Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Review Article
  • Published:

The neurobiology of rewards and values in social decision making

Key Points

  • Two historically separate lines of research on social versus non-social decision making are converging in a focus on neural value computations. These value signals may reflect neural mechanisms that enable unified control of behaviour across social and non-social contexts.

  • Two competing theoretical accounts propose that neural value computations underlying both types of choice may either be performed by the very same neurons — therefore providing a 'common motivational currency' for social and non-social information — or that they may involve different, functionally specialized neuronal populations. There is evidence for both accounts, but existing methodical limitations preclude unambiguous support for just one of them.

  • Social versus non-social choices differ in terms of functional connectivity between regions that are involved in representing value signals and other brain areas that specifically encode social-cognitive functions. This suggests that social and non-social choices mainly differ in the information that is used as input for similar neural value computations.

  • Neural value computations and associated patterns of functional connectivity have been documented for social decisions in three distinct classes of situation that differ with respect to the target and the reference frame of valuation. These classes respectively reflect situations in which interactions with other people are rewarding to the agent, situations in which agents assess value vicariously for other people they observe, and situations in which agents behave in line with abstract social principles.

  • Studies in animal models suggest that some of the social neural value signals are also computed in the non-human primate brain but by different neuronal populations than comparable non-social value signals.

  • A few results from clinical and neural intervention studies show that disruptions of some of these value signals can change social decision making, suggesting an important causal role of these signals in the control of behaviour in social contexts.

Abstract

How does our brain choose the best course of action? Choices between material goods are thought to be steered by neural value signals that encode the rewarding properties of the choice options. Social decisions, by contrast, are traditionally thought to rely on neural representations of the self and others. However, recent studies show that many types of social decisions may also involve neural value computations. This suggests a unified mechanism for motivational control of behaviour that may incorporate both social and non-social factors. In this Review, we outline a theoretical framework that may help to identify possible overlaps and differences between the neural processes that guide social and non-social decision making.

This is a preview of subscription content, access via your institution

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Two schemas for neural value computation in social versus non-social contexts.
Figure 2: Social influences on brain activity during reward processing.
Figure 3: Social influences on brain activity during choice behaviour and learning.

Similar content being viewed by others

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

Acknowledgements

Preparation of this article was made possible by funding from the Swiss National Science Foundation (SNSF) to C.C.R. and E.F. E.F. also acknowledges support from the European Research Council Grant on the “Foundations of Economic Preferences”. The authors thank P. Tobler, S. Huettel and two anonymous referees for helpful comments.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Christian C. Ruff or Ernst Fehr.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

PowerPoint slides

Glossary

Delay discounting

The systematic decrease in a given item's value with increasing delay until it will be received. Excessive delay discounting is often thought to underlie impulsive choices.

Trust game

An experimental paradigm to measure trust between anonymous players. Player 1 decides how much of his or her money to transfer to player 2. The transferred amount is multiplied by a factor >1 before player 2 decides how much money to give back to player 1, thus honouring the trust evident in the initial transfer.

Reciprocity

A behavioural strategy whereby an individual responds to another agent's kind (or hostile) action with a kind (or hostile) action. Reciprocity lies at the heart of 'tit-for-tat' and is often thought to be an important motivation for altruism.

Priors

Beliefs about a state of the world that can strongly influence the interpretation of new information. The concept is taken from Bayesian statistics, where incoming evidence is multiplied with a prior estimate to determine an event's posterior likelihood (which is the new prior before the next information arrives).

Proximate mechanism

Biological mechanism that enables an organism to behave in the way it does. These mechanisms develop in response to the ultimate evolutionary causes for a given behaviour.

Inequality aversion

Distaste for inequality in the distribution of outcomes. This concept — also referred to as inequity aversion — may motivate altruistic or fairness-related choices.

Prisoner's dilemma game

An experimental paradigm to measure social cooperation. Two anonymous players decide whether to cooperate or to defect. For each individual player, unilateral cooperation yields the worst material payoff, whereas unilateral defection leads to the best material payoff. However, bilateral cooperation leads to a better payoff for each of the players than bilateral defection.

Ultimatum game

An experimental paradigm to measure fairness preferences. Two anonymous players decide how to split a given sum of money. Player 1 can make an offer on how to split the money between the two players. Player 2 can accept or reject the offer. In case of acceptance, the decision will be implemented, but in case of rejection both players receive nothing. By rejecting positive but unfair offers, player 2 can punish player 1 at the cost of receiving nothing.

Reverse inference

A scientific strategy of inferring the presence of a specific mental process when observing brain activity that has been correlated in previous studies with this process. This strategy can lead to invalid conclusions when used carelessly (because activity in a brain region may often be triggered by several different mental processes) and should be applied with caution.

Repetition suppression

Phenomenon that repetition of the same stimulus elicits reduced activity in neurons specialized for this stimulus, possibly reflecting adaptation.

Multivariate pattern analyses

Neuroimaging analyses that do not examine activity changes in each voxel in isolation but rather identify patterns of activity changes across spatially distributed voxels.

Adaptive coding

Neural computations that are not fixed but adapt to the environment. For example, the same range of neural activity can encode different value ranges in different settings.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ruff, C., Fehr, E. The neurobiology of rewards and values in social decision making. Nat Rev Neurosci 15, 549–562 (2014). https://doi.org/10.1038/nrn3776

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nrn3776

This article is cited by

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing