Pathological choice: The neuroscience of gambling and gambling addiction

Journal of Neuroscience

Volumn 33, Issue 45, 2013, Pages 17617-17623

  Clark, Luke ^a   Averbeck, Bruno ^b   Payer, Doris ^c   Sescousse, Guillaume ^d   Winstanley, Catharine A ^e   Xue, Gui ^f  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b NATIONAL INSTITUTE OF MENTAL HEALTH   (United States)

^c CENTRE FOR ADDICTION AND MENTAL HEALTH   (Canada)

^d RADBOUD UNIVERSITY   (Netherlands)

^e UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^f BEIJING NORMAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

AMPHETAMINE; DOPAMINE; RACLOPRIDE C 11; SEROTONIN;

ARTICLE; AUTORADIOGRAPHY; COGNITION; DECISION MAKING; DOPAMINERGIC TRANSMISSION; FUNCTIONAL MAGNETIC RESONANCE IMAGING; FUNCTIONAL NEUROIMAGING; HUMAN; NERVE CONDUCTION; NEUROPSYCHOLOGY; NONHUMAN; OUTCOME ASSESSMENT; PARKINSON DISEASE; PATHOLOGICAL GAMBLING; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL; PSYCHOTHERAPY; STROOP TEST; VENTROMEDIAL PREFRONTAL CORTEX; WORKING MEMORY;

BEHAVIOR, ADDICTIVE; BRAIN; CHOICE BEHAVIOR; GAMBLING; HUMANS; MOTIVATION; NERVE NET; NEURONS; REWARD;

EID: 84887108557     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3231-13.2013     Document Type: Article

References (98)

