The social brain and reward: Social information processing in the human striatum

Wiley Interdisciplinary Reviews: Cognitive Science

Volumn 5, Issue 1, 2014, Pages 61-73

  Bhanji, Jamil P ^a   Delgado, Mauricio R ^a  

^a RUTGERS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84890366972     PISSN: 19395078     EISSN: 19395086     Source Type: Journal    
DOI: 10.1002/wcs.1266     Document Type: Review

References (108)

1. Delgado MR. Reward-related responses in the human striatum. Ann N Y Acad Sci 2007, 1104:70-88.
2. Izuma K, Saito DN, Sadato N. Processing of social and monetary rewards in the human striatum. Neuron 2008, 58:284-294.
3. Behrens TEJ, Hunt LT, Woolrich MW, Rushworth MFS. Associative learning of social value. Nature 2008, 456:245-249.
4. Haber SN, Knutson B. The reward circuit: linking primate anatomy and human imaging. Neuropsychopharmacology 2010, 35:4-26.
5. Alexander GE, DeLong MR, Strick PL. Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Annu Rev Neurosci 1986, 9:357-381.
6. Cardinal RN, Parkinson JA, Hall J, Everitt BJ. Emotion and motivation: the role of the amygdala, ventral striatum, and prefrontal cortex. Neurosci Biobehav Rev 2002, 26:321-352.
7. Alexander GE, Crutcher MD, DeLong MR. Basal ganglia-thalamocortical circuits: parallel substrates for motor, oculomotor, "prefrontal" and "limbic" functions. Prog Brain Res 1990, 85:119-146.
8. Haber SN, Fudge JL, McFarland NR. Striatonigrostriatal pathways in primates form an ascending spiral from the shell to the dorsolateral striatum. J Neurosci 2000, 20:2369-2382.
9. Lehéricy S, Ducros M, Van de Moortele P-F, Francois C, Thivard L, Poupon C, Swindale N, Ugurbil K, Kim D-S. Diffusion tensor fiber tracking shows distinct corticostriatal circuits in humans. Ann Neurol 2004, 55:522-529.
10. Knutson B, Cooper JC. Functional magnetic resonance imaging of reward prediction. Curr Opin Neurobiol 2005, 18:411-417.
11. Liljeholm M, O'Doherty JP. Contributions of the striatum to learning, motivation, and performance: an associative account. Trends Cogn Sci 2012, 16:467-475.
12. Knutson B, Adams CM, Fong GW, Hommer D. Anticipation of increasing monetary reward selectively recruits nucleus accumbens. J Neurosci 2001, 21:RC159.
13. O'Doherty JP, Deichmann R, Critchley HD, Dolan RJ. Neural responses during anticipation of a primary taste reward. Neuron 2002, 33:815-826.
14. Delgado MR, Nystrom LE, Fissell C, Noll DC, Fiez JA. Tracking the hemodynamic responses to reward and punishment in the striatum. J Neurophysiol 2000, 84:3072-3077.
15. O'Doherty J, Dayan P, Friston K, Critchley H, Dolan RJ. Temporal difference models and reward-related learning in the human brain. Neuron 2003, 38:329-337.
16. McClure SM, Berns GS, Montague PR. Temporal prediction errors in a passive learning task activate human striatum. Neuron 2003, 38:339-346.
17. Schultz W, Dayan P, Montague PR. A neural substrate of prediction and reward. Science 1997, 275:1593-1599.
18. Rescorla RA, Wagner AR. A theory of Pavolovian conditioning: variations in the effectiveness of reinforcement and nonreinforcement. In: Black AH, Prokasy WF, eds. Classical Conditioning II. New York:Appleton-Century-Crofts; 1972, 64-99.
19. Sutton RS, Barto AG. Reinforcement Learning. Cambridge, MA: MIT Press, New York; 1998.
20. Berridge KC, Robinson TE. What is the role of dopamine in reward: hedonic impact, reward learning, or incentive salience? Brain Res Brain Res Rev 1998, 28:309-369.
