Journal of Neurology

, Volume 262, Issue 6, pp 1504–1514 | Cite as

Single versus multiple impulse control disorders in Parkinson’s disease: an 11C-raclopride positron emission tomography study of reward cue-evoked striatal dopamine release

  • Kit Wu
  • Marios Politis
  • Sean S. O’Sullivan
  • Andrew D. Lawrence
  • Sarah Warsi
  • Subrata Bose
  • Andrew J. Lees
  • Paola Piccini
Original Communication

Abstract

Impulse control disorders (ICDs) are reported in Parkinson’s disease (PD) in association with dopaminergic treatment. Approximately 25 % of patients with ICDs have multiple co-occurring ICDs (i.e. more than one diagnosed ICD). The extent to which dopaminergic neurotransmission in PD patients with multiple ICDs differs from those with only one diagnosed ICD is unknown. The aims of this study are: (1) to investigate dopamine neurotransmission in PD patients diagnosed with multiple ICDs, single ICDs and non-ICD controls in response to reward-related visual cues using positron emission tomography with 11C-raclopride. (2) to  compare clinical features of the above three groups. PD individuals with mulitple ICDs (n = 10), single ICD (n = 7) and no ICDs (n = 9) were recruited and underwent two positron emission tomography (PET) scans with 11C-raclopride: one where they viewed neutral visual cues and the other where they viewed a range of visual cues related to different rewards. Individuals with both multiple ICDs and single ICDs showed significantly greater ventral striatal dopamine release compared to non-ICD PD individuals in response to reward cues, but the two ICD groups did not differ from each other in the extent of dopamine release. Subjects with multiple ICDs were, however, significantly more depressed, and had higher levels of impulsive sensation-seeking compared to subjects with single ICDs and without ICDs. This is the first study to compare dopamine neurotransmission using PET neuroimaging in PD subjects with multiple vs. single ICDs. Our results suggest that striatal dopamine neurotransmission is not directly related to the co-occurrence of ICDs in PD, potentially implicating non-dopaminergic mechanisms linked to depression; and suggest that physicians should be vigilant in managing depression in PD patients with ICDs.

Keywords

Parkinson’s disease Impulse control disorders PET Comorbidity Neuroimaging Addiction 

Notes

Acknowledgments

This work was supported by funding from Parkinson’s UK and the Reta Lila Weston Institute for Neurological studies. The authors wish to thank all participants for taking part in this study.

Conflicts of interest

This work was supported by funding from Parkinson’s UK and the Reta Lila Weston Institute for Neurological studies. We confirm that all authors have read the manuscript, the paper has not been previously published, and it is not under simultaneous consideration by another journal. There has been no ghost writing by anyone not named on the author list. We confirm that there is no potential conflict of interest with this research study.

Ethical standard

This study has been approved by the appropriate ethics committee and has therefore been performed in the accordance with the ethical standards laid down in the 1964 Declaration of Helsinki.

