Damage to insula abolishes cognitive distortions during simulated gambling

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 16, 2014, Pages 6098-6103

  Clark, Luke ^a   Studer, Bettina ^a,b   Bruss, Joel ^c   Tranel, Daniel ^c,d   Bechara, Antoine ^e  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c UNIVERSITY OF IOWA   (United States)

^d E11 SSH   (United States)

^e UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

Emotion; Insular cortex; Neuropsychology

Indexed keywords

AMYGDALOID NUCLEUS; ARTICLE; BRAIN INJURY; BRAIN REGION; CEREBROVASCULAR ACCIDENT; CLINICAL ARTICLE; COGNITIVE BIAS; COGNITIVE DEFECT; COGNITIVE DISTORTION; CONTROLLED STUDY; DECISION MAKING; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GAMBLING; GAME; HUMAN; INSULA; MOTIVATION; NEUROPSYCHOLOGICAL TEST; OUTCOME ASSESSMENT; PRIORITY JOURNAL; REINFORCEMENT; SECONDARY SOMATOSENSORY CORTEX; TASK PERFORMANCE; VENTROMEDIAL PREFRONTAL CORTEX;

EMOTION; INSULAR CORTEX; NEUROPSYCHOLOGY;

AMYGDALA; CEREBRAL CORTEX; CHOICE BEHAVIOR; COGNITION DISORDERS; COMPUTER SIMULATION; GAMBLING; HUMANS; MOTIVATION; PREFRONTAL CORTEX; TASK PERFORMANCE AND ANALYSIS;

EID: 84899106192     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1322295111     Document Type: Article

References (66)

