Abstract
Impulse control disorders (ICD) are common in Parkinson’s disease (PD) and are associated with dopaminergic medication. The purpose of this study was to investigate executive function and risk-taking behavior in PD patients with ICD. 17 PD patients with ICD (ICD-PD) were compared to 20 PD patients without ICD (CTRL-PD) using neuropsychological and experimental tasks. Executive functions were assessed using standard executive testing (Conner’s Performance Test, Modified Wisconsin Card Sorting Test, Trail Making Test and phonological verbal fluency). Subjects were also submitted to an experimental gambling task consisted of three decks of money cards: neutral deck (equal opportunity for gains as losses), winning deck (small amount of money with a positive balance) and loser deck (high amount of money with a negative balance), evaluating risk-taking behavior (number of cards picked in each deck) and valuation of the reward (subjective appreciation of the value of each deck). There was no significant difference in executive functioning between groups. Both groups selected more cards in the losing deck (high amount of money) as compared to the neutral deck (Mann–Whitney test, ICD-PD, p = 0.02; CTRL-PD, p = 0.003) and to the winning deck (Mann–Whitney test, ICD-PD p = 0.0001; CTRL-PD p = 0.003), suggesting an increased risk-taking behavior. Interestingly, we found that ICD-PD patients estimated the value of decks differently from CTRL-PD patients, taking into account mainly the positive reinforced value of the decks (Mann–Whitney test, p = 0.04). This study showed that executive pattern and risk-taking behavior are similar between ICD-PD and CTRL-PD patients. However, ICD-PD patients showed a specific deficit of the subjective estimation of the reward. Links between this deficit and metacognitive skills are discussed.
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References
Ardouin C, Chéreau I, Llorca PM et al (2009) Assessment of hyper- and hypodopaminergic behaviors in Parkinson’s disease. Rev Neurol 165:845–856. doi:10.1016/j.neurol.2009.06.003
Bechara A, Damasio AR, Damasio H, Anderson SW (1994) Insensitivity to future consequences following damages to human prefrontal cortex. Cognition 50:7–15
Brevers D, Cleeremans A, Bechara A et al (2013) Impaired self-awareness in pathological gamblers. J Gamb 29:119–129. doi:10.1007/s10899-012-9292-2
Brevers D, Cleermans A, Bechara A et al (2014) Impaired metacognitive capacities in individual with problem gambling. J Gamb Stud 30:141–152. doi:10.1007/s10899-012-9348-3
Cardebat D, Doyon B, Puel M, Goulet P, Joannette Y (1990) Formal and semantic lexical evocation in normal subjects. Performance and dynamics of production as a function of sex, age and educational level. Acta Neurol Belg 90:207–217
Cilia R, Cho SS, Van Eimeren T et al (2011) Pathological gambling in patients with Parkinson’s disease is associated with fronto-striatal disconnection: a path modeling analysis. Mov Disord 26:225–233. doi:10.1002/mds.23480
Connors K (2004) Conners’s continous performance test II (CPT-II V.5). Multi-Heath Systems Inc, Toronto
Delazer M, Sinz H, Zamarian L et al (2009) Decision-making under risk and under ambiguity in Parkinson’s disease. Neuropsychologia 47:1901–1908. doi:10.1016/j.neuropsychologia.2009.02.034
Djamshidian A, Jha A, O’Sullivan SS et al (2010) Risk and learning in impulsive and nonimpulsive patients with Parkinson’s disease. Mov Disord 25:2003–2010. doi:10.1002/mds.23247
Djamshidian A, O’Sullivan SS, Lees A, Averbeck BB (2011a) Stroop test performance in impulsive and non impulsive patients with Parkinson’s disease. Parkinsonism Relat Disord 17:212–214. doi:10.1016/j.parkreldis.2010.12.014
Djamshidian A, O’Sullivan SS, Wittmann BC, Lees AJ, Averbeck BB (2011b) Novelty seeking behavior in Parkinson’s disease. Neuropsychologia 49:2483–2488. doi:10.1016/j.neuropsychologia.2011.04.026