References

  1. 1.
    American Psychiatric Association (2013) Diagnostic and statistical manual of mental disorders, 5th edn. American Psychiatric Publishing, ArlingtonGoogle Scholar
  2. 2.
    Weintraub D, Koester J, Potenza MN et al (2010) Impulse control disorders in Parkinson disease: a cross-sectional study of 3090 patients. Arch Neurol 67(5):589–595. doi:10.1001/archneurol.2010.65 (published online first: Epub date)CrossRefPubMedGoogle Scholar
  3. 3.
    Voon V, Sohr M, Lang AE et al (2011) Impulse control disorders in Parkinson disease: a multicenter case–control study. Ann Neurol 69(6):986–996. doi:10.1002/ana.22356 (published online first: Epub date)CrossRefPubMedGoogle Scholar
  4. 4.
    Grant JE, Kim SW (2003) Comorbidity of impulse control disorders in pathological gamblers. Acta Psychiatr Scand 108(3):203–207CrossRefPubMedGoogle Scholar
  5. 5.
    Krueger RF, Bezdjian S (2009) Enhancing research and treatment of mental disorders with dimensional concepts: toward DSM-V and ICD-11. World psychiatry Off J World Psychiatr Assoc 8(1):3–6Google Scholar
  6. 6.
    Verhulst FC, van der Ende J (1993) “Comorbidity” in an epidemiological sample: a longitudinal perspective. J Child Psychol Psychiatry 34(5):767–783CrossRefPubMedGoogle Scholar
  7. 7.
    Robinson TE, Berridge KC (1993) The neural basis of drug craving: an incentive-sensitization theory of addiction. Brain Res Brain Res Rev 18(3):247–291CrossRefPubMedGoogle Scholar
  8. 8.
    Joutsa J, Johansson J, Niemela S et al (2012) Mesolimbic dopamine release is linked to symptom severity in pathological gambling. Neuroimage 60(4):1992–1999. doi:10.1016/j.neuroimage.2012.02.006 (published online first: Epub date)CrossRefPubMedGoogle Scholar
  9. 9.
    Berridge KC (2012) From prediction error to incentive salience: mesolimbic computation of reward motivation. Eur J Neurosci 35(7):1124–1143. doi:10.1111/j.1460-9568.2012.07990.x (published online first: Epub date)PubMedCentralCrossRefPubMedGoogle Scholar
  10. 10.
    Nocjar C, Panksepp J (2002) Chronic intermittent amphetamine pretreatment enhances future appetitive behavior for drug- and natural-reward: interaction with environmental variables. Behav Brain Res 128(2):189–203CrossRefPubMedGoogle Scholar
  11. 11.
    Piccini PP (2003) Dopamine transporter: basic aspects and neuroimaging. Mov Disord 18(Suppl 7):S3–S8. doi:10.1002/mds.10571 (published online first: Epub date)CrossRefPubMedGoogle Scholar
  12. 12.
    Hughes AJ, Daniel SE, Kilford L et al (1992) Accuracy of clinical diagnosis of idiopathic Parkinson’s disease: a clinico-pathological study of 100 cases. J Neurol Neurosurg Psychiatry 55(3):181–184PubMedCentralCrossRefPubMedGoogle Scholar
  13. 13.
    Voon V, Fox SH (2007) Medication-related impulse control and repetitive behaviors in Parkinson disease. Arch Neurol 64(8):1089–1096. doi:10.1001/archneur.64.8.1089 (published online first: Epub date)CrossRefPubMedGoogle Scholar
  14. 14.
    McElroy SL, Keck PE Jr, Pope HG Jr et al (1994) Compulsive buying: a report of 20 cases. J Clin Psychiatry 55(6):242–248PubMedGoogle Scholar
  15. 15.
    Folstein MF, Folstein SE, McHugh PR (1975) “Mini-mental state”. A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 12(3):189–198CrossRefPubMedGoogle Scholar
  16. 16.
    O’Sullivan SS, Wu K, Politis M et al (2011) Cue-induced striatal dopamine release in Parkinson’s disease-associated impulsive-compulsive behaviours. Brain 134(Pt 4):969–978. doi:10.1093/brain/awr003 (published online first: Epub date)CrossRefPubMedGoogle Scholar
  17. 17.
    Beck AT, Steer RA, Ball R et al (1996) Comparison of Beck Depression Inventories-IA and -II in psychiatric outpatients. J Pers Assess 67(3):588–597. doi:10.1207/s15327752jpa6703_13 (published online first: Epub date)CrossRefPubMedGoogle Scholar
