Effects of direct social experience on trust decisions and neural reward circuitry

Frontiers in Neuroscience

Volumn , Issue OCT, 2012, Pages

  Fareri, Dominic S ^a   Chang, Luke J ^b,c   Delgado, Mauricio R ^a  

^a RUTGERS UNIVERSITY   (United States)

^b UNIVERSITY OF COLORADO   (United States)

^c University of Arizona   (United States)

Author keywords

Learning; Prediction error; Reward; Social experience; Striatum; Trust

Indexed keywords

ADULT; ANTERIOR CINGULATE; ARTICLE; BEHAVIOR; BOLD SIGNAL; CONTROLLED STUDY; CORPUS STRIATUM; DECISION MAKING; EXPERIENCE; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; FUNCTIONAL NEUROIMAGING; HUMAN; MALE; PERSONALITY; PREDICTION; REINFORCEMENT; REWARD; SOCIAL BELIEF; TRUST;

EID: 84870954060     PISSN: 16624548     EISSN: 1662453X     Source Type: Journal    
DOI: 10.3389/fnins.2012.00148     Document Type: Article

References (90)

1. Adolphs, R., Tranel, D., and Damasio, A. R. (1998). The human amygdala in social judgment. Nature 393, 470-474.
2. Akaike, H. (1974). A new look at the statistical model identification. IEEE Trans. Automat. Contr. 19, 716-723.
3. Amodio, D. M., and Frith, C. D. (2006). Meeting of minds: the medial frontal cortex and social cognition. Nat. Rev. Neurosci. 7, 268-277.
4. Baumgartner,T.,Heinrichs,M.,Vonlan-then,A., Fischbacher, U., and Fehr, E. (2008). Oxytocin shapes the neural circuitry of trust and trust adapta-tioninhumans.Neuron 58,639-650.
5. Behrens, T. E., Hunt, L. T., Woolrich, M. W., and Rushworth, M. F. (2008). Associative learning of social value. Nature 456, 245-249.
6. Behrens,T. E.,Woolrich,M.W.,Walton, M. E., and Rushworth, M. F. (2007). Learning the value of information in an uncertain world. Nat. Neurosci. 10, 1214-1221.
7. Belova, M. A., Paton, J. J., and Salz-man, C. D. (2008). Moment-to-moment tracking of state value in the amygdala. J. Neurosci. 28, 10023-10030.
8. Berg, J., Dickhaut, J., and McCabe, K. (1995). Trust, reciprocity, and social history. Games Econ. Behav. 10, 122-142.
9. Bush, G., Luu, P., and Posner, M. I. (2000). Cognitive and emotional influences in anterior cingulate cortex. Trends Cogn. Sci. (Regul. Ed.) 4, 215-222.
10. Chang, L. J., Doll, B. B., van 't Wout, M., Frank, M. J., and Sanfey, A. G. (2010). Seeing is believing: trustworthiness as a dynamic belief. Cogn. Psychol. 61, 87-105.
11. Chang, L. J., and Sanfey, A. G. (2009). Unforgettable ultimatums? Expectation violations promote enhanced social memory following economic bargaining. Front. Behav. Neurosci. 3:36. doi:10.3389/neuro.08.036.2009
12. Chang, L. J., and Sanfey, A. G. (2011). Great expectations: neural computations underlying the use of social norms in decision-making. Soc. Cogn. Affect. Neurosci. PMID: 22198968. [Epub ahead of print].
13. Chang,L. J., Smith, A.,Dufwenberg,M., and Sanfey, A. G. (2011). Triangulating the neural, psychological, and economic bases of guilt aversion. Neuron 70, 560-572.
14. Chang, L. J., Yarkoni, T., Khaw, M. W., and Sanfey, A. G. (2012). Decoding the role of the insula in human cognition: functional parcellation and large-scale reverse inference. Cereb. Cortex. PMID: 22437053. [Epub ahead of print].
15. Daw, N. D., Gershman, S. J., Seymour, B., Dayan, P., and Dolan, R. J. (2011). Model-based influences on humans' choices and stri-atal prediction errors. Neuron 69, 1204-1215.
