Serotonin modulates striatal responses to fairness and retaliation in humans

Journal of Neuroscience

Volumn 33, Issue 8, 2013, Pages 3505-3513

  Crockett, Molly J ^a,b,c   Apergis Schoute, Annemieke ^a,b   Herrmann, Benedikt ^d   Lieberman, Matt ^e   Müller, Ulrich ^a,b   Robbins, Trevor W ^a,b   Clark, Luke ^a,b  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c UNIVERSITY OF ZURICH   (Switzerland)

^d JOINT RESEARCH CENTRE   (Italy)

^e UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

SEROTONIN; TRYPTOPHAN;

ADULT; ARTICLE; BEHAVIOR; BOLD SIGNAL; CONTROLLED STUDY; CORPUS STRIATUM; DECISION MAKING; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GAME; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; MALE; MONEY; NERVE POTENTIAL; NORMAL HUMAN; PREDICTION; PRIORITY JOURNAL; PUNISHMENT; RESPONSE TIME; TASK PERFORMANCE;

ADULT; ALTRUISM; COOPERATIVE BEHAVIOR; CORPUS STRIATUM; CROSS-OVER STUDIES; DOUBLE-BLIND METHOD; FEMALE; GAMES, EXPERIMENTAL; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; PHOTIC STIMULATION; PUNISHMENT; SEROTONIN; TRYPTOPHAN; YOUNG ADULT;

EID: 84874195854     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2761-12.2013     Document Type: Article

References (61)

