Abstract
Subthalamic deep brain stimulation (DBS) for Parkinson’s disease (PD) may modulate chronometric and instrumental aspects of choice behaviour, including motor inhibition, decisional slowing, and value sensitivity. However, it is not well known whether subthalamic DBS affects more complex aspects of decision-making, such as the influence of subjective estimates of uncertainty on choices. In this study, 38 participants with PD played a virtual casino prior to subthalamic DBS (whilst ‘on’ medication) and again, 3-months postoperatively (whilst ‘on’ stimulation). At the group level, there was a small but statistically significant decrease in impulsivity postoperatively, as quantified by the Barratt Impulsiveness Scale (BIS). The gambling behaviour of participants (bet increases, slot machine switches and double or nothing gambles) was associated with this self-reported measure of impulsivity. However, there was a large variance in outcome amongst participants, and we were interested in whether individual differences in subjective estimates of uncertainty (specifically, volatility) were related to differences in pre- and postoperative impulsivity. To examine these individual differences, we fit a computational model (the Hierarchical Gaussian Filter, HGF), to choices made during slot machine game play as well as a simpler reinforcement learning model based on the Rescorla-Wagner formalism. The HGF was superior in accounting for the behaviour of our participants, suggesting that participants incorporated beliefs about environmental uncertainty when updating their beliefs about gambling outcome and translating these beliefs into action. A specific aspect of subjective uncertainty, the participant’s estimate of the tendency of the slot machine’s winning probability to change (volatility), increased subsequent to DBS. Additionally, the decision temperature of the response model decreased post-operatively, implying greater stochasticity in the belief-to-choice mapping of participants. Model parameter estimates were significantly associated with impulsivity; specifically, increased uncertainty was related to increased postoperative impulsivity. Moreover, changes in these parameter estimates were significantly associated with the maximum post-operative change in impulsivity over a six month follow up period. Our findings suggest that impulsivity in PD patients may be influenced by subjective estimates of uncertainty (environmental volatility) and implicate a role for the subthalamic nucleus in the modulation of outcome certainty. Furthermore, our work outlines a possible approach to characterising those persons who become more impulsive after subthalamic DBS, an intervention in which non-motor outcomes can be highly variable.
Highlights
The subthalamic nucleus (STN) is a subcortical nucleus of central pathophysiological relevance for Parkinson’s disease (PD)
Estimates of the hierarchical gaussian filter (HGF) model perceptual parameter ω significantly increased postoperatively (t37 = −61.328, p < 0.001), and estimates of β significantly decreased (t37 = 2.124, p = 0.04), implying larger subjective estimates of uncertainty and greater stochasticity in the selection of responses after deep brain stimulation (DBS) (Table 5 and Fig. 4). ω represents a subject’s estimate about the tonic component of environmental volatility; i.e., how quickly the likelihood of winning on a given slot machine might be changing, while β represents the decision noise, or the stochasticity involved in the belief-to-choice mapping process
We employed a naturalistic gambling task and a hierarchical Bayesian model in order to investigate impulsive decision-making in participants with PD undertaking subthalamic DBS
Summary
The subthalamic nucleus (STN) is a subcortical nucleus of central pathophysiological relevance for Parkinson’s disease (PD). A computational modelling study of behaviour across three tasks commonly used to probe impulsivity (information sampling, temporal discounting and novelty bias) suggested that PD participants with ICDs are more uncertain about the relationship between possible actions and future rewards than patients without ICDs23 Based on these findings, we hypothesised that changes in impulsivity after STN-DBS may relate to estimates of environmental uncertainty about future rewards. We assessed whether a perioperative computational characterisation of subjective aspects of uncertainty (estimates of environmental volatility and stochasticity of belief-response mappings) would be associated with longitudinal changes in impulsivity during clinical follow up This latter question is clinically important as the non-motor outcomes from subthalamic DBS can be varied. There is little evidence to guide the identification of surgical candidates at risk of postoperative impulsivity[4,44]
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