21. Robinson TE, Flagel SB. Dissociating the predictive and incentive motivational properties of reward-related cues through the study of individual differences. Biol Psychiatry 2009, 65:869-873.
22. D'Ardenne K, McClure SM, Nystrom LE, Cohen JD. BOLD responses reflecting dopaminergic signals in the human ventral tegmental area. Science 2008, 319:1264-1267.
23. O'Doherty J, Dayan P, Schultz J, Deichmann R, Friston K, Dolan RJ. Dissociable roles of ventral and dorsal striatum in instrumental conditioning. Science 2004, 304:452-454.
24. Tricomi EM, Delgado MR, Fiez JA. Modulation of caudate activity by action contingency. Neuron 2004, 41:281-292.
25. Schonberg T, Daw ND, Joel D, O'Doherty JP. Reinforcement learning signals in the human striatum distinguish learners from nonlearners during reward-based decision making. J Neurosci 2007, 27:12860-12867.
26. Tricomi E, Fiez JA. Information content and reward processing in the human striatum during performance of a declarative memory task. Cogn Affect Behav Neurosci 2012, 12:361-372.
27. Rodriguez PF, Aron AR, Poldrack RA. Ventral-striatal/nucleus-accumbens sensitivity to prediction errors during classification learning. Hum Brain Mapp 2006, 27:306-313.
28. Shohamy D, Myers CE, Onlaor S, Gluck MA. Role of the basal ganglia in category learning: how do patients with Parkinson's disease learn? Behav Neurosci 2004, 118:676-686.
29. Kable JW, Glimcher PW. The neural correlates of subjective value during intertemporal choice. Nat Neurosci 2007, 10:1625-1633.
30. Chib VS, Rangel A, Shimojo S, O'Doherty JP. Evidence for a common representation of decision values for dissimilar goods in human ventromedial prefrontal cortex. J Neurosci 2009, 29:12315-12320.
31. Rangel A, Hare T. Neural computations associated with goal-directed choice. Curr Opin Neurobiol 2010, 20:262-270.
32. Peters J, Büchel C. Neural representations of subjective reward value. Behav Brain Res 2010, 213:135-141.
33. O'Doherty J, Winston J, Critchley H, Perrett D, Burt DM, Dolan RJ. Beauty in a smile: the role of medial orbitofrontal cortex in facial attractiveness. Neuropsychologia 2003, 41:147-155.
34. Cunningham WA, Johnson MK, Gatenby JC, Gore JC, Banaji MR. Neural components of social evaluation. J Pers Soc Psychol 2003, 85:639-649.
35. Aharon I, Etcoff N, Ariely D, Chabris CF, O'Connor E, Breiter HC. Beautiful faces have variable reward value: fMRI and behavioral evidence. Neuron 2001, 32:537-551.
36. Smith DV, Hayden BY, Truong T-K, Song AW, Platt ML, Huettel SA. Distinct value signals in anterior and posterior ventromedial prefrontal cortex. J Neurosci 2010, 30:2490-2495.
37. Spreckelmeyer KN, Krach S, Kohls G, Rademacher L, Irmak A, Konrad K, Kircher T, Gründer G. Anticipation of monetary and social reward differently activates mesolimbic brain structures in men and women. Soc Cogn Affect Neurosci 2009, 4:158-165.
38. Lin A, Adolphs R, Rangel A. Social and monetary reward learning engage overlapping neural substrates. Soc Cogn Affect Neurosci 2012, 7:274-281.
39. Fisher HE, Aron A, Brown LL. Romantic love: a mammalian brain system for mate choice. Philos Trans R Soc Lond B Biol Sci 2006, 361:2173-2186.
40. Hughes BL, Beer JS. Orbitofrontal cortex and anterior cingulate cortex are modulated by motivated social cognition. Cereb Cortex 2012, 22:1372-1381.
41. Zink CF, Tong Y, Chen Q, Bassett DS, Stein JL, Meyer-Lindenberg A. Know your place: neural processing of social hierarchy in humans. Neuron 2008, 58:273-283.
42. Gunther Moor B, van Leijenhorst L, Rombouts SARB, Crone EA, Van der Molen MW. Do you like me? Neural correlates of social evaluation and developmental trajectories. Soc Neurosci 2010, 5:461-482.