1. Akitsuki Y, Sugiura M, Watanabe J, Yamashita K, Sassa Y, Awata S, Matsuoka H, Maeda Y, Matsue Y, Fukuda H, Kawashima R (2003) Contextdependent cortical activation in response to financial reward and penalty: an event-related fMRI study. Neuroimage 19:1674-1685. CrossRef Medline
2. Ambermoon P, Carter A, Hall WD, Dissanayaka NN, O'Sullivan JD (2011) Impulse control disorders in patients with Parkinson's disease receiving dopamine replacement therapy: evidence and implications for the addictions field. Addiction 106:283-293. CrossRef Medline
3. Ayton P, Fischer I (2004) The hot hand fallacy and the gambler's fallacy: two faces of subjective randomness? Mem Cognit 32:1369-1378. CrossRef Medline
4. Baarendse PJ, Winstanley CA, Vanderschuren LJ (2013) Simultaneous blockade of dopamine and noradrenaline reuptake promotes disadvantageous decision making in a rat gambling task. Psychopharmacology 225: 719-731. CrossRef Medline
5. Balodis IM, Kober H, Worhunsky PD, Stevens MC, Pearlson GD, Potenza MN (2012) Diminished frontostriatal activity during processing of monetary rewards and losses in pathological gambling. Biol Psychiatry 71:749-757. CrossRef Medline
6. Balzan RP, Delfabbro PH, Galletly CA, Woodward TS (2013) Illusory correlations and control across the psychosis continuum: the contribution of hypersalient evidence-hypothesis matches. J Nerv Ment Dis 201:319-327. CrossRef Medline
7. Bechara A, Damasio AR, Damasio H, Anderson SW (1994) Insensitivity to future consequences following damage to human prefrontal cortex. Cognition 50:7-15. CrossRef Medline
8. Bechara A, Damasio H, Damasio AR, Lee GP (1999) Different contributions of the human amygdala and ventromedial prefrontal cortex to decisionmaking. J Neurosci 19:5473-5481. Medline
9. Bechara A, Tranel D, Damasio H (2000) Characterization of the decisionmaking deficit of patients with ventromedial prefrontal cortex lesions. Brain 123:2189-2202. CrossRef Medline
10. 11C]-(+)-propyl-hexahydro-naphtho-oxazin in methamphetamine polydrug users: a positron emission tomography study. J Neurosci 32: 1353-1359. CrossRef Medline
11. 11C]-(+)-propyl-hexahydro-naphtho-oxazin and [ 11C]raclopride. Addiction 108:953-963. CrossRef Medline
12. Brevers D, Cleeremans A, Goudriaan AE, Bechara A, Kornreich C, Verbanck P, Noël X (2012) Decision making under ambiguity but not under risk is related to problem gambling severity. Psychiatry Res 200:568-574. CrossRef Medline
13. Brunborg GS, Johnsen BH, Mentzoni RA, Myrseth H, Molde H, Lorvik IM, Bu ET, Pallesen S (2012) Diminished aversive classical conditioning in pathological gamblers. Addiction 107:1660-1666. CrossRef Medline
14. Bühler M, Vollstädt-Klein S, Kobiella A, Budde H, Reed LJ, Braus DF, Büchel C, Smolka MN (2010) Nicotine dependence is characterized by disordered reward processing in a network driving motivation. Biol Psychiatry 67:745-752. CrossRef Medline
15. Campbell-Meiklejohn DK, Woolrich MW, Passingham RE, Rogers RD (2008) Knowing when to stop: the brain mechanisms of chasing losses. Biol Psychiatry 63:293-300. CrossRef Medline
16. Campbell-Meiklejohn D, Wakeley J, Herbert V, Cook J, Scollo P, Ray MK, Selvaraj S, Passingham RE, Cowen P, Rogers RD (2011) Serotonin and dopamine play complementary roles in gambling to recover losses. Neuropsychopharmacology 36:402-410. CrossRef Medline
17. Campbell-Meiklejohn D, Simonsen A, Scheel-Krüger J, Wohlert V, Gjerløff T, Frith CD, Rogers RD, Roepstorff A, Møller A (2012) In for a penny, in for a pound: methylphenidate reduces the inhibitory effect of high stakes on persistent risky choice. J Neurosci 32:13032-13038. CrossRef Medline
18. Clark L (2010) Decision-making during gambling: an integration of cognitive and psychobiological approaches. Philos Trans R Soc Lond B Biol Sci 365:319-330. CrossRef Medline
19. Clark L, Lawrence AJ, Astley-Jones F, Gray N (2009) Gambling near-misses enhance motivation to gamble and recruit win-related brain circuitry. Neuron 61:481-490. CrossRef Medline
