Intact reward learning but elevated delay discounting in Parkinson's disease patients with impulsive-compulsive spectrum behaviors

Abstract

It has been postulated that impulsive-compulsive spectrum behaviors (ICBs) in Parkinson's disease (PD) reflect overvaluation of rewards, resulting from excessive dopaminergic transmission in the ventral striatum. However, as the ventral striatum is also strongly implicated in delay discounting, an alternative explanation would be that, similar to stimulant-dependent individuals, PD patients with ICBs impulsively discount future rewards. To test these hypotheses, we investigated whether 36 medicated PD patients with and without ICBs differed from controls on measures of stimulus-reinforcement learning and delay discounting. There was a clear double dissociation between reward learning and impulsivity in PD patients with and without ICBs. Although PD patients without ICBs were impaired at learning stimulus-reward associations for high-probability stimuli, PD patients with ICBs were able to learn such associations equally as well as controls. By contrast, PD patients with ICBs showed highly elevated delay discounting, whereas PD patients without ICBs did not differ from controls on this measure. These results contradict the hypothesis that ICBs in PD result from overvaluation of rewards. Instead, our data are more consistent with a model in which excessive dopaminergic transmission induces a strong preference for immediate over future rewards, driving maladaptive behavior in PD patients with ICBs.

Figure 1

Hyperbolic discounting measure, k, from the Kirby delay discounting questionnaire. PD+ICB patients were significantly less tolerant of delay than PD−ICB patients (p=0.00068) and control participants (p=0.00002), who did not differ (p=0.42). Values are means; error bars indicate SEM. ^***p<0.001.

Figure 2

Visual analog scale (VAS) ratings for high- and low-probability-reinforced stimuli. (a) Both the control (p=0.0006) and the PD+ICB (p=0.048) groups rated high-probability-reinforced stimuli as significantly more likely to yield reward than the PD−ICB group, but did not differ from each other (p=0.158). (b) The groups did not differ in terms of VAS ratings for stimuli that had a low probability of being reinforced. Values are means; error bars indicate SEM. ^*p<0.05; ^***p<0.001.