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.
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
Open Access articles citing this article.
Neuro-computational mechanisms and individual biases in action-outcome learning under moral conflict
Nature Communications Open Access 06 March 2023
Mindfulness training reduces slippery slope effects in moral decision-making and moral judgment
Scientific Reports Open Access 20 February 2023
Social feedback enhances learning in Williams syndrome
Scientific Reports Open Access 04 January 2023
Subscribe to this journal
Receive 12 print issues and online access
$189.00 per year
only $15.75 per issue
Rent or buy this article
Get just this article for as long as you need it
Prices may be subject to local taxes which are calculated during checkout
Kishida, K. T., King-Casas, B. & Montague, P. R. Neuroeconomic approaches to mental disorders. Neuron 67, 543–554 (2010).
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).
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).
Kable, J. W. & Glimcher, P. W. The neurobiology of decision: consensus and controversy. Neuron 63, 733–745 (2009).
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).
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).
Dunbar, R. I. M. & Shultz, S. Evolution in the social brain. Science 317, 1344–1347 (2007).
Peelen, M. V. & Downing, P. E. The neural basis of visual body perception. Nature Rev. Neurosci. 8, 636–648 (2007).
Amodio, D. M. & Frith, C. D. Meeting of minds: the medial frontal cortex and social cognition. Nature Rev. Neurosci. 7, 268–277 (2006).
Saxe, R. Uniquely human social cognition. Curr. Opin. Neurobiol. 16, 235–239 (2006).
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).
Adolphs, R. Conceptual challenges and directions for social neuroscience. Neuron 65, 752–767 (2010).
Aharon, I. et al. Beautiful faces have variable reward value: fMRI and behavioral evidence. Neuron 32, 537–551 (2001).
O'Doherty, J. P. et al. Beauty in a smile: the role of medial orbitofrontal cortex in facial attractiveness. Neuropsychologia 41, 147–155 (2003).
Kampe, K. K. W., Frith, C. D., Dolan, R. J. & Frith, U. Psychology: reward value of attractiveness and gaze. Nature 413, 589 (2001).
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).
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).
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).
Sescousse, G., Redouté, J. & Dreher, J.-C. The architecture of reward value coding in the human orbitofrontal cortex. J. Neurosci. 30, 13095–13104 (2010).
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).
Rademacher, L. et al. Dissociation of neural networks for anticipation and consumption of monetary and social rewards. Neuroimage 49, 3276–3285 (2010).
Lin, A., Adolphs, R. & Rangel, A. Social and monetary reward learning engage overlapping neural substrates. Soc. Cogn. Affect. Neurosci. 7, 274–281 (2012).
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).
Smith, D. V. et al. Distinct value signals in anterior and posterior ventromedial prefrontal cortex. J. Neurosci. 30, 2490–2495 (2010).
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).
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.
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).
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).
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).
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).
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).
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).
Zink, C. F. et al. Know your place: neural processing of social hierarchy in humans. Neuron 58, 273–283 (2008).
Eisenberger, N. I., Lieberman, M. D. & Williams, K. D. Does rejection hurt? An fMRI study of social exclusion. Science 302, 290–292 (2003).
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).
Dewall, C. N. et al. Acetaminophen reduces social pain: behavioral and neural evidence. Psychol. Sci. 21, 931–937 (2010).
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).
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).
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).
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).
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).
Moll, J. et al. Human fronto–mesolimbic networks guide decisions about charitable donation. Proc. Natl Acad. Sci. USA 103, 15623–15628 (2006).
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).
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).
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.
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).
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).
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.
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.
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).
Schultz, W. Multiple dopamine functions at different time courses. Annu. Rev. Neurosci. 30, 259–288 (2007).
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).
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).
Fouragnan, E. et al. Reputational priors magnify striatal responses to violations of trust. J. Neurosci. 33, 3602–3611 (2013).
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.
Kosfeld, M., Heinrichs, M., Zak, P. J., Fischbacher, U. & Fehr, E. Oxytocin increases trust in humans. Nature 435, 673–676 (2005).
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.
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).
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.
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).
Singer, T. et al. Empathy for pain involves the affective but not sensory components of pain. Science 303, 1157–1162 (2004).
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).