20. Clark L, Stokes PR, Wu K, Michalczuk R, Benecke A, Watson BJ, Egerton A, Piccini P, Nutt DJ, Bowden-Jones H, Lingford-Hughes AR (2012) Striatal dopamine D(2)/D(3) receptor binding in pathological gambling is correlated with mood-related impulsivity. Neuroimage 63:40-46. CrossRef Medline
21. Cocker PJ, Dinelle K, Kornelson R, Sossi V, Winstanley CA (2012) Irrational choice under uncertainty correlates with lower striatal D(2/3) receptor binding in rats. J Neurosci 32:15450-15457. CrossRef Medline
22. Comings DE, Blum K (2000) Reward deficiency syndrome: genetic aspects of behavioral disorders. Prog Brain Res 126:325-341. CrossRef Medline
23. De Martino B, Camerer CF, Adolphs R (2010) Amygdala damage eliminates monetary loss aversion. Proc Natl Acad Sci U S A 107:3788-3792. CrossRef Medline
24. de Ruiter MB, Veltman DJ, Goudriaan AE, Oosterlaan J, Sjoerds Z, van den Brink W (2009) Response perseveration and ventral prefrontal sensitivity to reward and punishment in male problem gamblers and smokers. Neuropsychopharmacology 34:1027-1038. CrossRef Medline
25. Dombrovski AY, Szanto K, Siegle GJ, Wallace ML, Forman SD, Sahakian B, Reynolds CF 3rd, Clark L (2011) Lethal forethought: delayed reward discounting differentiates high- and low-lethality suicide attempts in old age. Biol Psychiatry 70:138-144. CrossRef Medline
26. Fehr C, Yakushev I, Hohmann N, Buchholz HG, Landvogt C, Deckers H, Eberhardt A, Kläger M, Smolka MN, Scheurich A, Dielentheis T, Schmidt LG, Rösch F, Bartenstein P, Gründer G, Schreckenberger M (2008) Association of low striatal dopamine D2 receptor availability with nicotine dependence similar to that seen with other drugs of abuse. Am J Psychiatry 165:507-514. CrossRef Medline
27. Fellows LK, Farah MJ (2005) Different underlying impairments in decisionmaking following ventromedial and dorsolateral frontal lobe damage in humans. Cereb Cortex 15:58-63. Medline
28. Fortune EE, Goodie AS (2012) Cognitive distortions as a component and treatment focus of pathological gambling: a review. Psychol Addict Behav 2012:298-310. CrossRef Medline
29. Goldstein RZ, Alia-Klein N, Tomasi D, Zhang L, Cottone LA, Maloney T, Telang F, Caparelli EC, Chang L, Ernst T, Samaras D, Squires NK, Volkow ND (2007) Is decreased prefrontal cortical sensitivity to monetary reward associated with impaired motivation and self-control in cocaine addiction? Am J Psychiatry 164:43-51. CrossRef Medline
30. Groman SM, Lee B, Seu E, James AS, Feiler K, Mandelkern MA, London ED, Jentsch JD (2012) Dysregulation of D(2)-mediated dopamine transmission in monkeys after chronic escalating methamphetamine exposure. J Neurosci 32:5843-5852. CrossRef Medline
31. Heidbreder CA, Gardner EL, Xi ZX, Thanos PK, Mugnaini M, Hagan JJ, Ashby CR Jr (2005) The role of central dopamine D3 receptors in drug addiction: a review of pharmacological evidence. Brain Res Brain Res Rev 49:77-105. CrossRef Medline
32. Hewig J, Kretschmer N, Trippe RH, Hecht H, Coles MG, Holroyd CB, Miltner WH (2010) Hypersensitivity to reward in problem gamblers. Biol Psychiatry 67:781-783. CrossRef Medline
33. Hodgins DC, Stea JN, Grant JE (2011) Gambling disorders. Lancet 378: 1874-1884. CrossRef Medline
34. Hollander E, Wong CM (1995) Obsessive-compulsive spectrum disorders. J Clin Psychiatry 56 [Suppl 4]:3-6, discussion 53-55.
35. Hsu M, Krajbich I, Zhao C, Camerer CF (2009) Neural response to reward anticipation under risk is nonlinear in probabilities. J Neurosci 29:2231-2237. CrossRef Medline
36. Johnson J, Tellis GJ, Macinnis DJ (2005) Losers, winners, and biased trades. J Consumer Res 32:329.
37. Joutsa J, Johansson J, Niemelä S, Ollikainen A, Hirvonen MM, Piepponen P, Arponen E, Alho H, Voon V, Rinne JO, Hietala J, Kaasinen V (2012) Mesolimbic dopamine release is linked to symptom severity in pathological gambling. Neuroimage 60:1992-1999. CrossRef Medline
38. Kahneman D (2011) Thinking, fast and slow. New York: Penguin.