  18. 18.
    Visser M, Leentjens AF, Marinus J et al (2006) Reliability and validity of the Beck depression inventory in patients with Parkinson’s disease. Mov Disord 21(5):668–672. doi:10.1002/mds.20792 (published online first: Epub date)CrossRefPubMedGoogle Scholar
  19. 19.
    Stephenson MT, Hoyle RH, Palmgreen P et al (2003) Brief measures of sensation seeking for screening and large-scale surveys. Drug Alcohol Depend 72(3):279–286. doi:10.1016/j.drugalcdep.2003.08.003 (published online first: Epub date)CrossRefPubMedGoogle Scholar
  20. 20.
    Saunders J, Aasland O, Babor T et al (1993) Development of the Alcohol Use Disorders Identification Test (AUDIT): WHO Collaborative Project on early detection of persons with harmful alcohol consumption-II. Addiction 88(6):791–804CrossRefPubMedGoogle Scholar
  21. 21.
    Heatherton T, Kozlowski L, Frecker R et al (1993) The Fagerstrom test for nicotine dependence: a revision of the Fagerstrom tolerance questionnaire. Br J Addict 1991(86):1119–1127Google Scholar
  22. 22.
    Evans AH, Katzenschlager R, Paviour D et al (2004) Punding in Parkinson’s disease: its relation to the dopamine dysregulation syndrome. Mov Disord 19(4):397–405. doi:10.1002/mds.20045 (published online first: Epub date)CrossRefPubMedGoogle Scholar
  23. 23.
    Stebbins GT, Goetz CG (1998) Factor structure of the unified Parkinson’s disease rating scale: motor examination section. Mov Disord 13(4):633–636. doi:10.1002/mds.870130404 (published online first: Epub date)CrossRefPubMedGoogle Scholar
  24. 24.
    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(6):1063–1070CrossRefPubMedGoogle Scholar
  25. 25.
    Crawford JR, Henry JD (2004) The positive and negative affect schedule (PANAS): construct validity, measurement properties and normative data in a large non-clinical sample. Br J Clin Psychol 43(Pt 3):245–265. doi:10.1348/0144665031752934 (published online first: Epub date)CrossRefPubMedGoogle Scholar
  26. 26.
    Carter BL, Tiffany ST (1999) Cue-reactivity and the future of addiction research. Addiction 94(3):349–351CrossRefPubMedGoogle Scholar
  27. 27.
    Sodano R, Wulfert E (2010) Cue reactivity in active pathological, abstinent pathological, and regular gamblers. J Gambl Stud 26(1):53–65. doi:10.1007/s10899-009-9146-8 (published online first: Epub date)PubMedCentralCrossRefPubMedGoogle Scholar
  28. 28.
    Starcke K, Schlereth B, Domass D, Schöler T, Brand M (2013) Cue reactivity towards shopping cues in female participants. J Behav Addict 2:17–22CrossRefPubMedGoogle Scholar
  29. 29.
    Sobik L, Hutchison K, Craighead L (2005) Cue-elicited craving for food: a fresh approach to the study of binge eating. Appetite 44(3):253–261. doi:10.1016/j.appet.2004.12.001 (published online first: Epub date)CrossRefPubMedGoogle Scholar
  30. 30.
    Lang PJ, Bradley MM, Cuthbert BN (2008) International affective picture system (IAPS): affective ratings of pictures and instruction manual. Unversity of Florida, GainsvilleGoogle Scholar
  31. 31.
    Mahler SV, de Wit H (2010) Cue-reactors: individual differences in cue-induced craving after food or smoking abstinence. PLoS One 5(11):e15475. doi:10.1371/journal.pone.0015475 (published online first: Epub date)PubMedCentralCrossRefPubMedGoogle Scholar
  32. 32.
    Brix G, Zaers J, Adam LE et al (1997) Performance evaluation of a whole-body PET scanner using the NEMA protocol. National Electrical Manufacturers Association. J Nucl Med 38(10):1614–1623PubMedGoogle Scholar
  33. 33.
    Duvernoy HM (1999) The human brain: surface, blood supply, and three-dimensional sectional anatomy. Springer Wien, New YorkCrossRefGoogle Scholar
  34. 34.