1. Kessler RC, et al. (2008) DSM-IV pathological gambling in the National Comorbidity Survey Replication. Psychol Med 38(9):1351-1360.
2. Wardle H, et al. (2010) British Gambling Prevalence Survey (National Centre for Social Research, London).
3. Clark L (2010) Decision-making during gambling: An integration of cognitive and psychobiological approaches. Philos Trans R Soc Lond B Biol Sci 365(1538):319-330.
4. Ladouceur R, Walker M (1996) A cognitive perspective on gambling. Trends in Cognitive and Behavioural Therapies, ed Salkovskis PM (Wiley, Chichester, UK), pp 89-120.
5. Langer EJ (1975) The illusion of control. J Pers Soc Psychol 32:311-328.
6. 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(3):481-490.
7. Ayton P, Fischer I (2004) The hot hand fallacy and the gambler's fallacy: Two faces of subjective randomness? Mem Cognit 32(8):1369-1378. (Pubitemid 40524884)
8. Croson R, Sundali J (2005) The gambler's fallacy and the hot hand: Empirical data from casinos. J Risk Uncertain 30:195-209. (Pubitemid 40937231)
9. Fenton-O'Creevy M, Nicholson N, Soane E, Willman P (2003) Trading on illusions: Unrealistic perceptions of control and trading performance. J Occup Organ Psychol 76:53-68.
10. Tinsley CH, Dillon R, Cronin M (2012) How near-miss events amplify or attenuate risky decision making. Manage Sci 58:1596-1613.
11. Michalczuk R, Bowden-Jones H, Verdejo-Garcia A, Clark L (2011) Impulsivity and cognitive distortions in pathological gamblers attending the UK National Problem Gambling Clinic: A preliminary report. Psychol Med 41(12):2625-2635.
12. Miller NV, Currie SR (2008) A Canadian population level analysis of the roles of irrational gambling cognitions and risky gambling practices as correlates of gambling intensity and pathological gambling. J Gambl Stud 24(3):257-274.
13. Fortune EE, Goodie AS (2012) Cognitive distortions as a component and treatment focus of pathological gambling: A review. Psychol Addict Behav 26(2):298-310.
14. Balodis IM, et al. (2012) Diminished frontostriatal activity during processing of monetary rewards and losses in pathological gambling. Biol Psychiatry 71(8):749-757.
15. Miedl SF, Peters J, Büchel C (2012) Altered neural reward representations in pathological gamblers revealed by delay and probability discounting. Arch Gen Psychiatry 69(2):177-186.
16. Reuter J, et al. (2005) Pathological gambling is linked to reduced activation of the mesolimbic reward system. Nat Neurosci 8(2):147-148. (Pubitemid 40194043)
17. 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(8):741-748.
18. Limbrick-Oldfield EH, van Holst RJ, Clark L (2013) Fronto-striatal dysregulation in drug addiction and pathological gambling: Consistent inconsistencies? Neuroimage Clin 2:385-393.
19. 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. Translat Psychiatry 3:e235.
20. Akitsuki Y, et al. (2003) Context-dependent cortical activation in response to financial reward and penalty: An event-related fMRI study. Neuroimage 19(4):1674-1685. (Pubitemid 37025863)
21. Elliott R, Friston KJ, Dolan RJ (2000) Dissociable neural responses in human reward systems. J Neurosci 20(16):6159-6165. (Pubitemid 30658409)
22. Xue G, Lu Z, Levin IP, Bechara A (2010) The impact of prior risk experiences on subsequent risky decision-making: the role of the insula. Neuroimage 50(2):709-716.
23. Rorden C, Karnath HO (2004) Using human brain lesions to infer function: A relic from a past era in the fMRI age? Nat Rev Neurosci 5(10):813-819. (Pubitemid 39336218)
24. Bechara A, Tranel D, Damasio H (2000) Characterization of the decision-making deficit of patients with ventromedial prefrontal cortex lesions. Brain 123(pt 11):2189-2202.
25. Damasio A, Damasio H, Tranel D (2013) Persistence of feelings and sentience after bilateral damage of the insula. Cereb Cortex 23(4):833-846.
26. Shiv B, Loewenstein G, Bechara A, Damasio H, Damasio AR (2005) Investment behavior and the negative side of emotion. Psychol Sci 16(6):435-439. (Pubitemid 40855730)
27. Goudriaan AE, Oosterlaan J, de Beurs E, van den Brink W (2006) Neurocognitive functions in pathological gambling: A comparison with alcohol dependence, Tourette syndrome and normal controls. Addiction 101(4):534-547. (Pubitemid 43375617)
28. Lawrence AJ, Luty J, Bogdan NA, Sahakian BJ, Clark L (2009) Problem gamblers share deficits in impulsive decision-making with alcohol-dependent individuals. Addiction 104(6):1006-1015.
29. Arana FS, et al. (2003) Dissociable contributions of the human amygdala and orbitofrontal cortex to incentive motivation and goal selection. J Neurosci 23(29):9632-9638. (Pubitemid 37352063)
30. Bechara A, Damasio H, Damasio AR, Lee GP (1999) Different contributions of the human amygdala and ventromedial prefrontal cortex to decision-making. J Neurosci 19(13):5473-5481. (Pubitemid 29300212)
31. Clark L, et al. (2008) Differential effects of insular and ventromedial prefrontal cortex lesions on risky decision-making. Brain 131(pt 5):1311-1322.
32. Lesieur HR, Blume SB (1987) The South Oaks Gambling Screen (SOGS): A new instrument for the identification of pathological gamblers. Am J Psychiatry 144(9):1184-1188. (Pubitemid 17147523)
33. Raylu N, Oei TP (2004) The Gambling Related Cognitions Scale (GRCS): Development, confirmatory factor validation and psychometric properties. Addiction 99(6):757-769. (Pubitemid 38747913)