1. Abler B, Grön G, Hartmann A, Metzger C, Walter M (2012) Modulation of frontostriatal interaction aligns with reduced primary reward processing under serotonergic drugs. J Neurosci 32:1329-1335. CrossRef Medline
2. Amat J, Baratta MV, Paul E, Bland ST, Watkins LR, Maier SF (2005) Medial prefrontal cortex determines how stressor controllability affects behavior and dorsal raphe nucleus. Nat Neurosci 8:365-371. CrossRef Medline
3. Baumgartner T, Heinrichs M, Vonlanthen A, Fischbacher U, Fehr E (2008) Oxytocin shapes the neural circuitry of trust and trust adaptation in humans. Neuron 58:639-650. CrossRef Medline
4. Baumgartner T, Knoch D, Hotz P, Eisenegger C, Fehr E (2011) Dorsolateral and ventromedial prefrontal cortex orchestrate normative choice. Nat Neurosci 14:1468-1474. CrossRef Medline
5. Bilderbeck AC, McCabe C, Wakeley J, McGlone F, Harris T, Cowen PJ, Rogers RD (2011) Serotonergic activity influences the cognitive appraisal of close intimate relationships in healthy adults. Biol Psychiatry 69:720-725. CrossRef Medline
6. Bjork JM, Dougherty DM, Moeller FG, Swann AC (2000) Differential behavioral effects of plasma tryptophan depletion and loading in aggressive and nonaggressive men. Neuropsychopharmacology 22:357-369. CrossRef Medline
7. Blake PR, McAuliffe K (2011) "I had so much it didn't seem fair": eight-year-olds reject two forms of inequity. Cognition 120:215-224. CrossRef Medline
8. Booij L, Van der Does AJ, Riedel WJ (2003) Monoamine depletion in psychiatric and healthy populations: review. Mol Psychiatry 8:951-973. CrossRef Medline
9. Boureau YL, Dayan P (2011) Opponency revisited: competition and cooperation between dopamine and serotonin. Neuropsychopharmacology 36:74-97. CrossRef Medline
10. Camerer CF (2003) Behavioral game theory: experiments in strategic interaction. Princeton UP, Princeton, NJ.
11. Crockett MJ, Clark L, Robbins TW (2009) Reconciling the role of serotonin in behavioral inhibition and aversion: acute tryptophan depletion abolishes punishment-induced inhibition in humans. J Neurosci 29:11993-11999. CrossRef Medline
12. Crockett MJ, Clark L, Tabibnia G, Lieberman MD, Robbins TW (2008) Serotonin modulates behavioral reactions to unfairness. Science 320:1739. CrossRef Medline
13. Crockett MJ, Clark L, Hauser MD, Robbins TW (2010a) Serotonin selectively influences moral judgment and behavior through effects on harm aversion. Proc Natl Acad Sci U S A 107:17433-17438. CrossRef Medline
14. Crockett MJ, Clark L, Lieberman MD, Tabibnia G, Robbins TW (2010b) Impulsive choice and altruistic punishment are correlated and increase in tandem with serotonin depletion. Emotion 10:855-862. CrossRef Medline
15. Crockett MJ, Clark L, Apergis-Schoute AM, Morein-Zamir S, Robbins TW (2012) Serotonin modulates the effects of pavlovian aversive predictions on response vigor. Neuropsychopharmacology 37:2244-2252. CrossRef Medline
16. Delgado MR, Jou RL, Ledoux JE, Phelps EA (2009) Avoiding negative outcomes: tracking the mechanisms of avoidance learning in humans during fear conditioning. Front Behav Neurosci 3:33. CrossRef Medline
17. Delgado MR, Li J, Schiller D, Phelps EA (2008) The role of the striatum in aversive learning and aversive prediction errors. Philos Trans R Soc Lond B Biol Sci 363:3787-3800. CrossRef Medline
18. de Quervain DJ, Fischbacher U, Treyer V, Schellhammer M, Schnyder U, Buck A, Fehr E (2004) The neural basis of altruistic punishment. Science 305:1254-1258. CrossRef Medline
19. Di Cara B, Dusticier N, Forni C, Lievens JC, Daszuta A (2001) Serotonin depletion produces long lasting increase in striatal glutamatergic transmission. J Neurochem 78:240-248. CrossRef Medline
20. Dreber A, Rand DG (2012) Retaliation and antisocial punishment are overlooked in many theoretical models as well as behavioral experiments. Behav Brain Sci 35:24. CrossRef Medline
21. Dufwenberg M, Kirchsteiger G (2004) A theory of sequential reciprocity. Games Econ Behav 47:268-298. CrossRef
22. Espín AM, Brañas-Garza P, Herrmann B, Gamella JF (2012) Patient and impatient punishers of free-riders. Proc Biol Sci 279:4923-4928. CrossRef Medline
23. Fehr E, Fischbacher U (2003) The nature of human altruism. Nature 425: 785-791. CrossRef Medline
24. Fehr E, Fischbacher U (2004) Third-party punishment and social norms. Evol Hum Behav 25:63-87. CrossRef
25. Fehr E, Schmidt K (1999) A theory of fairness, competition, and cooperation. Q J Econ 114:817-868. CrossRef
26. Harlé KM, Sanfey AG (2007) Incidental sadness biases social economic decisions in the Ultimatum Game. Emotion 7:876-881. CrossRef Medline
27. Harlé KM, Chang LJ, van't Wout M, Sanfey AG (2012) The neural mechanisms of affect infusion in social economic decision-making: a mediating role of the anterior insula. Neuroimage 61:32-40. CrossRef Medline
28. Henrich J, McElreath R, Barr A, Ensminger J, Barrett C, Bolyanatz A, Cardenas JC, Gurven M, Gwako E, Henrich N, Lesorogol C, Marlowe F, Tracer D, Ziker J (2006) Costly punishment across human societies. Science 312:1767-1770. CrossRef Medline
29. Herrmann B, Thöni C, Gächter S (2008) Antisocial punishment across societies. Science 319:1362-1367. CrossRef Medline
30. Higley JD, King ST Jr, Hasert MF, Champoux M, Suomi SJ, Linnoila M (1996) Stability of interindividual differences in serotonin function and its relationship to severe aggression and competent social behavior in rhesus macaque females. Neuropsychopharmacology 14:67-76. CrossRef Medline
31. Houser D, Xiao E (2010) Inequality-seeking punishment. Econ Lett 109: 20-23. CrossRef
