Studies of reward learning have implicated the striatum as part of a neural circuit that guides and adjusts future behavior on the basis of reward feedback. Here we investigate whether prior social and moral information about potential trading partners affects this neural circuitry. Participants made risky choices about whether to trust hypothetical trading partners after having read vivid descriptions of life events indicating praiseworthy, neutral or suspect moral character. Despite equivalent reinforcement rates for all partners, participants were persistently more likely to make risky choices with the 'good' partner. As expected from previous studies, activation of the caudate nucleus differentiated between positive and negative feedback, but only for the 'neutral' partner. Notably, it did not do so for the 'good' partner and did so only weakly for the 'bad' partner, suggesting that prior social and moral perceptions can diminish reliance on feedback mechanisms in the neural circuitry of trial-and-error reward learning.
This is a preview of subscription content, access via your institution
Open Access articles citing this article.
Nature Communications Open Access 20 October 2022
Current Psychology Open Access 12 August 2022
Communications Biology Open Access 25 November 2021
Subscribe to Journal
Get full journal access for 1 year
only $6.58 per issue
All prices are NET prices.
VAT will be added later in the checkout.
Tax calculation will be finalised during checkout.
Get time limited or full article access on ReadCube.
All prices are NET prices.
White, N.M. Mnemonic functions of the basal ganglia. Curr. Opin. Neurobiol. 7, 164–169 (1997).
Packard, M.G. & Knowlton, B.J. Learning and memory functions of the basal ganglia. Annu. Rev. Neurosci. 25, 563–593 (2002).
Takikawa, Y., Kawagoe, R. & Hikosaka, O. Reward-dependent spatial selectivity of anticipatory activity in monkey caudate neurons. J. Neurophysiol. 87, 508–515 (2002).
Shohamy, D. et al. Cortico-striatal contributions to feedback-based learning: converging data from neuroimaging and neuropsychology. Brain 127, 851–859 (2004).
Poldrack, R.A. et al. Interactive memory systems in the human brain. Nature 414, 546–550 (2001).
Filoteo, J.V. et al. Cortical and subcortical brain regions involved in rule-based category learning. Neuroreport 16, 111–115 (2005).
Elliott, R., Sahakian, B.J., Michael, A., Paykel, E.S. & Dolan, R.J. Abnormal neural response to feedback on planning and guessing tasks in patients with unipolar depression. Psychol. Med. 28, 559–571 (1998).
Delgado, M.R., Nystrom, L.E., Fissell, C., Noll, D.C. & Fiez, J.A. Tracking the hemodynamic responses to reward and punishment in the striatum. J. Neurophysiol. 84, 3072–3077 (2000).
Cromwell, H.C. & Schultz, W. Effects of expectations for different reward magnitudes on neuronal activity in primate striatum. J. Neurophysiol. 89, 2823–2838 (2003).
Delgado, M.R., Locke, H.M., Stenger, V.A. & Fiez, J.A. Dorsal striatum responses to reward and punishment: effects of valence and magnitude manipulations. Cogn. Affect. Behav. Neurosci. 3, 27–38 (2003).
Delgado, M.R., Miller, M.M., Inati, S. & Phelps, E.A. An fMRI study of reward-related probability learning. Neuroimage 24, 862–873 (2005).
Haruno, M. et al. A neural correlate of reward-based behavioral learning in caudate nucleus: a functional magnetic resonance imaging study of a stochastic decision task. J. Neurosci. 24, 1660–1665 (2004).
Tricomi, E.M., Delgado, M.R. & Fiez, J.A. Modulation of caudate activity by action contingency. Neuron 41, 281–292 (2004).
O'Doherty, J. et al. Dissociable roles of ventral and dorsal striatum in instrumental conditioning. Science 304, 452–454 (2004).
Barto, A.G. Adaptive critics and the basal ganglia. in Models of Information Processing in the Basal Ganglia (eds. Houk, J.C., Davis, J.L. & Beiser, D.G.) 215–232 (MIT Press, Cambridge, Massachusetts, 1995).
King-Casas, B. et al. Getting to know you: reputation and trust in a two-person economic exchange. Science 308, 78–83 (2005).
Frank, R.H., Gilovich, T. & Regan, D. The evolution of one-shot cooperation. Ethol. Sociobiol. 14, 247–256 (1993).
Frank, R.H. What Price the Moral High Ground? (Princeton Univ. Press, Princeton, New Jersey, 2004).
Camerer, C.F. & Weigelt, K. Experimental tests of a sequential equilibrium reputation model. Econometrica 56, 1–36 (1988).
Berg, J., Dickhaut, J. & McCabe, K. Trust, reciprocity, and social history. Games Econ. Behav. 10, 122–142 (1995).
Rilling, J. et al. A neural basis for social cooperation. Neuron 35, 395–405 (2002).
Glimcher, P.W. & Rustichini, A. Neuroeconomics: the consilience of brain and decision. Science 306, 447–452 (2004).
Coleman, J.S. Foundations of Social Theory (Belknap Press, Cambridge, Massachusetts, 1990).