16. Delgado,M.R.,Frank,R.H.,and Phelps, E. A. (2005a). Perceptions of moral character modulate the neural systems of reward during the trust game. Nat. Neurosci. 8, 1611-1618.
17. Delgado, M. R., Miller, M. M., Inati, S., and Phelps, E. A. (2005b). An fMRI study of reward-related probability learning. Neuroimage 24, 862-873.
18. Delgado, M. R., Li, J., Schiller, D., and Phelps, E. A. (2008). The role of the striatum in aversive learning and aversive prediction errors. Phi-los. Trans. R. Soc. Lond. B Biol. Sci. 363, 3787-3800.
19. Delgado, M. R., Locke, H. M., Stenger, V. A., and Fiez, J. A. (2003). Dorsal striatum responses to reward and punishment: effects of valence and magnitude manipulations. Cogn. Affect. Behav. Neurosci. 3, 27-38.
20. Delgado, M. R., Nystrom, L. E., Fis-sell, C., Noll, D. C., and Fiez, J. A. (2000). Tracking the hemodynamic responsestorewardand punishment in the striatum. J. Neurophysiol. 84, 3072-3077.
21. Delgado, M. R., Stenger, V. A., and Fiez, J. A. (2004). Motivation-dependent responses in the human caudate nucleus. Cereb. Cortex 14, 1022-1030.
22. Doll, B. B., Hutchison, K. E., and Frank, M. J. (2011). Dopaminergic genes predict individual differences in susceptibility to confirmation bias. J. Neurosci. 31, 6188-6198.
23. Doll, B. B., Jacobs, W. J., Sanfey, A. G., and Frank, M. J. (2009). Instructional control of reinforcement learning: a behavioral and neurocomputational investigation. Brain Res. 1299, 74-94.
24. Eisenberger, N. I., Lieberman, M. D., and Williams, K. D. (2003). Does rejection hurt? An FMRI study of social exclusion. Science 302, 290-292.
25. Elliott, R., Newman, J. L., Longe, O. A., and William Deakin, J. F. (2004). Instrumental responding for rewards is associated with enhanced neuronal response in subcortical reward systems. Neuroimage 21, 984-990.
26. Engell, A. D., Haxby, J. V., and Todorov, A. (2007). Implicit trustworthiness decisions: automatic coding of face properties in the human amygdala. J. Cogn. Neurosci. 19, 1508-1519.
27. Everitt, B. J., Morris, K. A., O'Brien, A., and Robbins, T. W. (1991). The basolateral amygdala-ventral striatal system and conditioned place preference: further evidence of limbic-striatal interactions underlying reward-related processes. Neuro-science 42, 1-18.
28. Everitt, B. J., Parkinson, J. A., Olmstead, M. C., Arroyo, M., Robledo, P., and Robbins, T. W. (1999). Associative processes in addiction and reward. The role of amygdala-ventral striatal subsystems. Ann. N. Y. Acad. Sci. 877, 412-438.
29. Fareri, D. S., Niznikiewicz, M. A., Lee, V. K., and Delgado, M. R. (2012). Social network modulation of reward-related signals.J. Neurosci. 32, 9045-9052.
30. Fehr, E., and Camerer, C. F. (2007). Social neuroeconomics: the neural circuitry of social preferences.Trends Cogn. Sci. (Regul. Ed.) 11, 419-427.
31. Ferguson, J. N., Aldag, J. M., Insel, T. R., and Young, L. J. (2001). Oxytocin in the medial amygdala is essential for social recognition in the mouse. J. Neurosci. 21, 8278-8285.
32. Forman, S. D., Cohen, J. D., Fitzgerald, M., Eddy, W. F., Mintun, M. A., and Noll, D. C. (1995). Improved assessment of significant activation in functional magnetic resonance imaging (fMRI): use of a cluster-sizethreshold.Magn.Reson.Med.33, 636-647.