    Ahsan RL, Allom R, Gousias IS et al (2007) Volumes, spatial extents and a probabilistic atlas of the human basal ganglia and thalamus. Neuroimage 38(2):261–270. doi:10.1016/j.neuroimage.2007.06.004 (published online first: Epub date)CrossRefPubMedGoogle Scholar
  35. 35.
    Lammertsma AA, Hume SP (1996) Simplified reference tissue model for PET receptor studies. Neuroimage 4(3 Pt 1):153–158. doi:10.1006/nimg.1996.0066 (published online first: Epub date)CrossRefPubMedGoogle Scholar
  36. 36.
    Gunn RN, Lammertsma AA, Hume SP et al (1997) Parametric imaging of ligand-receptor binding in PET using a simplified reference region model. Neuroimage 6(4):279–287. doi:10.1006/nimg.1997.0303 (published online first: Epub date)CrossRefPubMedGoogle Scholar
  37. 37.
    Watson D, Wiese D, Vaidya J et al (1999) The two general activation systems of affect: structural findings, evolutionary considerations, and psychobiological evidence. J Pers Soc Psychol 76:820–838CrossRefGoogle Scholar
  38. 38.
    Laruelle M, Huang Y (2001) Vulnerability of positron emission tomography radiotracers to endogenous competition. New insights. Q J Nucl Med 45(2):124–138PubMedGoogle Scholar
  39. 39.
    Steeves TD, Miyasaki J, Zurowski M et al (2009) Increased striatal dopamine release in Parkinsonian patients with pathological gambling: a [11C] raclopride PET study. Brain 132(Pt 5):1376–1385. doi:10.1093/brain/awp054 (published online first: Epub date)PubMedCentralCrossRefPubMedGoogle Scholar
  40. 40.
    Berridge KC, Robinson TE (1998) What is the role of dopamine in reward: hedonic impact, reward learning, or incentive salience? Brain Res Brain Res Rev 28(3):309–369CrossRefPubMedGoogle Scholar
  41. 41.
    Evans AH, Pavese N, Lawrence AD et al (2006) Compulsive drug use linked to sensitized ventral striatal dopamine transmission. Ann Neurol 59(5):852–858. doi:10.1002/ana.20822 (published online first: Epub date)CrossRefPubMedGoogle Scholar
  42. 42.
    Holroyd KB, Adrover MF, Fuino RL et al (2014) Loss of feedback inhibition via D2 autoreceptors enhances acquisition of cocaine taking and reactivity to drug-paired cues. Neuropsychopharmacology. doi:10.1038/npp.2014.336 (published online first: Epub date)PubMedGoogle Scholar
  43. 43.
    Buckholtz JW, Treadway MT, Cowan RL et al (2010) Dopaminergic network differences in human impulsivity. Science 329(5991):532. doi:10.1126/science.1185778 (published online first: Epub date)PubMedCentralCrossRefPubMedGoogle Scholar
  44. 44.
    Ray NJ, Miyasaki JM, Zurowski M et al (2012) Extrastriatal dopaminergic abnormalities of DA homeostasis in Parkinson’s patients with medication-induced pathological gambling: a [11C] FLB-457 and PET study. Neurobiol Dis 48(3):519–525. doi:10.1016/j.nbd.2012.06.021 (published online first: Epub date)PubMedCentralCrossRefPubMedGoogle Scholar
  45. 45.
    Lawrence AD, Brooks DJ, Whone AL (2013) Ventral striatal dopamine synthesis capacity predicts financial extravagance in Parkinson’s disease. Front Psychol 4:90. doi:10.3389/fpsyg.2013.00090 (published online first: Epub date)PubMedCentralCrossRefPubMedGoogle Scholar
  46. 46.
    Lawrence AD, Brooks DJ (2014) Ventral striatal dopamine synthesis capacity is associated with individual differences in behavioral disinhibition. Front Behav Neurosci 8:86. doi:10.3389/fnbeh.2014.00086 (published online first: Epub date)PubMedCentralCrossRefPubMedGoogle Scholar
  47. 47.
    Engber TM, Susel Z, Juncos JL et al (1989) Continuous and intermittent levodopa differentially affect rotation induced by D-1 and D-2 dopamine agonists. Eur J Pharmacol 168(3):291–298CrossRefPubMedGoogle Scholar
  48. 48.
    Robinson TE, Berridge KC (2003) Addiction. Annu Rev Psychol 54:25–53. doi:10.1146/annurev.psych.54.101601.145237 (published online first: Epub date)CrossRefPubMedGoogle Scholar
