Advertisement

Psychopharmacology

, Volume 207, Issue 4, pp 645–659 | Cite as

Impulsive choice and response in dopamine agonist-related impulse control behaviors

  • Valerie Voon
  • Brady Reynolds
  • Christina Brezing
  • Cecile Gallea
  • Meliha Skaljic
  • Vindhya Ekanayake
  • Hubert Fernandez
  • Marc N. Potenza
  • Raymond J. Dolan
  • Mark Hallett
Original Investigation

Abstract

Rationale

Dopaminergic medication-related impulse control disorders (ICDs) such as pathological gambling and compulsive shopping have been reported in Parkinson’s disease (PD).

Hypothesis

We hypothesized that dopamine agonists (DAs) would be associated with greater impulsive choice or greater discounting of delayed rewards in PD patients with ICDs (PDI).

Methods

Fourteen PDI patients, 14 PD controls without ICDs, and 16 medication-free matched normal controls were tested on the Experiential Discounting Task (EDT), a feedback-based intertemporal choice task, spatial working memory, and attentional set shifting. The EDT was used to assess choice impulsivity (hyperbolic K value), reaction time (RT), and decision conflict RT (the RT difference between high conflict and low conflict choices). PDI patients and PD controls were tested on and off DA.

Results

On the EDT, there was a group by medication interaction effect [F(1,26) = 5.62; p = 0.03] with pairwise analyses demonstrating that DA status was associated with increased impulsive choice in PDI patients (p = 0.02) but not in PD controls (p = 0.37). PDI patients also had faster RT compared to PD controls [F(1,26) = 7.51, p = 0.01]. DA status was associated with shorter RT [F(3,24) = 8.39, p = 0.001] and decision conflict RT [F(1,26) = 6.16, p = 0.02] in PDI patients but not in PD controls. There were no correlations between different measures of impulsivity. PDI patients on DA had greater spatial working memory impairments compared to PD controls on DA (t = 2.13, df = 26, p = 0.04).

Conclusion

Greater impulsive choice, faster RT, faster decision conflict RT, and executive dysfunction may contribute to ICDs in PD.

Keywords

Dopamine agonist Gambling Impulse control Parkinson’s disease Delay discounting 

Notes

Acknowledgments

This study was supported by intramural NINDS, R01 DA019039, and the VA VISN1 MIRECC. We would like to thank the intramural Parkinson’s disease clinic and Dr. Grisel Lopez for assessments and referral of subjects.