43. Davey CG, Allen NB, Harrison BJ, Dwyer DB, Yücel M. Being liked activates primary reward and midline self-related brain regions. Hum Brain Mapp 2010, 31:660-668.
44. Klucharev V, Hytönen K, Rijpkema M, Smidts A, Fernández G. Reinforcement learning signal predicts social conformity. Neuron 2009, 61:140-151.
45. Izuma K, Adolphs R. Social manipulation of preference in the human brain. Neuron 2013, 78:563-573.
46. Mason MF, Dyer R, Norton MI. Neural mechanisms of social influence. Organ Behav Hum Decis Process 2009, 110:152-159.
47. Zaki J, Schirmer J, Mitchell JP. Social influence modulates the neural computation of value. Psychol Sci 2011, 22:894-900.
48. Burke CJ, Tobler PN, Schultz W, Baddeley M. Striatal BOLD response reflects the impact of herd information on financial decisions. Front Hum Neurosci 2010, 4(June):48.
49. Berns GS, Chappelow J, Zink CF, Pagnoni G, Martin-Skurski ME, Richards J. Neurobiological correlates of social conformity and independence during mental rotation. Biol Psychiatry 2005, 58:245-253.
50. Campbell-Meiklejohn DK, Bach DR, Roepstorff A, Dolan RJ, Frith CD. How the opinion of others affects our valuation of objects. Curr Biol 2010, 20:1165-1170.
51. Klucharev V, Smidts A, Fernández G. Brain mechanisms of persuasion: how "expert power" modulates memory and attitudes. Soc Cogn Affect Neurosci 2008, 3:353-366.
52. Meshi D, Biele G, Korn CW, Heekeren HR. How expert advice influences decision making. PLoS One 2012, 7:1-12.
53. Biele G, Rieskamp J, Krugel LK, Heekeren HR. The neural basis of following advice. PLoS Biol 2011, 9:1-11.
54. Fareri DS, Niznikiewicz MA, Lee VK, Delgado MR. Social network modulation of reward-related signals. J Neurosci 2012, 32:9045-9052.
55. 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 2011, 14:F1-F10.
56. Knutson B, Taylor J, Kaufman M, Peterson R, Glover G. Distributed neural representation of expected value. J Neurosci 2005, 25:4806-4812.
57. Preuschoff K, Bossaerts P, Quartz SR. Neural differentiation of expected reward and risk in human subcortical structures. Neuron 2006, 51:381-390.
58. Onoda K, Okamoto Y, Nakashima K, Nittono H, Ura M, Yamawaki S. Decreased ventral anterior cingulate cortex activity is associated with reduced social pain during emotional support. Soc Neurosci 2009, 4:443-454.
59. Izuma K, Saito DN, Sadato N. Processing of the incentive for social approval in the ventral striatum during charitable donation. J Cogn Neurosci 2010, 22:621-631.
60. Moll J, Krueger F, Zahn R, Pardini M, de Oliveira-Souza R, Grafman J. Human fronto-mesolimbic networks guide decisions about charitable donation. Proc Natl Acad Sci USA 2006, 103:15623-15628.
61. Harbaugh WT, Mayr U, Burghart DR. Neural responses to taxation and voluntary giving reveal motives for charitable donations. Science 2007, 316:1622-1625.
62. Mobbs D, Yu R, Meyer M, Passamonti L, Seymour B, Calder AJ, Schweizer S, Frith CD, Dalgleish T. A key role for similarity in vicarious reward. Science 2009, 324:900.
63. Kuss K, Falk A, Trautner P, Elger CE, Weber B, Fliessbach K. A reward prediction error for charitable donations reveals outcome orientation of donators. Soc Cogn Affect Neurosci 2013, 8:216-223.
64. Hare TA, Camerer CF, Knoepfle DT, Rangel A. Value computations in ventral medial prefrontal cortex during charitable decision making incorporate input from regions involved in social cognition. J Neurosci 2010, 30:583-590.