  49. 49.
    Zack M, Poulos CX (2004) Amphetamine primes motivation to gamble and gambling-related semantic networks in problem gamblers. Neuropsychopharmacology 29(1):195–207. doi:10.1038/sj.npp.1300333 (published online first: Epub date)CrossRefPubMedGoogle Scholar
  50. 50.
    Politis M, Loane C, Wu K et al (2013) Neural response to visual sexual cues in dopamine treatment-linked hypersexuality in Parkinson’s disease. Brain 136(Pt 2):400–411. doi:10.1093/brain/aws326 (published online first: Epub date)CrossRefPubMedGoogle Scholar
  51. 51.
    Joutsa J, Martikainen K, Vahlberg T et al (2012) Impulse control disorders and depression in Finnish patients with Parkinson’s disease. Parkinsonism Relat Disord 18(2):155–160. doi:10.1016/j.parkreldis.2011.09.007 (published online first: Epub date)CrossRefPubMedGoogle Scholar
  52. 52.
    Black DW, Moyer T (1998) Clinical features and psychiatric comorbidity of subjects with pathological gambling behavior. Psychiatr Serv 49(11):1434–1439CrossRefPubMedGoogle Scholar
  53. 53.
    El-Guebaly N (1995) Substance use disorders and mental illness: the relevance of comorbidity. Can J Psychiatry 40(1):2–3PubMedGoogle Scholar
  54. 54.
    Ibanez A, de Perez CI, Fernandez-Piqueras J et al (2000) Pathological gambling and DNA polymorphic markers at MAO-A and MAO-B genes. Mol Psychiatry 5(1):105–109CrossRefPubMedGoogle Scholar
  55. 55.
    Bondolfi G, Osiek C, Ferrero F (2000) Prevalence estimates of pathological gambling in Switzerland. Acta Psychiatr Scand 101(6):473–475CrossRefPubMedGoogle Scholar
  56. 56.
    Yip SW, White MA, Grilo CM et al (2011) An exploratory study of clinical measures associated with subsyndromal pathological gambling in patients with binge eating disorder. J Gambl Stud 27(2):257–270. doi:10.1007/s10899-010-9207-z (published online first: Epub date)PubMedCentralCrossRefPubMedGoogle Scholar
  57. 57.
    Dalley JW, Roiser JP (2012) Dopamine, serotonin and impulsivity. Neuroscience 215:42–58. doi:10.1016/j.neuroscience.2012.03.065 (published online first: Epub date)CrossRefPubMedGoogle Scholar
  58. 58.
    Carver CS, Johnson SL, Joormann J (2008) Serotonergic function, two-mode models of self-regulation, and vulnerability to depression: what depression has in common with impulsive aggression. Psychol Bull 134(6):912–943. doi:10.1037/a0013740 (published online first: Epub date)PubMedCentralCrossRefPubMedGoogle Scholar
  59. 59.
    Callesen MB, Weintraub D, Damholdt MF et al (2013) Impulsive and compulsive behaviors among Danish patients with Parkinson’s disease: Prevalence, depression, and personality. Parkinsonism Relat Disord. doi:10.1016/j.parkreldis.2013.09.006 (published online first: Epub date)PubMedGoogle Scholar
  60. 60.
    Munro CA, McCaul ME, Wong DF et al (2006) Sex differences in striatal dopamine release in healthy adults. Biol Psychiatry 59(10):966–974. doi:10.1016/j.biopsych.2006.01.008 (published online first: Epub date)CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Kit Wu
    • 1
  • Marios Politis
    • 1
    • 4
  • Sean S. O’Sullivan
    • 1
    • 2
  • Andrew D. Lawrence
    • 3
  • Sarah Warsi
    • 1
  • Subrata Bose
    • 1
  • Andrew J. Lees
    • 2
  • Paola Piccini
    • 1
  1. 1.Centre for Neuroinflammation and NeurodegenerationImperial College London, Hammersmith Hospital CampusLondonUK
  2. 2.Reta Lila Weston Institute of Neurological StudiesUniversity College LondonLondonUK
  3. 3.Cardiff University Brain Research Imaging Centre and School of PsychologyCardiff UniversityCardiffUK
  4. 4.Neurodegeneration Imaging Group, Department of Clinical NeuroscienceKing’s College LondonLondonUK

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