References

  1. Diagnostic and Statistical Manual of Mental Disorders, 4th edn (1994) American Psychiatric Association, American Psychiatric AssociationGoogle Scholar
  2. Belin D, Mar AC, Dalley JW, Robbins TW, Everitt BJ (2008) High impulsivity predicts the switch to compulsive cocaine-taking. Science 320:1352–1355CrossRefPubMedGoogle Scholar
  3. Bickel WK, Marsch LA (2001) Toward a behavioral economic understanding of drug dependence: delay discounting processes. Addiction 96:73–86CrossRefPubMedGoogle Scholar
  4. Blokland A, Sik A, Lieben C (2005) Evaluation of DOI, 8-OH-DPAT, eticlopride and amphetamine on impulsive responding in a reaction time task in rats. Behav Pharmacol 16:93–100CrossRefPubMedGoogle Scholar
  5. Bordet R, Ridray S, Carboni S, Diaz J, Sokoloff P, Schwartz JC (1997) Induction of dopamine D3 receptor expression as a mechanism of behavioral sensitization to levodopa. Proc Natl Acad Sci U S A 94:3363–3367CrossRefPubMedGoogle Scholar
  6. Cardinal RN (2006) Neural systems implicated in delayed and probabilistic reinforcement. Neural Netw 19:1277–1301CrossRefPubMedGoogle Scholar
  7. Cardinal RN, Pennicott DR, Sugathapala CL, Robbins TW, Everitt BJ (2001) Impulsive choice induced in rats by lesions of the nucleus accumbens core. Science 292:2499–2501CrossRefPubMedGoogle Scholar
  8. Cole BJ, Robbins TW (1989) Effects of 6-hydroxydopamine lesions of the nucleus accumbens septi on performance of a 5-choice serial reaction time task in rats: implications for theories of selective attention and arousal. Behav Brain Res 33:165–179CrossRefPubMedGoogle Scholar
  9. Cools R (2006) Dopaminergic modulation of cognitive function-implications for L-DOPA treatment in Parkinson’s disease. Neurosci Biobehav Rev 30:1–23CrossRefPubMedGoogle Scholar
  10. Cools R, Barker RA, Sahakian BJ, Robbins TW (2003) L-Dopa medication remediates cognitive inflexibility, but increases impulsivity in patients with Parkinson’s disease. Neuropsychologia 41:1431–1441CrossRefPubMedGoogle Scholar
  11. Dalley JW, Fryer TD, Brichard L, Robinson ES, Theobald DE, Laane K, Pena Y, Murphy ER, Shah Y, Probst K, Abakumova I, Aigbirhio FI, Richards HK, Hong Y, Baron JC, Everitt BJ, Robbins TW (2007) Nucleus accumbens D2/3 receptors predict trait impulsivity and cocaine reinforcement. Science 315:1267–1270CrossRefPubMedGoogle Scholar
  12. Diergaarde L, Pattij T, Poortvliet I, Hogenboom F, de Vries W, Schoffelmeer AN, De Vries TJ (2008) Impulsive choice and impulsive action predict vulnerability to distinct stages of nicotine seeking in rats. Biol Psychiatry 63:301–308CrossRefPubMedGoogle Scholar
  13. Dixon MR, Marley J, Jacobs EA (2003) Delay discounting by pathological gamblers. J Appl Behav Anal 36:449–458CrossRefPubMedGoogle Scholar
  14. Evans AH, Lawrence AD, Potts J, Appel S, Lees AJ (2005) Factors influencing susceptibility to compulsive dopaminergic drug use in Parkinson disease. Neurology 65:1570–1574CrossRefPubMedGoogle Scholar
  15. Evenden JL, Ryan CN (1996) The pharmacology of impulsive behaviour in rats: the effects of drugs on response choice with varying delays of reinforcement. Psychopharmacology (Berl) 128:161–170CrossRefGoogle Scholar
  16. Fields S, Collins C, Leraas K, Reynolds B (2009) Dimensions of impulsive behavior in adolescent smokers and nonsmokers. Exp Clin Psychopharmacol 17:302–311Google Scholar
  17. Floresco SB, Tse MT, Ghods-Sharifi S (2008) Dopaminergic and glutamatergic regulation of effort- and delay-based decision making. Neuropsychopharmacology 33:1966–1979CrossRefPubMedGoogle Scholar
  18. Frank MJ, Samanta J, Moustafa AA, Sherman SJ (2007) Hold your horses: impulsivity, deep brain stimulation, and medication in parkinsonism. Science 318:1309–1312CrossRefPubMedGoogle Scholar
  19. Goldman-Rakic PS (1992) Working memory and the mind. Sci Am 267:110–117PubMedCrossRefGoogle Scholar
  20. 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 101:534–547CrossRefPubMedGoogle Scholar
  21. Gregorios-Pippas L, Tobler PN, Schultz W (2009) Short-term temporal discounting of reward value in human ventral striatum. J Neurophysiol 101:1507–1523CrossRefPubMedGoogle Scholar