39. Kahneman D, Tversky A (1979) Prospect theory: an analysis of decision under risk. Econometrica 47:264-291.
40. Kassinove JI, Schare ML (2001) Effects of the "near miss" and the "big win" on persistence at slot machine gambling. Psychol Addict Behav 15:155-158. CrossRef Medline
41. Kessler RC, Hwang I, LaBrie R, Petukhova M, Sampson NA, Winters KC, Shaffer HJ (2008) DSM-IV pathological gambling in the National Comorbidity Survey Replication. Psychol Med 38:1351-1360. CrossRef Medline
42. Kim SH, Baik SH, Park CS, Kim SJ, Choi SW, Kim SE (2011) Reduced striatal dopamine D2 receptors in people with Internet addiction. Neuroreport 22:407-411. CrossRef Medline
43. Kool W, Getz SJ, Botvinick MM (2013) Neural representation of reward probability: evidence from the illusion of control. J Cogn Neurosci 25: 852-861. CrossRef Medline
44. Kühn S, Romanowski A, Schilling C, Lorenz R, Mörsen C, Seiferth N, Banaschewski T, Barbot A, Barker GJ, Büchel C, Conrod PJ, Dalley JW, Flor H, Garavan H, Ittermann B, Mann K, Martinot JL, Paus T, Rietschel M, Smolka MN, et al. (2011) The neural basis of video gaming. Transl Psychiatry 1:e53. CrossRef Medline
45. Ladouceur R, Walker M (1996) A cognitive perspective on gambling. In: Trends in cognitive and behavioural therapies (Salkovskis PM, ed), pp 89-120. Chichester, United Kingdom: Wiley.
46. Langer EJ (1975) The illusion of control. J Pers Soc Psychol 32:311-328. CrossRef
47. Leeman RF, Potenza MN (2012) Similarities and differences between pathological gambling and substance use disorders: a focus on impulsivity and compulsivity. Psychopharmacology 219:469-490. CrossRef Medline
48. Leyton M,Vezina P (2013) Striatal ups and downs: their roles in vulnerability to addictions in humans. Neurosci Biobehav Rev. Advance online publication. Retrieved Jan. 16, 2013. doi: 10.1016/j.neubiorev.2013.01.018. CrossRef Medline
49. Ligneul R, Sescousse G, Barbalat G, Domenech P, Dreher JC (2013) Shifted risk preferences in pathological gambling. Psychol Med 43:1059-1068. CrossRef Medline
50. Limbrick-Oldfield EH, Van Holst RJ, Clark L (2013) Fronto-striatal dysregulation in drug addiction and pathological gambling: consistent inconsistencies? Neuroimage 2:385-393. CrossRef
51. Linnet J, Møller A, Peterson E, Gjedde A, Doudet D (2011) Dopamine release in ventral striatum during Iowa Gambling Task performance is associated with increased excitement levels in pathological gambling. Addiction 106:383-390. CrossRef Medline
52. Martinez D, Broft A, Foltin RW, Slifstein M, Hwang DR, Huang Y, Perez A, Frankle WG, Cooper T, Kleber HD, Fischman MW, Laruelle M (2004) Cocaine dependence and D2 receptor availability in the functional subdivisions of the striatum: relationship with cocaine-seeking behavior. Neuropsychopharmacology 29:1190-1202. CrossRef Medline
53. Martinez D, Narendran R, Foltin RW, Slifstein M, Hwang DR, Broft A, Huang Y, Cooper TB, Fischman MW, Kleber HD, Laruelle M (2007) Amphetamine-induced dopamine release: markedly blunted in cocaine dependence and predictive of the choice to self-administer cocaine. Am J Psychiatry 164:622-629. CrossRef Medline
54. Michalczuk R, Bowden-Jones H, Verdejo-Garcia A, Clark L (2011) Impulsivity and cognitive distortions in pathological gamblers attending theUK National Problem Gambling Clinic: a preliminary report. Psychol Med 41:2625-2635. CrossRef Medline
55. Miedl SF, Peters J, Büchel C (2012) Altered neural reward representations in pathological gamblers revealed by delay and probability discounting. Arch Gen Psychiatry 69:177-186. CrossRef Medline
56. 11C]-(+)-PHNO is aD3 receptor preferring agonist in vivo. Synapse 60:485-495. CrossRef Medline
57. Orgaz C, Estévez A, Matute H (2013) Pathological gamblers are more vulnerable to the illusion of control in a standard associative learning task. Front Psychol 4:306. CrossRef Medline
58. Peters J, Miedl SF, Büchel C (2012) Formal comparison of dual-parameter temporal discounting models in controls and pathological gamblers. PLoS One 7:e47225. CrossRef Medline