34. Clark L, Crooks B, Clarke R, Aitken MR, Dunn BD (2012) Physiological responses to near-miss outcomes and personal control during simulated gambling. J Gambl Stud 28(1):123-137.
35. Jessup RK, O'Doherty JP (2011) Human dorsal striatal activity during choice discriminates reinforcement learning behavior from the gambler's fallacy. J Neurosci 31(17):6296-6304.
36. Huettel SA, Mack PB, McCarthy G (2002) Perceiving patterns in random series: Dynamic processing of sequence in prefrontal cortex. Nat Neurosci 5(5):485-490. (Pubitemid 34454256)
37. Xue G, Juan CH, Chang CF, Lu ZL, Dong Q (2012) Lateral prefrontal cortex contributes to maladaptive decisions. Proc Natl Acad Sci USA 109(12):4401-4406.
38. Dymond S, et al. (2014) Almost winning: Induced MEG theta power in insula and orbitofrontal cortex increases during gambling near-misses and is associated with BOLD signal and gambling severity. Neuroimage 91:210-219.
39. Choi JS, et al. (2012) Altered brain activity during reward anticipation in pathological gambling and obsessive-compulsive disorder. PLoS ONE 7(9):e45938.
40. Craig AD (2009) How do you feel - now? The anterior insula and human awareness. Nat Rev Neurosci 10(1):59-70.
41. Dixon MJ, et al. (2011) Psychophysiological arousal signatures of near-misses in slot machine play. Int Gambl Stud 11:1-14.
42. Naqvi NH, Rudrauf D, Damasio H, Bechara A (2007) Damage to the insula disrupts addiction to cigarette smoking. Science 315(5811):531-534. (Pubitemid 46175760)
43. Contreras M, et al. (2012) A role for the insular cortex in long-term memory for context-evoked drug craving in rats. Neuropsychopharmacology 37(9):2101-2108.
44. Pushparaj A, et al. (2013) Electrical stimulation of the insular region attenuates nicotine-taking and nicotine-seeking behaviors. Neuropsychopharmacology 38(4):690-698.
45. Kirk U, Downar J, Montague PR (2011) Interoception drives increased rational decision-making in meditators playing the ultimatum game. Front Neurosci 5:49.
46. Paulus MP, Stewart JL (2014) Interoception and drug addiction. Neuropharmacology 76(Pt B):342-350.
47. Wiebking C, et al. (2014) GABA in the insula - a predictor of the neural response to interoceptive awareness. Neuroimage 86:10-18.
48. Kuhnen CM, Knutson B (2005) The neural basis of financial risk taking. Neuron 47(5):763-770. (Pubitemid 41208013)
49. Paulus MP, Rogalsky C, Simmons A, Feinstein JS, Stein MB (2003) Increased activation in the right insula during risk-taking decision making is related to harm avoidance and neuroticism. Neuroimage 19(4):1439-1448. (Pubitemid 37025843)
50. Preuschoff K, Quartz SR, Bossaerts P (2008) Human insula activation reflects risk prediction errors as well as risk. J Neurosci 28(11):2745-2752. (Pubitemid 351398874)
51. Clark L, et al. (2013) Learning and affect following near-miss outcomes in simulated gambling. J Behav Decis Making 26:442-450.
52. Weller JA, Levin IP, Shiv B, Bechara A (2009) The effects of insula damage on decision-making for risky gains and losses. Soc Neurosci 4(4):347-358.
53. Singer T, Critchley HD, Preuschoff K (2009) A common role of insula in feelings, empathy and uncertainty. Trends Cogn Sci 13(8):334-340.
54. Chang LJ, Yarkoni T, Khaw MW, Sanfey AG (2013) Decoding the role of the insula in human cognition: Functional parcellation and large-scale reverse inference. Cereb Cortex 23(3):739-749.
55. Deen B, Pitskel NB, Pelphrey KA (2011) Three systems of insular functional connectivity identified with cluster analysis. Cereb Cortex 21(7):1498-1506.
56. Rømer Thomsen K, et al. (2013) Altered paralimbic interaction in behavioral addiction. Proc Natl Acad Sci USA 110(12):4744-4749.
57. De Martino B, Camerer CF, Adolphs R (2010) Amygdala damage eliminates monetary loss aversion. Proc Natl Acad Sci USA 107(8):3788-3792.
58. Rushworth MF, Noonan MP, Boorman ED, Walton ME, Behrens TE (2011) Frontal cortex and reward-guided learning and decision-making. Neuron 70(6):1054-1069.
59. Camille N, et al. (2004) The involvement of the orbitofrontal cortex in the experience of regret. Science 304(5674):1167-1170. (Pubitemid 38661855)
60. Gillihan SJ, et al. (2011) Contrasting roles for lateral and ventromedial prefrontal cortex in transient and dispositional affective experience. Soc Cogn Affect Neurosci 6(1):128-137.
61. Damasio AR, Tranel D, Damasio H (1990) Individuals with sociopathic behavior caused by frontal damage fail to respond autonomically to social stimuli. Behav Brain Res 41(2):81-94.
62. Palminteri S, et al. (2012) Critical roles for anterior insula and dorsal striatum in punishment-based avoidance learning. Neuron 76(5):998-1009.
63. Coricelli G, et al. (2005) Regret and its avoidance: A neuroimaging study of choice behavior. Nat Neurosci 8(9):1255-1262. (Pubitemid 43348146)
64. Tricomi EM, Delgado MR, Fiez JA (2004) Modulation of caudate activity by action contingency. Neuron 41(2):281-292. (Pubitemid 38125188)
65. Frank RJ, Damasio H, Grabowski TJ (1997) Brainvox: An interactive, multimodal visualization and analysis system for neuroanatomical imaging. Neuroimage 5(1):13-30. (Pubitemid 27481300)
66. Cardinal RN, Aitken MRF (2006) ANOVA for the Behavioural Sciences Researcher (Lawrence Erlbaum, Mahwah, NJ).