  22. Hamidovic A, Kang UJ, de Wit H (2008) Effects of low to moderate acute doses of pramipexole on impulsivity and cognition in healthy volunteers. J Clin Psychopharmacol 28:45–51CrossRefPubMedGoogle Scholar
  23. Harrison AA, Everitt BJ, Robbins TW (1997) Central 5-HT depletion enhances impulsive responding without affecting the accuracy of attentional performance: interactions with dopaminergic mechanisms. Psychopharmacology (Berl) 133:329–342CrossRefGoogle Scholar
  24. Helms CM, Reeves JM, Mitchell SH (2006) Impact of strain and D-amphetamine on impulsivity (delay discounting) in inbred mice. Psychopharmacology (Berl) 188:144–151CrossRefGoogle Scholar
  25. Hobson DE, Lang AE, Martin WR, Razmy A, Rivest J, Fleming J (2002) Excessive daytime sleepiness and sudden-onset sleep in Parkinson disease: a survey by the Canadian Movement Disorders Group. JAMA 287:455–463CrossRefPubMedGoogle Scholar
  26. Holt DD, Green L, Myerson J (2003) Is discounting impulsive? Evidence from temporal and probability discounting in gambling and non-gambling college students. Behav Processes 64:355–367CrossRefPubMedGoogle Scholar
  27. Hsu M, Krajbich I, Zhao C, Camerer CF (2009) Neural response to reward anticipation under risk is nonlinear in probabilities. J Neurosci 29:2231–2237CrossRefPubMedGoogle Scholar
  28. Kahnemann D, Tversky A (2000) Prospect theory: an analysis of decision under risk. In: Kahnemann D, Tversky A (eds) Choices, values and frames. Cambridge University Press, New YorkGoogle Scholar
  29. Kirby KN, Petry NM (2004) Heroin and cocaine abusers have higher discount rates for delayed rewards than alcoholics or non-drug-using controls. Addiction 99:461–471CrossRefPubMedGoogle Scholar
  30. Kobayashi S, Schultz W (2008) Influence of reward delays on responses of dopamine neurons. J Neurosci 28:7837–7846CrossRefPubMedGoogle Scholar
  31. Koskinen T, Ruotsalainen S, Sirvio J (2000) The 5-HT(2) receptor activation enhances impulsive responding without increasing motor activity in rats. Pharmacol Biochem Behav 66:729–738CrossRefPubMedGoogle Scholar
  32. Krishnan-Sarin S, Reynolds B, Duhig AM, Smith A, Liss T, McFetridge A, Cavallo DA, Carroll KM, Potenza MN (2007) Behavioral impulsivity predicts treatment outcome in a smoking cessation program for adolescent smokers. Drug Alcohol Depend 88:79–82CrossRefPubMedGoogle Scholar
  33. Laibson DI (1997) Golden eggs and hyperbolic discounting. Q J Econ 42:10Google Scholar
  34. Lawrence AJ, Luty J, Bogdan NA, Sahakian BJ, Clark L (2009) Problem gamblers share deficits in impulsive decision-making with alcohol-dependent individuals. Addiction 104:1006–1015CrossRefPubMedGoogle Scholar
  35. Leiserson V, Pihl RO (2007) Reward-sensitivity, inhibition of reward-seeking, and dorsolateral prefrontal working memory function in problem gamblers not in treatment. J Gambl Stud 23:435–455CrossRefPubMedGoogle Scholar
  36. Mazur JE (1987) The effect of delayed and intervening events on reinforcement value. In: Commons ML, Mazur JE, Nevin JA, Rachlin H (eds) An adjustment Procedure for Studying Delayed Reinforcement. Erlbaum, HillsdaleGoogle Scholar
  37. Melanko S, Leraas K, Collins C, Fields S, Reynolds B (2009) Characteristics of psychopathy in adolescent nonsmokers and smokers: Relations to delay discounting and self reported impulsivity. Exp Clin Psychopharmacol 17:258–265CrossRefPubMedGoogle Scholar
  38. Mitchell SH, Reeves JM, Li N, Phillips TJ (2006) Delay discounting predicts behavioral sensitization to ethanol in outbred WSC mice. Alcohol Clin Exp Res 30:429–437CrossRefPubMedGoogle Scholar
  39. Mobini S, Chiang TJ, Ho MY, Bradshaw CM, Szabadi E (2000) Effects of central 5-hydroxytryptamine depletion on sensitivity to delayed and probabilistic reinforcement. Psychopharmacology (Berl) 152:390–397CrossRefGoogle Scholar
  40. Owen AM, Iddon JL, Hodges JR, Summers BA, Robbins TW (1997) Spatial and non-spatial working memory at different stages of Parkinson’s disease. Neuropsychologia 35:519–532CrossRefPubMedGoogle Scholar
  41. Paine TA, Dringenberg HC, Olmstead MC (2003) Effects of chronic cocaine on impulsivity: relation to cortical serotonin mechanisms. Behav Brain Res 147:135–147CrossRefPubMedGoogle Scholar