Dubois B, Burn D, Goetz C et al (2007) Diagnostic procedures for Parkinson’s disease dementia: recommendations from the movement disorder society task force. Mov Disord 22:2314–2324
Evans AH, Strafella AP, Weintraub D, Stacy M (2009) Impulsive and compulsive behaviors in PD. Mov Disord 24:1561–1570. doi:10.1002/mds.22505
Fossati A, Di Ceglie A, Acquarini E, Barratt ES (2001) Psychometric properties of an Italian version of the Barrat Impulsiveness Scale-11 (BIS-11) in nonclinical subjects. J Clin Psychol 57:815–828
Franck MJ, Seeberger LC, O’Reilly RC (2004) By carrot or by stick: cognitive reinforcement learning in parkinsonism. Science 306:1940–1943
Gilleen J, Greenwood K, David A (2010) Lack of insight and awareness in schizophrenia and neuropsychiatric disorders. In: Miyoshi K, Morimura Y, Maeda K (eds) Neuropsychiatric Disorders, 1st edn. Springer, Japan, p 33–49
Goerlich-Dobre KS, Probst C, Winter L et al (2014) Alexithymia-an independent risk factor for impulsive-compulsive disorders in Parkinson’s disease. Mov Disord 29:214–220. doi:10.1002/mds.25679
Gurevich EV, Joyce JN (1999) Distribution of dopamine D3 receptor expressing neurons in the human forebrain: comparison with D2 receptor expressing neurons. Neuropsychopharmacology 20:60–80
Housden CR, O’Sullivan SS, Joyce EM, Lees AJ, Roiser J (2010) Intact reward learning but elevated delay discounting in Parkinson’s disease patients with impulsive-compulsive spectrum behaviors. Neuropsychopharmacology 235:2155–2164. doi:10.1038/npp.2010.84
Leroi I, Barraclough M, McKie S, Hinvest N, Evans J, Elliott R, McDonald K (2013) Dopaminergic influences on executive function and impulsive behavior in impulse control disorders in Parkinson’s disease. J Neuropsychol 7:306–325. doi:10.1111/jnp.12026
Mack J, Okai D, Brown RG et al (2013) The role of self-awareness and cognitive dysfunction in Parkinson’s disease with and without impulse-control disorder. J Neuropsychiatry Clin Neurosci 25:141–149. doi:10.1176/appi.neuropsych.12030076
Milner B (1963) Effects of different brain lesions on card sorting: the role of the frontal lobes. Arch Neurol 9:90–100
Paulus MP (2005) Neurobiology of decision-making: quo vadis? Brain Res Cogn Brain Res 23:2–10
Pessiglione M, Seymour B, Flandin G, Dolan RJ, Frith CD (2006) Dopamine-dependent prediction errors underpin reward-seeking behavior in humans. Nature 442:1042–1045
Piray P, Zeighami Y, Barhami F, Eissa AM, Hewedi DH, Moustafa AA (2014) Impulse control disorders in Parkinson’s disease are associated with dysfunction in stimulus valuation but not action valuation. J Neurosci 34:7814–7824. doi:10.1523/JNEUROSCI.4063-13.2014
Poletti M, Bonuccelli U (2012) Impulse control disorders in Parkinson’s disease: the role of personality and cognitive status. J Neurol 259:2269–2277. doi:10.1007/s00415-012-6506-6
Rao H, Mamikonyan E, Detre JA, Siderowf AD, Stern MB, Potenza MN, Weintraub D (2010) Decreased ventral striatal activity with impulse contrl disorders in Parkinson’s disease. Mov Disord 25:1660–1669. doi:10.1002/mds.23147
Reitan RM, Wolfson D (1985) The Trail making Test. Neuropsychological Press, Tucson
Rieu I, Martinez-Martin P, Pereira B et al (2015) International validation of a behavioral scale in Parkinson’s disease without dementia. Mov Disord 30:705–713. doi:10.1002/mds.26223
Rossi M, Gerschcovich ER, De Achaval D et al (2010) Decision making in Parkinson’s disease patients with and without PG. Eur J Neurol 17:97–102. doi:10.1111/j.1468-1331.2009.02792.x
Santangelo G, Vitale C, Trojano L, Verde F, Grossi D, Barone P (2009) Cognitive dysfunctions and pathological gambling in patients with Parkinson’s disease. Mov Disord 24:899–905. doi:10.1002/mds.22472
Siri C, Cilia R, De Gaspari D et al (2010) Cognitive status of patients with Parkinson’s disease and pathological gambling. J Neurol 257:247–252. doi:10.1007/s00415-009-5301-5
