz, W. Activity of striatal neurons reflects social action and own reward. Proc. Natl Acad. Sci. USA 110, 16634–16639 (2013).
    Article PubMed PubMed Central Google Scholar
  106. Chang, S. W. C., Gariépy, J.-F. & Platt, M. L. Neuronal reference frames for social decisions in primate frontal cortex. Nature Neurosci. 16, 243–250 (2013).
    Article CAS PubMed Google Scholar
  107. Poldrack, R. A. Can cognitive processes be inferred from neuroimaging data? Trends Cogn. Sci. 10, 59–63 (2006).
    Article PubMed Google Scholar
  108. Spitzer, M., Fischbacher, U., Herrnberger, B., Grön, G. & Fehr, E. The neural signature of social norm compliance. Neuron 56, 185–196 (2007).
    Article CAS PubMed Google Scholar
  109. Striepens, N. et al. Oxytocin enhances attractiveness of unfamiliar female faces independent of the dopamine reward system. Psychoneuroendocrinology 39, 74–87 (2014).
    Article CAS PubMed Google Scholar
  110. Pessiglione, M., Seymour, B., Flandin, G., Dolan, R. J. & Frith, C. D. Dopamine-dependent prediction errors underpin reward-seeking behaviour in humans. Nature 442, 1042–1045 (2006).
    Article CAS PubMed PubMed Central Google Scholar
  111. Grill-Spector, K., Henson, R. & Martin, A. Repetition and the brain: neural models of stimulus-specific effects. Trends Cogn. Sci. 10, 14–23 (2006).
    Article PubMed Google Scholar
  112. Norman, K. A., Polyn, S. M., Detre, G. J. & Haxby, J. V. Beyond mind-reading: multi-voxel pattern analysis of fMRI data. Trends Cogn. Sci. 10, 424–430 (2006).
    Article PubMed Google Scholar
  113. Baumgartner, T., Knoch, D., Hotz, P., Eisenegger, C. & Fehr, E. Dorsolateral and ventromedial prefrontal cortex orchestrate normative choice. Nature Neurosci. 14, 1468–1474 (2011).
    Article CAS PubMed Google Scholar
  114. Morishima, Y., Schunk, D., Bruhin, A., Ruff, C. C. & Fehr, E. Linking brain structure and activation in temporoparietal junction to explain the neurobiology of human altruism. Neuron 75, 73–79 (2012). This study shows that the individual tendency for altruistic giving is systematically related to both the structure and the functional response profile of the TPJ.
    Article CAS PubMed Google Scholar
  115. van den Bos, W., Talwar, A. & McClure, S. M. Neural correlates of reinforcement learning and social preferences in competitive bidding. J. Neurosci. 33, 2137–2146 (2013).
    Article CAS PubMed PubMed Central Google Scholar
  116. Seymour, B. & McClure, S. M. Anchors, scales and the relative coding of value in the brain. Curr. Opin. Neurobiol. 18, 173–178 (2008).
    Article CAS PubMed Google Scholar
  117. Han, S. & Northoff, G. Culture-sensitive neural substrates of human cognition: a transcultural neuroimaging approach. Nature Rev. Neurosci. 9, 646–654 (2008).
    Article CAS Google Scholar
  118. Pleger, B. et al. Influence of dopaminergically mediated reward on somatosensory decision-making. PLoS Biol. 7, e1000164 (2009).
    Article CAS PubMed PubMed Central Google Scholar
  119. Driver, J., Blankenburg, F., Bestmann, S., Vanduffel, W. & Ruff, C. C. Concurrent brain-stimulation and neuroimaging for studies of cognition. Trends Cogn. Sci. 13, 319–327 (2009).
    Article PubMed Google Scholar
  120. Cho, S. S. & Strafella, A. P. rTMS of the left dorsolateral prefrontal cortex modulates dopamine release in the ipsilateral anterior cingulate cortex and orbitofrontal cortex. PLoS ONE 4, e6725 (2009).
    Article CAS PubMed PubMed Central Google Scholar
  121. Friston, K. J. Functional and effective connectivity: a review. Brain Connect. 1, 13–36 (2011).
    Article PubMed Google Scholar
  122. Berridge, K. C. & Kringelbach, M. L. Affective neuroscience of pleasure: reward in humans and animals. Psychopharmacology 199, 457–480 (2008).
    Article CAS PubMed PubMed Central Google Scholar
  123. Padoa-Schioppa, C. & Assad, J. A. Neurons in the orbitofrontal cortex encode economic value. Nature 441, 223–226 (2006).