Krach, S. et al. Your flaws are my pain: linking empathy to vicarious embarrassment. PLoS ONE 6, e18675 (2011).
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).
Singer, T. et al. Empathic neural responses are modulated by the perceived fairness of others. Nature 439, 466–469 (2006).
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).
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).
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).
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).
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).
Olsson, A. & Phelps, E. A. Social learning of fear. Nature Neurosci. 10, 1095–1102 (2007).
Kuss, K. et al. A reward prediction error for charitable donations reveals outcome orientation of donators. Soc. Cogn. Affect. Neurosci. 8, 216–223 (2011).
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).
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.
Suzuki, S. et al. Learning to simulate others' decisions. Neuron 74, 1125–1137 (2012).
Fehr, E. & Fischbacher, U. The nature of human altruism. Nature 425, 785–791 (2003).
Fliessbach, K. et al. Social comparison affects reward-related brain activity in the human ventral striatum. Science 318, 1305–1308 (2007).
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).
Fehr, E. & Schmidt, K. M. A theory of fairness, competition, and cooperation. Q. J. Econ. 114, 817–868 (1999).
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.
Haruno, M. & Frith, C. D. Activity in the amygdala elicited by unfair divisions predicts social value orientation. Nature Neurosci. 13, 160–161 (2010).
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).
Pennisi, E. On the origin of cooperation. Science 325, 1196–1199 (2009).
Rilling, J. K. et al. Neural basis for social cooperation. Neuron 35, 395–405 (2002).
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).
Yoshida, W., Seymour, B., Friston, K. J. & Dolan, R. J. Neural mechanisms of belief inference during cooperative games. J. Neurosci. 30, 10744–10751 (2010).
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).
de Quervain, D. J.-F. et al. The neural basis of altruistic punishment. Science 305, 1254–1258 (2004).
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).
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).
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).
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).
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).
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).
Dawes, C. T. et al. Neural basis of egalitarian behavior. Proc. Natl Acad. Sci. USA 109, 6479–6483 (2012).
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).
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).
Shenhav, A. & Greene, J. D. Moral judgments recruit domain-general valuation mechanisms to integrate representations of probability and magnitude. Neuron 67, 667–677 (2010).
Preuschoff, K., Quartz, S. R. & Bossaerts, P. Human insula activation reflects risk prediction errors as well as risk. J. Neurosci. 28, 2745–2752 (2008).
Klucharev, V., Hytönen, K., Rijpkema, M., Smidts, A. & Fernández, G. Reinforcement learning signal predicts social conformity. Neuron 61, 140–151 (2009).
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).
Zaki, J., Schirmer, J. & Mitchell, J. P. Social influence modulates the neural computation of value. Psychol. Sci. 22, 894–900 (2011).
Logothetis, N. K. What we can do and what we cannot do with fMRI. Nature 453, 869–878 (2008).
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.
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).
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).
Poldrack, R. A. Can cognitive processes be inferred from neuroimaging data? Trends Cogn. Sci. 10, 59–63 (2006).
Spitzer, M., Fischbacher, U., Herrnberger, B., Grön, G. & Fehr, E. The neural signature of social norm compliance. Neuron 56, 185–196 (2007).
Striepens, N. et al. Oxytocin enhances attractiveness of unfamiliar female faces independent of the dopamine reward system. Psychoneuroendocrinology 39, 74–87 (2014).
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).
Grill-Spector, K., Henson, R. & Martin, A. Repetition and the brain: neural models of stimulus-specific effects. Trends Cogn. Sci. 10, 14–23 (2006).
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).
Baumgartner, T., Knoch, D., Hotz, P., Eisenegger, C. & Fehr, E. Dorsolateral and ventromedial prefrontal cortex orchestrate normative choice. Nature Neurosci. 14, 1468–1474 (2011).
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.
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).
Seymour, B. & McClure, S. M. Anchors, scales and the relative coding of value in the brain. Curr. Opin. Neurobiol. 18, 173–178 (2008).
Han, S. & Northoff, G. Culture-sensitive neural substrates of human cognition: a transcultural neuroimaging approach. Nature Rev. Neurosci. 9, 646–654 (2008).
Pleger, B. et al. Influence of dopaminergically mediated reward on somatosensory decision-making. PLoS Biol. 7, e1000164 (2009).
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).
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).