Schultz, W. & Dickinson, A. Neuronal coding of prediction errors. Annu. Rev. Neurosci. 23, 473–500 (2000).
Delgado, M.R., Stenger, V.A. & Fiez, J.A. Motivation-dependent responses in the human caudate nucleus. Cereb. Cortex 14, 1022–1030 (2004).
O'Doherty, J.P. Reward representations and reward-related learning in the human brain: insights from neuroimaging. Curr. Opin. Neurobiol. 14, 769–776 (2004).
Knutson, B., Adams, C.M., Fong, G.W. & Hommer, D. Anticipation of increasing monetary reward selectively recruits nucleus accumbens. J. Neurosci. 21, RC159 (2001).
Breiter, H.C., Aharon, I., Kahneman, D., Dale, A. & Shizgal, P. Functional imaging of neural responses to expectancy and experience of monetary gains and losses. Neuron 30, 619–639 (2001).
Carter, C.S. et al. Anterior cingulate cortex, error detection, and the online monitoring of performance. Science 280, 747–749 (1998).
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).
Ridderinkhof, K.R., Ullsperger, M., Crone, E.A. & Nieuwenhuis, S. The role of the medial frontal cortex in cognitive control. Science 306, 443–447 (2004).
Greene, J.D., Nystrom, L.E., Engell, A.D., Darley, J.M. & Cohen, J.D. The neural bases of cognitive conflict and control in moral judgment. Neuron 44, 389–400 (2004).
Zink, C.F., Pagnoni, G., Martin-Skurski, M.E., Chappelow, J.C. & Berns, G.S. Human striatal responses to monetary reward depend on saliency. Neuron 42, 509–517 (2004).
Elliott, R., Newman, J.L., Longe, O.A. & William Deakin, J.F. Instrumental responding for rewards is associated with enhanced neuronal response in subcortical reward systems. Neuroimage 21, 984–990 (2004).
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).
Schultz, W., Dayan, P. & Montague, P.R. A neural substrate of prediction and reward. Science 275, 1593–1599 (1997).
McClure, S.M., Berns, G.S. & Montague, P.R. Temporal prediction errors in a passive learning task activate human striatum. Neuron 38, 339–346 (2003).
O'Doherty, J.P., Dayan, P., Friston, K., Critchley, H. & Dolan, R.J. Temporal difference models and reward-related learning in the human brain. Neuron 38, 329–337 (2003).
Davidson, M.C. et al. Differential cingulate and caudate activation following unexpected nonrewarding stimuli. Neuroimage 23, 1039–1045 (2004).
Singer, T., Kiebel, S.J., Winston, J.S., Dolan, R.J. & Frith, C.D. Brain responses to the acquired moral status of faces. Neuron 41, 653–662 (2004).
de Quervain, D.J. et al. The neural basis of altruistic punishment. Science 305, 1254–1258 (2004).
Critchley, H.D., Mathias, C.J. & Dolan, R.J. Neural activity in the human brain relating to uncertainty and arousal during anticipation. Neuron 29, 537–545 (2001).
Gabrieli, J.D. Cognitive neuroscience of human memory. Annu. Rev. Psychol. 49, 87–115 (1998).
Squire, L.R., Knowlton, B. & Musen, G. The structure and organization of memory. Annu. Rev. Psychol. 44, 453–495 (1993).
Poldrack, R.A. & Packard, M.G. Competition among multiple memory systems: converging evidence from animal and human brain studies. Neuropsychologia 41, 245–251 (2003).
Zola-Morgan, S. & Squire, L.R. Neuroanatomy of memory. Annu. Rev. Neurosci. 16, 547–563 (1993).
Macwhinney, B., Cohen, J. & Provost, J. The PsyScope experiment-building system. Spat. Vis. 11, 99–101 (1997).
Talairach, J. & Tournoux, P. Co-planar Stereotaxic Atlas of the Human Brain: An Approach to Medical Cerebral Imaging (Thieme Medical Publishers, New York, 1988).
Forman, S.D. et al. Improved assessment of significant activation in functional magnetic resonance imaging (fMRI): use of a cluster-size threshold. Magn. Reson. Med. 33, 636–647 (1995).
The authors wish to acknowledge K. Nearing for assistance and useful discussion, J. Pearson and E. Neaville for technical assistance and S. Ravizza for informative discussion and constructive criticism. This work was supported by the US National Institute of Mental Health, the James S. McDonnell Foundation, the Beatrice and Samuel A. Seaver Foundation and Cornell's S.C. Johnson School of Management.
The authors declare no competing financial interests.
About this article
Cite this article
Delgado, M., Frank, R. & Phelps, E. Perceptions of moral character modulate the neural systems of reward during the trust game. Nat Neurosci 8, 1611–1618 (2005). https://doi.org/10.1038/nn1575
This article is cited by
Nature Communications (2022)
Current Psychology (2022)
Political Behavior (2022)
Current Psychology (2022)
Communications Biology (2021)