    Article CAS PubMed PubMed Central Google Scholar
  124. Morrison, S. E. & Salzman, C. D. Re-valuing the amygdala. Curr. Opin. Neurobiol. 20, 221–230 (2010).
    Article CAS PubMed PubMed Central Google Scholar
  125. Rushworth, M. F. S. & Behrens, T. E. J. Choice, uncertainty and value in prefrontal and cingulate cortex. Nature Neurosci. 11, 389–397 (2008).
    Article CAS PubMed Google Scholar
  126. Leknes, S. & Tracey, I. A common neurobiology for pain and pleasure. Nature Rev. Neurosci. 9, 314–320 (2008).
    Article CAS Google Scholar
  127. Schultz, W., Dayan, P. & Montague, P. R. A neural substrate of prediction and reward. Science 275, 1593–1599 (1997).
    Article CAS PubMed Google Scholar
  128. D'Ardenne, K., McClure, S. M., Nystrom, L. E. & Cohen, J. D. BOLD responses reflecting dopaminergic signals in the human ventral tegmental area. Science 319, 1264–1267 (2008).
    Article CAS PubMed Google Scholar
  129. O'Doherty, J. P. Reward representations and reward-related learning in the human brain: insights from neuroimaging. Curr. Opin. Neurobiol. 14, 769–776 (2004).
    Article CAS PubMed Google Scholar
  130. Hare, T. A., O'Doherty, J., Camerer, C. F., Schultz, W. & Rangel, A. Dissociating the role of the orbitofrontal cortex and the striatum in the computation of goal values and prediction errors. J. Neurosci. 28, 5623–5630 (2008).
    Article CAS PubMed PubMed Central Google Scholar
  131. Wallis, J. D. & Kennerley, S. W. Heterogeneous reward signals in prefrontal cortex. Curr. Opin. Neurobiol. 20, 191–198 (2010).
    Article CAS PubMed PubMed Central Google Scholar
  132. Sripada, C., Angstadt, M., Liberzon, I., McCabe, K. & Phan, K. L. Aberrant reward center response to partner reputation during a social exchange game in generalized social phobia. Depress. Anxiety 30, 353–361 (2013).
    Article PubMed PubMed Central Google Scholar
  133. Chiu, P. H. et al. Self responses along cingulate cortex reveal quantitative neural phenotype for high-functioning autism. Neuron 57, 463–473 (2008).
    Article CAS PubMed PubMed Central Google Scholar
  134. King-Casas, B. et al. The rupture and repair of cooperation in borderline personality disorder. Science 321, 806–810 (2008).
    Article CAS PubMed PubMed Central Google Scholar
  135. Rilling, J. K., Sanfey, A. G., Aronson, J. A., Nystrom, L. E. & Cohen, J. D. Opposing BOLD responses to reciprocated and unreciprocated altruism in putative reward pathways. Neuroreport 15, 2539–2543 (2004).
    Article PubMed Google Scholar
  136. Izuma, K., Matsumoto, K., Camerer, C. F. & Adolphs, R. Insensitivity to social reputation in autism. Proc. Natl Acad. Sci. USA 108, 17302–17307 (2011).
    Article PubMed PubMed Central Google Scholar
  137. Stone, V. E., Cosmides, L., Tooby, J., Kroll, N. & Knight, R. T. Selective impairment of reasoning about social exchange in a patient with bilateral limbic system damage. Proc. Natl Acad. Sci. USA 99, 11531–11536 (2002).
    Article CAS PubMed PubMed Central Google Scholar
  138. Krajbich, I., Adolphs, R., Tranel, D., Denburg, N. L. & Camerer, C. F. Economic games quantify diminished sense of guilt in patients with damage to the prefrontal cortex. J. Neurosci. 29, 2188–2192 (2009).
    Article CAS PubMed PubMed Central Google Scholar
  139. Koenigs, M. & Tranel, D. Irrational economic decision-making after ventromedial prefrontal damage: evidence from the ultimatum game. J. Neurosci. 27, 951–956 (2007).
    Article CAS PubMed PubMed Central Google Scholar
  140. Moretti, L., Dragone, D. & Pellegrino, G. D. Reward and social valuation deficits following ventromedial prefrontal damage. J. Cogn. Neurosci. 21, 128–140 (2009).
    Article PubMed Google Scholar
  141. Knoch, D., Pascual-Leone, A., Meyer, K., Treyer, V. & Fehr, E. Diminishing reciprocal fairness by disrupting the right prefrontal cortex. Science 314, 829–832 (2006).