59. Petry NM (2006) Should the scope of addictive behaviors be broadened to include pathological gambling? Addiction 101 [Suppl 1]:152-160.
60. Petry NM, Blanco C, Auriacombe M, Borges G, Bucholz K, Crowley TJ, Grant BF, Hasin DS, O'Brien C (2013) An overview of and rationale for changes proposed for pathological gambling in DSM-5. J Gambl Stud. Advance online publication. Retrieved March 23, 2013. doi: 10.1007/ s10899-013-9370-0. CrossRef Medline
61. Rabin M (2002) Inference by believers in the law of small numbers. QJ Econ 117:775-816. CrossRef
62. Raylu N, Oei TP (2004) The Gambling Related Cognitions Scale (GRCS): development, confirmatory factor validation and psychometric properties. Addiction 99:757-769. CrossRef Medline
63. Reuter J, Raedler T, Rose M, Hand I, Gläscher J, Büchel C (2005) Pathological gambling is linked to reduced activation of the mesolimbic reward system. Nat Neurosci 8:147-148. CrossRef Medline
64. Reuven-Magril O, Dar R, Liberman N (2008) Illusion of control and behavioral control attempts in obsessive-compulsive disorder. J Abnorm Psychol 117:334-341. CrossRef Medline
65. Robinson TE, Berridge KC (2003) Addiction. Annu Rev Psychol 54:25-53. CrossRef Medline
66. Rogers RD (2011) The roles of dopamine and serotonin in decision making: evidence from pharmacological experiments in humans. Neuropsychopharmacology 36:114-132. CrossRef Medline
67. Schonberg T, Fox CR, Poldrack RA (2011) Mind the gap: bridging economic and naturalistic risk-taking with cognitive neuroscience. Trends Cogn Sci 15:11-19. CrossRef Medline
68. Schott BH, Minuzzi L, Krebs RM, Elmenhorst D, Lang M, Winz OH, Seidenbecher CI, Coenen HH, Heinze HJ, Zilles K, Düzel E, Bauer A (2008) Mesolimbic functional magnetic resonance imaging activations during reward anticipation correlate with reward-related ventral striatal dopamine release. J Neurosci 28:14311-14319. CrossRef Medline
69. Seo M, Lee E, Averbeck BB (2012) Action selection and action value in frontal-striatal circuits. Neuron 74:947-960. CrossRef Medline
70. Sescousse G, den Ouden HE (2013) Gambling rats and gambling addiction: reconciling the role of dopamine in irrationality J Neurosci 338:3256-3258. CrossRef Medline
71. Sescousse G, Barbalat G, Domenech P, Dreher JC (2013) Imbalance in the sensitivity to different types of rewards in pathological gambling. Brain 136:2527-2538. CrossRef Medline
72. Shao R, Read J, Behrens TE, Rogers RD (2013) Shifts in reinforcement signalling while playing slot-machines as a function of prior experience and impulsivity. Transl Psychiatry 3:e235. CrossRef Medline
73. Shiv B, Loewenstein G, Bechara A, Damasio H, Damasio AR (2005) Investment behavior and the negative side of emotion. Psychol Sci 16:435-439.
74. Stagg CJ, Lin RL, Mezue M, Segerdahl A, Kong Y, Xie J, Tracey I (2013) Widespread modulation of cerebral perfusion induced during and after transcranial direct current stimulation applied to the left dorsolateral prefrontal cortex. J Neurosci 33:11425-11431. CrossRef Medline
75. Stefan S, David D (2013) Recent developments in the experimental investigation of the illusion of control: a meta-analytic review. J Appl Soc Psychol 43:377-386. CrossRef
76. Sundali J, Croson R (2006) Biases in casino betting: the hot hand and the gambler's fallacy. Judgment Decision Making 1:1-12.
77. Takahashi H, Matsui H, Camerer C, Takano H, Kodaka F, Ideno T, Okubo S, Takemura K, Arakawa R, Eguchi Y, Murai T, Okubo Y, Kato M, Ito H, Suhara T (2010) Dopamine D(1) receptors and nonlinear probability weighting in risky choice. J Neurosci 30:16567-16572. CrossRef Medline
78. Takahashi H, Fujie S, Camerer C, Arakawa R, Takano H, Kodaka F, Matsui H, Ideno T, Okubo S, Takemura K, Yamada M, Eguchi Y, Murai T, Okubo Y, Kato M, Ito H, Suhara T (2013) Norepinephrine in the brain is associated with aversion to financial loss. Mol Psychiatry 18:3-4. CrossRef Medline