33. Frank, M. J., Moustafa, A. A., Haughey, H. M., Curran, T., and Hutchison, K. E. (2007). Genetic triple dissociation reveals multiple roles for dopamine in reinforcement learning. Proc. Natl. Acad. Sci. U.S.A. 104, 16311-16316.
34. Galvan, A., Hare, T. A., Davidson, M., Spicer, J., Glover, G., and Casey, B. J. (2005). The role of ventral fron-tostriatal circuitry in reward-based learning in humans. J. Neurosci. 25, 8650-8656.
35. Goebel, R., Esposito, F., and Formisano, E. (2006). Analysis of functional image analysis contest (FIAC) data with brainvoyager QX: from single-subject to cortically aligned group general linear model analysis and self-organizing group independent component analysis. Hum. Brain Mapp. 27, 392-401.
36. Gottfried, J. A., O'Doherty, J., and Dolan,R.J.(2003). Encoding predictive reward value in human amygdala and orbitofrontal cortex. Science 301, 1104-1107.
37. Haber, S. N., and Knutson, B. (2010). The reward circuit: linking primate anatomy and human imaging. Neu-ropsychopharmacology 35, 4-26.
38. Hampton, A., and O'Doherty, J. (2007). Decoding the neural substrates of reward-related decision making with functional MRI. Proc. Natl. Acad. Sci. U.S.A. 104, 1377-1382.
39. Hampton, A. N., Bossaerts, P., and O'Doherty, J. P. (2008). Neural correlates of mentalizing-related computations during strategic interactions in humans. Proc. Natl. Acad. Sci. U.S.A. 105, 6741-6746.
40. Hollerman,J. R., and Schultz,W. (1998). Dopamine neurons report an error in the temporal prediction of reward during learning. Nat. Neurosci. 1, 304-309.
41. Holm, S. (1979). A simple sequentially rejective multiple test procedure. Scand. J. Stat. 6, 65-70.
42. Insel, T. R. (2010). The challenge of translation in social neuroscience: a review of oxytocin, vasopressin, and affiliative behavior. Neuron 65, 768-779.
43. Izuma, K., Saito, D. N., and Sadato, N. (2010). Processing of the incentive for social approval in the ventral striatum during charitable donation. J. Cogn. Neurosci. 22, 621-631.
44. Jones, R. M., Somerville, L. H., Li, J., Ruberry, E. J., Libby, V., Glover, G., et al. (2011). Behavioral and neural properties of social reinforcement learning. J. Neurosci. 31, 13039-13045.
45. King-Casas, B., Tomlin, D., Anen, C., Camerer, C. F., Quartz, S. R., and Montague, P. R. (2005). Getting to know you: reputation and trust in a two-person economic exchange. Science 308, 78-83.
46. Kishida, K. T., and Montague, P. R. (2012). Imaging modelsof valuation during social interaction in humans. Biol. Psychiatry 72, 93-100.
47. Knutson, B., Adams, C. M., Fong,G. W., and Hommer, D. (2001). Anticipation of increasing monetary reward selectively recruits nucleus accum-bens. J. Neurosci. 21, RC159.
48. Knutson, B., Fong, G. W., Bennett, S. M., Adams, C. M., and Hom-mer, D. (2003). A region of mesial prefrontal cortex tracks monetarily rewarding outcomes: characterization with rapid event-related fMRI. Neuroimage 18, 263-272.
49. Krueger, F., McCabe, K., Moll, J., Kriegeskorte, N.,Zahn, R., Strenziok, M., et al. (2007). Neural correlates of trust. Proc. Natl. Acad. Sci. U.S.A. 104, 20084-20089.
50. Krugel, L. K., Biele, G., Mohr, P. N., Li, S. C., and Heekeren, H. R. (2009). Genetic variation in dopaminer-gic neuromodulation influences the ability to rapidly and flexibly adapt decisions. Proc. Natl. Acad. Sci. U.S.A. 106, 17951-17956.