Starkstein SE, Mayberg HS, Leiguarda R, Preziosi TJ, Robinson R (1992) A prospective longitudinal study of depression, cognitive decline, and physical impairments in patients with Parkinson’s disease. J Neurol Neurosurg Psychiatry 55:377–382
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 132:1376–1385. doi:10.1093/brain/awp054
Suzuki A, Aoshima T, Fukasawa T et al (2005) A three-factor of the MADRS in major depressive disorder. Depress Anxiety 21:95–97
Vitale C, Santangelo G, Trojano L et al (2011) Comparative neuropsychological profile of pathological gambling, hypersexuality and compulsive eating in Parkinson’s disease. Mov Disord 26:830–836. doi:10.1002/mds.23567
Voon V, Reynolds B, Brezing C et al (2010a) Impulse choice and response in dopamine agonist-related impulse control behaviors. Psychopharmacology 207:645–659. doi:10.1007/s00213-009-1697-y
Voon V, Pessiglione M, Brezing C et al (2010b) Mechanisms underlying dopamine-mediated reward bias in compulsive behaviors. Neuron 65:135–142. doi:10.1016/j.neuron.2009.12.027
Voon V, Sohr M, Lang AE et al (2011a) Impulse control disorders in Parkinson’s disease: a multicenter case-control study. Ann Neurol 69:986–996. doi:10.1002/ana.22356
Voon V, Gao J, Brezing C et al (2011b) Dopamine agonists and risk: impulse control disorders in Parkinson’s disease. Brain 134:1438–1446. doi:10.1093/brain/awr080
Vriend C, Nordbeck AH, Booij J et al (2014) Reduced dopamine transporter binding predate impulse control disorders in Parkinson’s disease. Mov Disord 29:904–911. doi:10.1002/mds.25886
Weintraub D, Koester J, Potenza MN et al (2010) Impulse control disorders in Parkinson’s disease: a cross-sectional study of 3090 patients. Arch Neurol 67:589–595. doi:10.1001/archneurol.2010.65
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FP has received grants from Novartis Pharma. EFR has received Grants from “poste d’accueil” APHP/CNRS, Grants from INSERM (COSSEC), Grants from APHP (DRC-PHRC), Grants from Fondation pour la Recherche sur le Cerveau (FRC), Grants, personal fees and non-financial support from Merz-pharma, Grants and personal fees from Orkyn, Grants from IP Santé, Grants and personal fees from Ultragenyx, personal fees from Novartis, personal fees and non-financial support from Ipsen Pharma, non financial supports from Teva, non-financial support from Abbvie, non-financial support from Dystonia Europe, non-financial support from the Georgian Medical and Public Health Association, non financial support from the International Federation of Clinical neurophysiology, non-financial support from the Movement Disorders Society. LL has received personal fees from Novartis Pharma, personal fees from GE, non-financial supports from Merck-Serono, Grants from Sanofi-Aventis, Grants from GSK, Grants from Cytokinetic. MV has received personal fees from Mertz, non-financial support from Movement Disorders Society, non-financial support from EAN. JCC has received personal fees and non-financial support from abbvie, personal fees from Amarentus, personal fees from Zambon, personal fees from Pfizer, personal fees from Clevexel, non-financial support from UCB, Grants from Sanofi-Aventis, Grants from Ipsen, Grants from the Michael J. Fox foundation, and own stock in B&A Therapeutics.
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All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.
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Pineau, F., Roze, E., Lacomblez, L. et al. Executive functioning and risk-taking behavior in Parkinson’s disease patients with impulse control disorders. J Neural Transm 123, 573–581 (2016). https://doi.org/10.1007/s00702-016-1549-y
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DOI: https://doi.org/10.1007/s00702-016-1549-y