79. Tobler PN, Christopoulos GI, O'Doherty JP, Dolan RJ, Schultz W (2008) Neuronal distortions of reward probability without choice. J Neurosci 28:11703-11711. CrossRef Medline
80. Tom SM, Fox CR, Trepel C, Poldrack RA (2007) The neural basis of loss aversion in decision-making under risk. Science 315:515-518. CrossRef Medline
81. Trepel C, Fox CR, Poldrack RA (2005) Prospect theory on the brain? Toward a cognitive neuroscience of decision under risk. Brain Res Cogn Brain Res 23:34-50. CrossRef Medline
82. 11C]-(+)-PHNO: dissection of D3 signal and anatomy. Neuroimage 54:264-277. CrossRef Medline
83. van Holst RJ, van den Brink W, Veltman DJ, Goudriaan AE (2010) Why gamblers fail to win: a review of cognitive and neuroimaging findings in pathological gambling. Neurosci Biobehav Rev 34:87-107. CrossRef Medline
84. van Holst RJ, Veltman DJ, Büchel C, van den Brink W, Goudriaan AE (2012) Distorted expectancy coding in problem gambling: is the addictive in the anticipation? Biol Psychiatry 71:741-748. CrossRef Medline
85. Volkow ND, Wang GJ, Fowler JS, Logan J, Gatley SJ, Hitzemann R, Chen AD, Dewey SL, Pappas N (1997) Decreased striatal dopaminergic responsiveness in detoxified cocaine-dependent subjects. Nature 386:830-833. CrossRef Medline
86. Volkow ND, Fowler JS, Wang GJ, Swanson JM, Telang F (2007) Dopamine in drug abuse and addiction: results of imaging studies and treatment implications. Arch Neurol 64:1575-1579. CrossRef Medline
87. Voon V, Sohr M, Lang AE, Potenza MN, Siderowf AD, Whetteckey J, Weintraub D, Wunderlich GR, Stacy M (2011) Impulse control disorders in Parkinson disease: a multicenter case-control study. Ann Neurol 69:986-996. CrossRef Medline
88. 11C]-(+)-PHNO positron emission tomography study. Neuropsychopharmacology 33:279-289. CrossRef Medline
89. Winstanley CA, Cocker PJ, Rogers RD (2011) Dopamine modulates reward expectancy during performance of a slot machine task in rats: evidence for a "near-miss" effect. Neuropsychopharmacology 36:913-925. CrossRef Medline
90. Wrase J, Schlagenhauf F, Kienast T, Wüstenberg T, Bermpohl F, Kahnt T, Beck A, Ströhle A, Juckel G, Knutson B, Heinz A (2007) Dysfunction of reward processing correlates with alcohol craving in detoxified alcoholics. Neuroimage 35:787-794. CrossRef Medline
91. Xue G, Lu Z, Levin IP, Bechara A (2011) An fMRI study of risk-taking following wins and losses: implications for the gambler's fallacy. Hum Brain Mapp 32:271-281. CrossRef Medline
92. Xue G, He Q, Lei X, Chen C, Liu Y, Chen C, Lu ZL, Dong Q, Bechara A (2012a) The gambler's fallacy is associated with weak affective decision making but strong cognitive ability. PLoS One 7:e47019. CrossRef Medline
93. Xue G, Juan CH, Chang CF, Lu ZL, Dong Q (2012b) Lateral prefrontal cortex contributes to maladaptive decisions. Proc Natl Acad Sci U S A 109:4401-4406. CrossRef Medline
94. Xue G, He Q, Lu ZL, Levin IP, Dong Q, Bechara A (2013) Agency modulates the lateral and medial prefrontal cortex responses in belief-based decision making. PLoS One 8:e65274. CrossRef Medline
95. Zeeb FD, Winstanley CA (2011) Lesions of the basolateral amygdala and orbitofrontal cortex differentially affect acquisition and performance of a rodent gambling task. J Neurosci 31:2197-2204. CrossRef Medline
96. Zeeb FD, Winstanley CA (2013) Functional disconnection of the orbitofrontal cortex and basolateral amygdala impairs acquisition of a rat gambling task and disrupts animals' ability to alter decision-making behavior after reinforcer devaluation. J Neurosci 33:6434-6443. CrossRef Medline
97. Zeeb FD, Robbins TW, Winstanley CA (2009) Serotonergic and dopaminergic modulation of gambling behavior as assessed using a novel rat gambling task. Neuropsychopharmacology 34:2329-2343. CrossRef Medline
98. Zeeb FD, Wong AC, Winstanley CA (2013) Differential effects of environmental enrichment, social-housing, and isolation-rearing on a rat gambling task: dissociations between impulsive action and risky decision-making. Psychopharmacology 225:381-395. CrossRef Medline