65. Hsu M, Anen C, Quartz SR. The right and the good: distributive justice and neural encoding of equity and efficiency. Science 2008, 320:1092-1095.
66. Jones RM, Somerville LH, Li J, Ruberry EJ, Libby V, Glover G, Voss HU, Ballon DJ, Casey BJ. Behavioral and neural properties of social reinforcement learning. J Neurosci 2011, 31:13039-13045.
67. King-Casas B, Tomlin D, Anen C, Camerer CF, Quartz SR, Montague PR. Getting to know you: reputation and trust in a two-person economic exchange. Science 2005, 308:78-83.
68. Bhanji JP, Beer JS. Dissociable neural modulation underlying lasting first impressions, changing your mind for the better, and changing it for the worse. J Neurosci 2013, 33:9337-9344.
69. Harris LT, Fiske ST. Neural regions that underlie reinforcement learning are also active for social expectancy violations. Soc Neurosci 2010, 5:76-91.
70. Korn CW, Prehn K, Park SQ, Walter H, Heekeren HR. Positively biased processing of self-relevant social feedback. J Neurosci 2012, 32:16832-16844.
71. Rilling J, Gutman D, Zeh T, Pagnoni G, Berns G, Kilts C. A neural basis for social cooperation. Neuron 2002, 35:395-405.
72. Yoshida W, Seymour B, Friston KJ, Dolan RJ. Neural mechanisms of belief inference during cooperative games. J Neurosci 2010, 30:10744-10751.
73. Tabibnia G, Lieberman MD. Fairness and cooperation are rewarding evidence from social cognitive neuroscience. Ann N Y Acad Sci 2007, 9747:90-101.
74. Decety J, Jackson PL, Sommerville JA, Chaminade T, Meltzoff AN. The neural bases of cooperation and competition: an fMRI investigation. Neuroimage 2004, 23:744-751.
75. Phan KL, Sripada CS, Angstadt M, McCabe K. Reputation for reciprocity engages the brain reward center. Proc Natl Acad Sci USA 2010, 107:13099-13104.
76. Fareri DS, Chang LJ, Delgado MR. Effects of direct social experience on trust decisions and neural reward circuitry. Front Neurosci 2012, 6:148.
77. Fouragnan E, Chierchia G, Greiner S, Neveu R, Avesani P, Coricelli G. Reputational priors magnify striatal responses to violations of trust. J Neurosci 2013, 33:3602-3611.
78. Delgado MR, Frank RH, Phelps EA. Perceptions of moral character modulate the neural systems of reward during the trust game. Nat Neurosci 2005, 8:1611-1618.
79. Baumgartner T, Heinrichs M, Vonlanthen A, Fischbacher U, Fehr E. Oxytocin shapes the neural circuitry of trust and trust adaptation in humans. Neuron 2008, 58:639-650.
80. Reeder GD, Brewer MB. A schematic model of dispositional attribution in interpersonal perception. Psychol Rev 1979, 86:61-79.
81. Li J, Delgado MR, Phelps EA. How instructed knowledge modulates the neural systems of reward learning. Proc Natl Acad Sci USA 2011, 108:55-60.
82. Dvash J, Gilam G, Ben-Ze'ev A, Hendler T, Shamay-Tsoory SG. The envious brain: the neural basis of social comparison. Hum Brain Mapp 2010, 31:1741-1750.
83. 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 2011, 108:16044-16049.
84. Fliessbach K, Weber B, Trautner P, Dohmen T, Sunde U, Elger CE, Falk A. Social comparison affects reward-related brain activity in the human ventral striatum. Science 2007, 318:1305-1308.
85. Fareri DS, Delgado MR. Differential reward responses during competition against in- and out-of-network others. Soc Cogn Affect Neurosci 2013. doi: 10.1093/scan/nst006.
86. Ly M, Haynes MR, Barter JW, Weinberger DR, Zink CF. Subjective socioeconomic status predicts human ventral striatal responses to social status information. Curr Biol 2011, 21:794-797.
87. Cikara M, Botvinick MM, Fiske ST. Us versus them: social identity shapes neural responses to intergroup competition and harm. Psychol Sci 2011, 22:306-313.