Friston, K. J. Functional and effective connectivity: a review. Brain Connect. 1, 13–36 (2011).
Berridge, K. C. & Kringelbach, M. L. Affective neuroscience of pleasure: reward in humans and animals. Psychopharmacology 199, 457–480 (2008).
Padoa-Schioppa, C. & Assad, J. A. Neurons in the orbitofrontal cortex encode economic value. Nature 441, 223–226 (2006).
Morrison, S. E. & Salzman, C. D. Re-valuing the amygdala. Curr. Opin. Neurobiol. 20, 221–230 (2010).
Rushworth, M. F. S. & Behrens, T. E. J. Choice, uncertainty and value in prefrontal and cingulate cortex. Nature Neurosci. 11, 389–397 (2008).
Leknes, S. & Tracey, I. A common neurobiology for pain and pleasure. Nature Rev. Neurosci. 9, 314–320 (2008).
Schultz, W., Dayan, P. & Montague, P. R. A neural substrate of prediction and reward. Science 275, 1593–1599 (1997).
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).
O'Doherty, J. P. Reward representations and reward-related learning in the human brain: insights from neuroimaging. Curr. Opin. Neurobiol. 14, 769–776 (2004).
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).
Wallis, J. D. & Kennerley, S. W. Heterogeneous reward signals in prefrontal cortex. Curr. Opin. Neurobiol. 20, 191–198 (2010).
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).
Chiu, P. H. et al. Self responses along cingulate cortex reveal quantitative neural phenotype for high-functioning autism. Neuron 57, 463–473 (2008).
King-Casas, B. et al. The rupture and repair of cooperation in borderline personality disorder. Science 321, 806–810 (2008).
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).
Izuma, K., Matsumoto, K., Camerer, C. F. & Adolphs, R. Insensitivity to social reputation in autism. Proc. Natl Acad. Sci. USA 108, 17302–17307 (2011).
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).
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).
Koenigs, M. & Tranel, D. Irrational economic decision-making after ventromedial prefrontal damage: evidence from the ultimatum game. J. Neurosci. 27, 951–956 (2007).
Moretti, L., Dragone, D. & Pellegrino, G. D. Reward and social valuation deficits following ventromedial prefrontal damage. J. Cogn. Neurosci. 21, 128–140 (2009).
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).
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).
Ruff, C. C., Ugazio, G. & Fehr, E. Changing social norm compliance with noninvasive brain stimulation. Science 342, 482–484 (2013).
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).
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).
Barraclough, D. J., Conroy, M. L. & Lee, D. Prefrontal cortex and decision making in a mixed-strategy game. Nature Neurosci. 7, 404–410 (2004).
Chang, S. W., Winecoff, A. A. & Platt, M. L. Vicarious reinforcement in rhesus macaques (Macaca Mulatta). Front. Neurosci. 5, 27 (2011).
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).
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).
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).
Hare, B. & Kwetuenda, S. Bonobos voluntarily share their own food with others. Curr. Biol. 20, R230–R231 (2010).
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).
Warneken, F. & Tomasello, M. Altruistic helping in human infants and young chimpanzees. Science 311, 1301–1303 (2006).
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).
Brosnan, S. F. & de Waal, F. B. M. Monkeys reject unequal pay. Nature 425, 297–299 (2003).
Silk, J. B. et al. Chimpanzees are indifferent to the welfare of unrelated group members. Nature 437, 1357–1359 (2005).
Bräuer, J., Call, J. & Tomasello, M. Are apes really inequity averse? Proc. Biol. Sci. 273, 3123–3128 (2006).
Jensen, K., Call, J. & Tomasello, M. Chimpanzees are rational maximizers in an ultimatum game. Science 318, 107–109 (2007).
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).
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).
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.
The authors declare no competing financial interests.
- 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.
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.
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
About this article
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
This article is cited by
Mindfulness training reduces slippery slope effects in moral decision-making and moral judgment
Scientific Reports (2023)
Neuro-computational mechanisms and individual biases in action-outcome learning under moral conflict
Nature Communications (2023)
Social feedback enhances learning in Williams syndrome
Scientific Reports (2023)
Social rejection influences prosocial sharing decision-making in inequality contexts
Current Psychology (2023)
Frontal neurons driving competitive behaviour and ecology of social groups