51. Leotti, L. A., and Delgado, M. R. (2011). "Processing social and non-social rewards in the human brain," in The Oxford Handbook of Social Neu-roscience, eds J. Decety and J. T. Cacioppo (New York: Oxford University Press), 178-194.
52. Li, J., Delgado, M. R., and Phelps, E. A. (2011a). How instructed knowledge modulates the neural systems of reward learning. Proc. Natl. Acad. Sci. U.S.A. 108, 55-60.
53. Li, J., Schiller, D., Schoenbaum, G., Phelps, E. A., and Daw, N. D. (2011b). Differential roles of human striatum and amygdala in associative learning. Nat. Neurosci. 14, 1250-1252.
54. Lin, A., Adolphs, R., and Rangel, A. (2012). Social and monetary reward learning engage overlapping neural substrates. Soc. Cogn. Affect. Neu-rosci. 7, 274-281.
55. Maaswinkel,H.,Baars,A.M.,Gispen,W. H., and Spruijt, B. M. (1996). Roles of the basolateral amygdala and hippocampus in social recognition in rats. Physiol. Behav. 60, 55-63.
56. Markram, K., Rinaldi, T., La Mendola, D., Sandi, C., and Markram, H. (2008). Abnormal fear conditioning and amygdala processing in an animal model of autism. Neuropsy-chopharmacology 33, 901-912.
57. Menon, V., and Uddin, L. Q. (2010). Saliency, switching, attention and control: a network model of insula function. Brain Struct. Funct. 214, 655-667.
58. Miller,E. K., and Cohen,J. D. (2001). An integrative theory of prefrontal cortex function.Annu. Rev. Neurosci.24, 167-202.
59. Mobbs, D., Yu, R., Meyer, M., Passa-monti, L., Seymour, B., Calder, A. J., et al. (2009). A key role for similarity in vicarious reward. Science 324, 900.
60. Niv, Y., and Schoenbaum, G. (2008). Dialogues on prediction errors. Trends Cogn. Sci. (Regul. Ed.) 12, 265-272.
61. O'Doherty, J., Dayan, P., Schultz, J., Deichmann, R., Friston, K., and Dolan, R. J. (2004). Dissociable roles of ventral and dorsal striatum in instrumental conditioning. Science 304, 452-454.
62. O'Doherty, J. P., Dayan, P., Friston, K., Critchley, H., and Dolan, R. J. (2003). Temporal difference models and reward-related learning in the human brain. Neuron 38, 329-337.
63. O'Doherty, J. P., Deichmann, R., Critch-ley, H. D., and Dolan, R. J. (2002). Neural responses during anticipation of a primary taste reward. Neuron 33, 815-826.
64. O'Doherty, J. P., Hampton, A., and Kim, H. (2007). Model-based fMRI and its application to reward learning and decision making. Ann. N. Y. Acad. Sci. 1104, 35-53.
65. Oosterhof, N. N., and Todorov, A. (2008). The functional basis of face evaluation. Proc. Natl. Acad. Sci. U.S.A. 105, 11087-11092.
66. Paton, J. J., Belova, M. A., Morrison, S. E., and Salzman, C. D. (2006). Theprimateamygdala represents the positive and negative value of visual stimuli during learning. Nature 439, 865-870.
67. Pessiglione, M., Seymour, B., Flandin, G., Dolan, R. J., and Frith, C. D. (2006). Dopamine-dependent prediction errors underpin reward-seeking behaviour in humans. Nature 442, 1042-1045.
68. Phan, K. L., Sripada, C. S., Angstadt, M., and McCabe, K. (2010). Reputation for reciprocity engages the brain reward center. Proc. Natl. Acad. Sci. U.S.A. 107, 13099-13104.
69. Prelec, D., and Lowenstein, L. (1991). Decision making over time and under uncertainty: a common approach. Manage. Sci. 37, 770-786.