88. Van den Bos W, Talwar A, McClure SM. Neural correlates of reinforcement learning and social preferences in competitive bidding. J Neurosci 2013, 33:2137-2146.
89. Delgado MR, Schotter A, Ozbay EY, Phelps EA. Understanding overbidding: using the neural circuitry of reward to design economic auctions. Science 2008, 321:1849-1852.
90. Zhu L, Mathewson KE, Hsu M. Dissociable neural representations of reinforcement and belief prediction errors underlie strategic learning. Proc Natl Acad Sci USA 2012, 109:1419-1424.
91. Sanfey AG, Rilling JK, Aronson JA, Nystrom LE, Cohen JD. The neural basis of economic decision-making in the ultimatum game. Science 2003, 300:1755-1758.
92. Tricomi E, Rangel A, Camerer CF, O'Doherty JP. Neural evidence for inequality-averse social preferences. Nature 2010, 463:1089-1091.
93. Tabibnia G, Satpute AB, Lieberman MD. The sunny side of fairness: preference for fairness activates reward circuitry (and disregarding unfairness activates self-control circuitry). Psychol Sci 2008, 19:339-347.
94. Xiang T, Lohrenz T, Montague PR. Computational substrates of norms and their violations during social exchange. J Neurosci 2013, 33:1099-1108.
95. Chang LJ, Smith A, Dufwenberg M, Sanfey AG. Triangulating the neural, psychological, and economic bases of guilt aversion. Neuron 2011, 70:560-572.
96. De Quervain DJ-F, Fischbacher U, Treyer V, Schellhammer M, Schnyder U, Buck A, Fehr E. The neural basis of altruistic punishment. Science 2004, 305:1254-1258.
97. Crockett MJ, Apergis-Schoute A, Herrmann B, Lieberman M, Müller U, Robbins TW, Clark L. Serotonin modulates striatal responses to fairness and retaliation in humans. J Neurosci 2013, 33:3505-3513.
98. Singer T, Seymour B, O'Doherty JP, Stephan KE, Dolan RJ, Frith CD. Empathic neural responses are modulated by the perceived fairness of others. Nature 2006, 439:466-469.
99. Crockett MJ, Clark L, Lieberman MD, Tabibnia G, Robbins TW. Impulsive choice and altruistic punishment are correlated and increase in tandem with serotonin depletion. Emotion 2010, 10:855-862.
100. Vostroknutov A, Tobler PN, Rustichini A. Causes of social reward differences encoded in human brain. J Neurophysiol 2012, 107:1403-1412.
101. Van den Bos W, van Dijk E, Westenberg M, Rombouts SA, Crone EA. What motivates repayment? Neural correlates of reciprocity in the Trust Game. Soc Cogn Affect Neurosci 2009, 4:294-304.
102. Bandura A. Social cognitive theory of self-regulation. Organ Behav Hum Decis Process 1991, 50:248-287.
103. Bhanji JP, Beer JS. Taking a different perspective: mindset influences neural regions that represent value and choice. Soc Cogn Affect Neurosci 2012, 7:782-793.
104. Hare TA, Malmaud J, Rangel A. Focusing attention on the health aspects of foods changes value signals in vmPFC and improves dietary choice. J Neurosci 2011, 31:11077-11087.
105. Hutcherson CA, Plassmann H, Gross JJ, Rangel A. Cognitive regulation during decision making shifts behavioral control between ventromedial and dorsolateral prefrontal value systems. J Neurosci 2012, 32:13543-13554.
106. Kober H, Mende-Siedlecki P, Kross EF, Weber J, Mischel W, Hart CL, Ochsner KN. Prefrontal-striatal pathway underlies cognitive regulation of craving. Proc Natl Acad Sci USA 2010, 107:14811-14816.
107. Martin L, Delgado M. The influence of emotion regulation on decision-making under risk. J Cogn Neurosci 2011, 23:2569-2581.
108. Delgado MR, Gillis MM, Phelps EA. Regulating the expectation of reward via cognitive strategies. Nat Neurosci 2008, 11:880-881.