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Brain. 2019 Jan 1;142(1):146-162. doi: 10.1093/brain/awy298.

Wait and you shall see: sexual delay discounting in hypersexual Parkinson's disease.

Girard R1,2,3, Obeso I1,2,4, Thobois S5,6,7, Park SA1,2, Vidal T8,9, Favre E6, Ulla M8, Broussolle E2,6,7, Krack P10,11, Durif F8,9, Dreher JC1,2.

Author information

1
Neuroeconomics, Reward and Decision-making Team, Institut des Sciences Cognitives Marc Jeannerod, Centre National de la Recherche Scientifique, UMR 5229, Bron, France.
2
University Claude Bernard Lyon, Lyon 1, Villeurbanne, France.
3
Section of Neurosurgery, The University of Chicago Medicine and Biological Sciences, Chicago, IL, USA.
4
HM Hospitales - Centro Integral en Neurociencias HM CINAC, Móstoles, Madrid, Spain.
5
Université de Lyon, Université Claude Bernard Lyon 1, Faculté de Médecine Lyon Sud Charles Mérieux, Oullins, France.
6
Neurologie C, Hôpital Neurologique Pierre Wertheimer, Hospices Civils de Lyon, Lyon, France.
7
Physiopathology of basal ganglia, Institut des Sciences Cognitives Marc Jeannerod, Centre National de la Recherche Scientifique, UMR 5229, Bron, France.
8
Neurology Department, CHU de Clermont-Ferrand, Clermont-Ferrand, France.
9
University Clermont Auvergne, Clermont Ferrand, France.
10
University Grenoble Alpes, Grenoble Institut des Neurosciences, Grenoble, France, Inserm, Grenoble, France.
11
Movement Disorders Unit, Neurology Department, CHU de Grenoble, Grenoble, France.

Abstract

Patients with Parkinson's disease may develop impulse control disorders under dopaminergic treatments. Impulse control disorders include a wide spectrum of behaviours, such as hypersexuality, pathological gambling or compulsive shopping. Yet, the neural systems engaged in specific impulse control disorders remain poorly characterized. Here, using model-based functional MRI, we aimed to determine the brain systems involved during delay-discounting of erotic rewards in hypersexual patients with Parkinson's disease (PD+HS), patients with Parkinson's disease without hypersexuality (PD - HS) and controls. Patients with Parkinson's disease were evaluated ON and OFF levodopa (counterbalanced). Participants had to decide between two options: (i) wait for 1.5 s to briefly view an erotic image; or (ii) wait longer to see the erotic image for a longer period of time. At the time of decision-making, we investigated which brain regions were engaged with the subjective valuation of the delayed erotic reward. At the time of the rewarded outcome, we searched for the brain regions responding more robustly after waiting longer to view the erotic image. PD+HS patients showed reduced discounting of erotic delayed rewards, compared to both patients with Parkinson's disease and controls, suggesting that they accepted waiting longer to view erotic images for a longer period of time. Thus, when using erotic stimuli that motivate PD+HS, these patients were less impulsive for the immediate reward. At the brain system level, this effect was paralleled by the fact that PD+HS, as compared to controls and PD - HS, showed a negative correlation between subjective value of the delayed reward and activity of medial prefrontal cortex and ventral striatum. Consistent with the incentive salience hypothesis combining learned cue-reward associations with current relevant physiological state, dopaminergic treatment in PD+HS boosted excessive 'wanting' of rewards and heightened activity in the anterior medial prefrontal cortex and the posterior cingulate cortex, as reflected by higher correlation with subjective value of the option associated to the delayed reward when ON medication as compared to the OFF medication state. At the time of outcome, the anterior medial prefrontal/rostral anterior cingulate cortex showed an interaction between group (PD+HS versus PD - HS) and medication (ON versus OFF), suggesting that dopaminergic treatment boosted activity of this brain region in PD+HS when viewing erotic images after waiting for longer periods of time. Our findings point to reduced delay discounting of erotic rewards in PD+HS, both at the behavioural and brain system levels, and abnormal reinforcing effect of levodopa when PD+HS patients are confronted with erotic stimuli.10.1093/brain/awy298_video1awy298media15983845074001.

PMID:
30590514
DOI:
10.1093/brain/awy298
[Indexed for MEDLINE]

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