32. Kiser D, Steemers B, Branchi I, Homberg JR (2012) The reciprocal interaction between serotonin and social behaviour. Neurosci Biobehav Rev 36:786-798. CrossRef Medline
33. Knoch D, Pascual-Leone A, Meyer K, Treyer V, Fehr E (2006) Diminishing reciprocal fairness by disrupting the right prefrontal cortex. Science 314: 829-832. CrossRef Medline
34. Krakowski M (2003) Violence and serotonin: influence of impulse control, affect regulation, and social functioning. J Neuropsychiatry Clin Neurosci 15:294-305. CrossRef Medline
35. Krämer UM, Jansma H, Tempelmann C, Munte TF (2007) Tit-for-tat: the neural basis of reactive aggression. Neuroimage 38:203-211. CrossRef Medline
36. Linnoila M, Virkkunen M, Scheinin M, Nuutila A, Rimon R, Goodwin FK (1983) Low cerebrospinal fluid 5-hydroxyindoleacetic acid concentration differentiates impulsive from nonimpulsive violent behavior. Life Sci 33:2609-2614. CrossRef Medline
37. Maldjian JA, Laurienti PJ, Kraft RA, Burdette JH (2003) An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets. Neuroimage 19:1233-1239. CrossRef Medline
38. Martinez D, Slifstein M, Broft A, Mawlawi O, Hwang DR, Huang Y, Cooper T, Kegeles L, Zarahn E, Abi-Dargham A, Haber SN, Laruelle M (2003) Imaging human mesolimbic dopamine transmission with positron emission tomography. Part II: amphetamine-induced dopamine release in the functional subdivisions of the striatum. J Cereb Blood Flow Metab 23: 285-300. Medline
39. McCabe C, Mishor Z, Cowen PJ, Harmer CJ (2010) Diminished neural processing of aversive and rewarding stimuli during selective serotonin reuptake inhibitor treatment. Biol Psychiatry 67:439-445. CrossRef Medline
40. Moja EA, Cipolla P, Castoldi D, Tofanetti O (1989) Dose-response decrease in plasma tryptophan and in brain tryptophan and serotonin after tryptophan-free amino acid mixtures in rats. Life Sci 44:971-976. CrossRef Medline
41. O'Doherty J, Dayan P, Schultz J, Deichmann R, Friston K, Dolan RJ (2004) Dissociable roles of ventral and dorsal striatum in instrumental conditioning. Science 304:452-454. CrossRef Medline
42. Rabin M (1993) Incorporating fairness into game theory and economics. Am Econ Rev 83:1281-1302.
43. Rand DG, Greene JD, Nowak MA (2012) Spontaneous giving and calculated greed. Nature 489:427-430. CrossRef Medline
44. Rilling JK, Sanfey AG (2011) The neuroscience of social decision-making. Annu Rev Psychol 62:23-48. CrossRef Medline
45. Rilling J, Gutman D, Zeh T, Pagnoni G, Berns G, Kilts C (2002) A neural basis for social cooperation. Neuron 35:395-405. CrossRef Medline
46. Rilling JK, Goldsmith DR, Glenn AL, Jairam MR, Elfenbein HA, Dagenais JE, Murdock CD, Pagnoni G (2008) The neural correlates of the affective response to unreciprocated cooperation. Neuropsychologia 46:1256-1266. CrossRef Medline
47. Roiser JP, Blackwell AD, Cools R, Clark L, Rubinsztein DC, Robbins TW, Sahakian BJ (2006) Serotonin transporter polymorphism mediates vulnerability to loss of incentive motivation following acute tryptophan depletion. Neuropsychopharmacology 31:2264-2272. Medline
48. Sanfey AG, Rilling JK, Aronson JA, Nystrom LE, Cohen JD (2003) The neural basis of economic decision-making in the ultimatum game. Science 300:1755-1758. CrossRef Medline
49. Seymour B, Daw ND, Roiser JP, Dayan P, Dolan R (2012) Serotonin selectively modulates reward value in human decision-making. J Neurosci 32:5833-5842. CrossRef Medline
50. Stancampiano R, Melis F, Sarais L, Cocco S, Cugusi C, Fadda F (1997) Acute administration of a tryptophan-free amino acid mixture decreases 5-HT release in rat hippocampus in vivo. Am J Physiol 272:R991-R994. Medline
51. Strobel A, Zimmermann J, Schmitz A, Reuter M, Lis S, Windmann S, Kirsch P (2011) Beyond revenge: neural and genetic bases of altruistic punishment. Neuroimage 54:671-680. CrossRef Medline
52. Tabibnia G, Satpute AB, Lieberman MD (2008) The sunny side of fairness. Psychol Sci 19:339-347. CrossRef Medline
53. Tricomi EM, Delgado MR, Fiez JA (2004) Modulation of caudate activity by action contingency. Neuron 41:281-292. CrossRef Medline
54. Tricomi E, Rangel A, Camerer CF, O'Doherty JP (2010) Neural evidence for inequality-averse social preferences. Nature 463:1089-1091. CrossRef Medline
55. Tse WS, Bond AJ (2002) Serotonergic intervention affects both social dominance and affiliative behaviour. Psychopharmacology 161:324-330. CrossRef Medline
56. Tzourio-Mazoyer N, Landeau B, Papathanassiou D, Crivello F, Etard O, Delcroix N, Mazoyer B, Joliot M (2002) Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage 15:273-289. CrossRef Medline
57. Virkkunen M, Rawlings R, Tokola R, Poland RE, Guidotti A, Nemeroff C, Bissette G, Kalogeras K, Karonen SL, Linnoila M (1994) CSF biochemistries, glucose metabolism, and diurnal activity rhythms in alcoholic, violent offenders, fire setters, and healthy volunteers. Arch Gen Psychiatry 51:20-27. CrossRef Medline
58. Watson D, Clark LA, Tellegen A (1988) Development and validation of brief measures of positive and negative affect: the PANAS scales. J Pers Soc Psychol 54:1063-1070. CrossRef Medline
59. Williams JH, Perrett DI, Waiter GD, Pechey S (2007) Differential effects of tryptophan depletion on emotion processing according to face direction. Soc Cogn Affect Neurosci 2:264-273. CrossRef Medline
60. Wood RM, Rilling JK, Sanfey AG, Bhagwagar Z, Rogers RD (2006) Effects of tryptophan depletion on the performance of an iterated prisoner's dilemma game in healthy adults. Neuropsychopharmacology 31:1075-1084. CrossRef Medline
61. Zaki J, Mitchell JP (2011) Equitable decision making is associated with neural markers of intrinsic value. Proc Natl Acad Sci U S A 108:19761-19766. CrossRef Medline