    Article CAS PubMed Google Scholar
  142. Knoch, D., Schneider, F., Schunk, D., Hohmann, M. & Fehr, E. Disrupting the prefrontal cortex diminishes the human ability to build a good reputation. Proc. Natl Acad. Sci. USA 106, 20895–20899 (2009).
    Article PubMed PubMed Central Google Scholar
  143. Ruff, C. C., Ugazio, G. & Fehr, E. Changing social norm compliance with noninvasive brain stimulation. Science 342, 482–484 (2013).
    Article CAS PubMed Google Scholar
  144. Deaner, R. O., Khera, A. V. & Platt, M. L. Monkeys pay per view: adaptive valuation of social images by rhesus macaques. Curr. Biol. 15, 543–548 (2005).
    Article CAS PubMed Google Scholar
  145. Rudebeck, P. H., Buckley, M. J., Walton, M. E. & Rushworth, M. F. S. A role for the macaque anterior cingulate gyrus in social valuation. Science 313, 1310–1312 (2006).
    Article CAS PubMed Google Scholar
  146. Barraclough, D. J., Conroy, M. L. & Lee, D. Prefrontal cortex and decision making in a mixed-strategy game. Nature Neurosci. 7, 404–410 (2004).
    Article CAS PubMed Google Scholar
  147. Chang, S. W., Winecoff, A. A. & Platt, M. L. Vicarious reinforcement in rhesus macaques (Macaca Mulatta). Front. Neurosci. 5, 27 (2011).
    Article PubMed PubMed Central Google Scholar
  148. Chang, S. W., Barter, J. W., Ebitz, R. B., Watson, K. K. & Platt, M. L. Inhaled oxytocin amplifies both vicarious reinforcement and self reinforcement in rhesus macaques (Macaca mulatta). Proc. Natl Acad. Sci. USA 109, 959–964 (2012).
    Article PubMed PubMed Central Google Scholar
  149. Bonnie, K. E. & de Waal, F. B. M. Copying without rewards: socially influenced foraging decisions among brown capuchin monkeys. Animal Cogn. 10, 283–292 (2007).
    Article Google Scholar
  150. de Waal, F. B. M., Leimgruber, K. & Greenberg, A. R. Giving is self-rewarding for monkeys. Proc. Natl Acad. Sci. USA 105, 13685–13689 (2008).
    Article PubMed PubMed Central Google Scholar
  151. Hare, B. & Kwetuenda, S. Bonobos voluntarily share their own food with others. Curr. Biol. 20, R230–R231 (2010).
    Article CAS PubMed Google Scholar
  152. Burkart, J. M., Fehr, E., Efferson, C. & Schaik, C. P. V. Other-regarding preferences in a non-human primate: common marmosets provision food altruistically. Proc. Natl Acad. Sci. USA 104, 19762–19766 (2007).
    Article PubMed PubMed Central Google Scholar
  153. Warneken, F. & Tomasello, M. Altruistic helping in human infants and young chimpanzees. Science 311, 1301–1303 (2006).
    Article CAS PubMed Google Scholar
  154. Wolkenten, M. V., Brosnan, S. F. & de Waal, F. B. M. Inequity responses of monkeys modified by effort. Proc. Natl Acad. Sci. USA 104, 18854–18859 (2007).
    Article PubMed PubMed Central Google Scholar
  155. Brosnan, S. F. & de Waal, F. B. M. Monkeys reject unequal pay. Nature 425, 297–299 (2003).
    Article CAS PubMed Google Scholar
  156. Silk, J. B. et al. Chimpanzees are indifferent to the welfare of unrelated group members. Nature 437, 1357–1359 (2005).
    Article CAS PubMed Google Scholar
  157. Bräuer, J., Call, J. & Tomasello, M. Are apes really inequity averse? Proc. Biol. Sci. 273, 3123–3128 (2006).
    Article PubMed PubMed Central Google Scholar
  158. Jensen, K., Call, J. & Tomasello, M. Chimpanzees are rational maximizers in an ultimatum game. Science 318, 107–109 (2007).
    Article CAS PubMed Google Scholar
  159. Parr, L. A., Hecht, E., Barks, S. K., Preuss, T. M. & Votaw, J. R. Face processing in the chimpanzee brain. Curr. Biol. 19, 50–53 (2009).
    Article CAS PubMed Google Scholar
  160. Rilling, J. K. et al. A comparison of resting-state brain activity in humans and chimpanzees. Proc. Natl Acad. Sci. USA 104, 17146–17151 (2007).
    Article PubMed PubMed Central Google Scholar

Download references