70. Rescorla, R. A., and Wagner, A. R. (1972)."Atheory of Pavolovian conditioning: variations in the effectiveness of reinforcement and non-reinforcement," in Classical Conditioning II, eds A. H. Black and W. F. Prokasy (New York: Appleton-Century-Crofts), 64-99.
71. Rice, W. R. (1989). Analyzing tables of statistical tests. Evolution 6, 223-225.
72. Rilling, J. K., and Sanfey, A. G. (2011). The neuroscience of social decision-making. Annu. Rev. Psychol. 62, 23-48.
73. Robbins, T. W., and Everitt, B. J. (1996). Neurobehavioural mechanisms of reward and motivation. Curr. Opin. Neurobiol. 6, 228-236.
74. Rolls, E. T. (2000). The orbitofrontal cortex and reward. Cereb. Cortex 10, 284-294.
75. Saxe, R. (2006). Uniquely human social cognition. Curr. Opin. Neurobiol. 16, 235-239.
76. Schonberg, T., Daw, N. D., Joel, D., and O'Doherty, J. P. (2007). Reinforcement learning signals in the human striatum distinguish learners from nonlearners during reward-based decision making. J. Neurosci. 27, 12860-12867.
77. Schultz, W., Dayan, P., and Montague, P. R. (1997). A neural substrate of prediction and reward. Science 275, 1593-1599.
78. Somerville, L. H., Heatherton, T. F., and Kelley, W. M. (2006). Anterior cingulate cortex responds differentially to expectancy violation and social rejection. Nat. Neurosci. 9, 1007-1008.
79. Sridharan, D., Levitin, D. J., and Menon, V. (2008). A critical role for the right fronto-insular cortexin switching between central-executive and default-mode networks. Proc. Natl. Acad. Sci. U.S.A. 105, 12569-12574.
80. Stanley, D. A., Sokol-Hessner, P., Banaji, M. R., and Phelps, E. A. (2011). Implicit race attitudes predict trustworthiness judgments and economic trust decisions. Proc. Natl. Acad. Sci. U.S.A. 108, 7710-7715.
81. Sutton, R. S., and Barto, A. G. (1998). Reinforcement Learning. Cambridge, MA: MIT Press.
82. Talairach, J., and Tournoux, P. (1988). Co-planar Stereotaxic Atlas of the Human Brain: An Approach to Medical Cerebral Imaging. New York: Thieme Medical Publisher.
83. Todorov, A., Baron, S. G., and Oost-erhof, N. N. (2008). Evaluating face trustworthiness: a model based approach.Soc. Cogn. Affect. Neurosci. 3, 119-127.
84. Tomlin, D., Kayali, M. A., King-Casas, B., Anen, C., Camerer, C. F., Quartz, S. R., et al. (2006). Agent-specific responses in the cingulate cortex during economic exchanges. Science 312, 1047-1050.
85. Tottenham, N., Tanaka, J. W., Leon, A. C., McCarry, T., Nurse, M., Hare, T. A., et al. (2009). The NimStim set of facial expressions: judgments from untrained research participants. Psychiatry Res 168, 242-249.
86. Tricomi, E. M., Delgado, M. R., and Fiez,J.A. (2004). Modulationof caudate activity by action contingency. Neuron 41, 281-292.
87. van den Bos, W., van Dijk, E., West-enberg, M., Rombouts, S. A., and Crone, E. A. (2009). What motivates repayment? Neural correlates of reciprocity in the Trust Game. Soc. Cogn. Affect. Neurosci. 4, 294-304.
88. Williams, K. D., Cheung, C. K., and Choi, W. (2000). Cyberostracism: effects of being ignored over the Internet. J. Pers. Soc. Psychol. 79, 748-762.
89. Willis, J., and Todorov, A. (2006). First impressions: making up your mind after a 100-ms exposure to a face. Psychol. Sci. 17, 592-598.
90. Zink, C. F., Pagnoni, G., Martin-Skurski, M. E., Chappelow, J. C., and Berns, G. S. (2004). Human stri-atal responses to monetary reward depend on saliency. Neuron 42, 509-517.