  42. Patak M, Reynolds B (2007) Question-based assessments of delay discounting: do respondents spontaneously incorporate uncertainty into their valuations for delayed rewards? Addict Behav 32:351–357CrossRefPubMedGoogle Scholar
  43. Perry JL, Larson EB, German JP, Madden GJ, Carroll ME (2005) Impulsivity (delay discounting) as a predictor of acquisition of IV cocaine self-administration in female rats. Psychopharmacology (Berl) 178:193–201CrossRefGoogle Scholar
  44. Perry JL, Nelson SE, Carroll ME (2008a) Impulsive choice as a predictor of acquisition of IV cocaine self- administration and reinstatement of cocaine-seeking behavior in male and female rats. Exp Clin Psychopharmacol 16:165–177CrossRefPubMedGoogle Scholar
  45. Perry JL, Stairs DJ, Bardo MT (2008b) Impulsive choice and environmental enrichment: effects of d-amphetamine and methylphenidate. Behav Brain Res 193:48–54CrossRefPubMedGoogle Scholar
  46. Petry NM (2001a) Pathological gamblers, with and without substance use disorders, discount delayed rewards at high rates. J Abnorm Psychol 110:482–487CrossRefPubMedGoogle Scholar
  47. Petry NM (2001b) Substance abuse, pathological gambling, and impulsiveness. Drug Alcohol Depend 63:29–38CrossRefPubMedGoogle Scholar
  48. Pezze MA, Dalley JW, Robbins TW (2009) Remediation of attentional dysfunction in rats with lesions of the medial prefrontal cortex by intra-accumbens administration of the dopamine D(2/3) receptor antagonist sulpiride. Psychopharmacology (Berl) 202:307–313CrossRefGoogle Scholar
  49. Pontone G, Williams JR, Bassett SS, Marsh L (2006) Clinical features associated with impulse control disorders in Parkinson disease. Neurology 67:1258–1261CrossRefPubMedGoogle Scholar
  50. Potenza MN (2008) Review. The neurobiology of pathological gambling and drug addiction: an overview and new findings. Philos Trans R Soc Lond B Biol Sci 363:3181–3189CrossRefPubMedGoogle Scholar
  51. Poulos CX, Le AD, Parker JL (1995) Impulsivity predicts individual susceptibility to high levels of alcohol self-administration. Behav Pharmacol 6:810–814CrossRefPubMedGoogle Scholar
  52. Reynolds B (2006a) A review of delay-discounting research with humans: relations to drug use and gambling. Behav Pharmacol 17:651–667CrossRefPubMedGoogle Scholar
  53. Reynolds B (2006b) The Experiential Discounting Task is sensitive to cigarette-smoking status and correlates with a measure of delay discounting. Behav Pharmacol 17:133–142CrossRefPubMedGoogle Scholar
  54. Reynolds B, Patak M, Shroff P (2007) Adolescent smokers rate delayed rewards as less certain than adolescent nonsmokers. Drug Alcohol Depend 90:301–303CrossRefPubMedGoogle Scholar
  55. Reynolds B, Penfold RB, Patak M (2008) Dimensions of impulsive behavior in adolescents: laboratory behavioral assessments. Exp Clin Psychopharmacol 16:124–131CrossRefPubMedGoogle Scholar
  56. Reynolds B, Richards JB, de Wit H (2006) Acute-alcohol effects on the Experiential Discounting Task (EDT) and a question-based measure of delay discounting. Pharmacol Biochem Behav 83:194–202CrossRefPubMedGoogle Scholar
  57. Reynolds B, Schiffbauer R (2004) Measuring state changes in human delay discounting: an experiential discounting task. Behav Processes 67:343–356PubMedGoogle Scholar
  58. Richards JB, Sabol KE, de Wit H (1999) Effects of methamphetamine on the adjusting amount procedure, a model of impulsive behavior in rats. Psychopharmacology (Berl) 146:432–439CrossRefGoogle Scholar
  59. Robbins TW, James M, Owen AM, Sahakian BJ, McInnes L, Rabbitt P (1994) Cambridge Neuropsychological Test Automated Battery (CANTAB): a factor analytic study of a large sample of normal elderly volunteers. Dementia 5:266–281PubMedGoogle Scholar
  60. Robinson ES, Dalley JW, Theobald DE, Glennon JC, Pezze MA, Murphy ER, Robbins TW (2008) Opposing roles for 5-HT2A and 5-HT2C receptors in the nucleus accumbens on inhibitory response control in the 5-choice serial reaction time task. Neuropsychopharmacology 33:2398–2406CrossRefPubMedGoogle Scholar
  61. Roesch MR, Takahashi Y, Gugsa N, Bissonette GB, Schoenbaum G (2007) Previous cocaine exposure makes rats hypersensitive to both delay and reward magnitude. J Neurosci 27:245–250CrossRefPubMedGoogle Scholar
  62. Schweighofer N, Shishida K, Han CE, Okamoto Y, Tanaka SC, Yamawaki S, Doya K (2006) Humans can adopt optimal discounting strategy under real-time constraints. PLoS Comput Biol 2:e152CrossRefPubMedGoogle Scholar
  63. Simon NW, Mendez IA, Setlow B (2007) Cocaine exposure causes long-term increases in impulsive choice. Behav Neurosci 121:543–549CrossRefPubMedGoogle Scholar
  64. Stanis JJ, Burns RM, Sherrill LK, Gulley JM (2008) Disparate cocaine-induced locomotion as a predictor of choice behavior in rats trained in a delay-discounting task. Drug Alcohol Depend 98:54–62CrossRefPubMedGoogle Scholar
  65. Tobler PN, Christopoulos GI, O’Doherty JP, Dolan RJ, Schultz W (2008) Neuronal distortions of reward probability without choice. J Neurosci 28:11703–11711CrossRefPubMedGoogle Scholar
  66. Tobler PN, Christopoulos GI, O’Doherty JP, Dolan RJ, Schultz W (2009) Risk-dependent reward value signal in human prefrontal cortex. Proc Natl Acad Sci U S A 106:7185–7190CrossRefPubMedGoogle Scholar
  67. van den Bergh FS, Bloemarts E, Groenink L, Olivier B, Oosting RS (2006) Delay aversion: effects of 7-OH-DPAT, 5-HT1A/1B-receptor stimulation and D-cycloserine. Pharmacol Biochem Behav 85:736–743CrossRefPubMedGoogle Scholar
  68. van Gaalen MM, van Koten R, Schoffelmeer AN, Vanderschuren LJ (2006) Critical involvement of dopaminergic neurotransmission in impulsive decision making. Biol Psychiatry 60:66–73CrossRefPubMedGoogle Scholar
  69. Voon V, Hassan K, Zurowski M, de Souza M, Thomsen T, Fox S, Lang AE, Miyasaki J (2006) Prevalence of repetitive and reward-seeking behaviors in Parkinson disease. Neurology 67:1254–1257CrossRefPubMedGoogle Scholar
  70. Voon V, Potenza MN, Thomsen T (2007) Medication-related impulse control and repetitive behaviors in Parkinson’s disease. Curr Opin Neurol 20:484–492CrossRefPubMedGoogle Scholar
  71. Wade TR, de Wit H, Richards JB (2000) Effects of dopaminergic drugs on delayed reward as a measure of impulsive behavior in rats. Psychopharmacology (Berl) 150:90–101CrossRefGoogle Scholar
  72. Weintraub D, Koester J, Potenza MN, Siderowf AD, Stacy MA, Whetteckey J, Wunderlich GR, Lang AE (2009) Dopaminergic therapy and impulse control disorders in Parkinson’s disease: a cross sectional study of over 3000 patients. Mov Disord (in press)Google Scholar
  73. Weintraub D, Siderowf AD, Potenza MN, Goveas J, Morales KH, Duda JE, Moberg PJ, Stern MB (2006) Association of dopamine agonist use with impulse control disorders in Parkinson disease. Arch Neurol 63:969–973CrossRefPubMedGoogle Scholar
  74. Winstanley CA, Dalley JW, Theobald DE, Robbins TW (2003) Global 5-HT depletion attenuates the ability of amphetamine to decrease impulsive choice on a delay-discounting task in rats. Psychopharmacology (Berl) 170:320–331CrossRefGoogle Scholar
  75. Winstanley CA, Dalley JW, Theobald DE, Robbins TW (2004a) Fractionating impulsivity: contrasting effects of central 5-HT depletion on different measures of impulsive behavior. Neuropsychopharmacology 29:1331–1343CrossRefPubMedGoogle Scholar
  76. Winstanley CA, Theobald DE, Dalley JW, Glennon JC, Robbins TW (2004b) 5-HT2A and 5-HT2C receptor antagonists have opposing effects on a measure of impulsivity: interactions with global 5-HT depletion. Psychopharmacology (Berl) 176:376–385CrossRefGoogle Scholar
  77. Winstanley CA, Theobald DE, Dalley JW, Robbins TW (2005) Interactions between serotonin and dopamine in the control of impulsive choice in rats: therapeutic implications for impulse control disorders. Neuropsychopharmacology 30:669–682PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • Valerie Voon
    • 1
  • Brady Reynolds
    • 2
  • Christina Brezing
    • 1
  • Cecile Gallea
    • 1
  • Meliha Skaljic
    • 1
  • Vindhya Ekanayake
    • 1
  • Hubert Fernandez
    • 3
  • Marc N. Potenza
    • 4
  • Raymond J. Dolan
    • 5
  • Mark Hallett
    • 1
  1. 1.National Institutes of HealthBethesdaUSA
  2. 2.Ohio State UniversityColumbusUSA
  3. 3.University of FloridaGainesvilleUSA
  4. 4.Yale UniversityNew HavenUSA
  5. 5.University College LondonLondonUK

Personalised recommendations