Paradoxical Decision-Making: A Framework for Understanding Cognition in Parkinson's Disease

Abstract

People with Parkinson's disease (PD) show impaired decision-making when sensory and memory information must be combined. This recently identified impairment results from an inability to accumulate the proper amount of information needed to make a decision and appears to be independent of dopamine tone and reinforcement learning mechanisms. Although considerable work focuses on PD and decisions involving risk and reward, in this Opinion article we propose that the emerging findings in perceptual decision-making highlight the multisystem nature of PD, and that unraveling the neuronal circuits underlying perceptual decision-making impairment may help in understanding other cognitive impairments in people with PD. We also discuss how a decision-making framework may be extended to gain insights into mechanisms of motor impairments in PD.

Keywords: basal ganglia; decision threshold; drift diffusion model; freezing of gait; paradoxical movement; perception.

Figure 1

Memory-based perceptual decision-making task [1]. (A) Manipulation of prior information: an equal number of red and green Glass patterns was randomly interleaved over the course of the session, however stimuli of one color had an equal probability of being leftward or rightward (Equal prior); whereas for stimuli of the other color, one of the orientations occurred three times more often than the other (Unequal prior). Thus, participants had to integrate color, orientation and likelihood to determine the decision, similar in some aspects to the weather prediction task. The color and orientation were randomly interleaved across trials and which orientation occurred more often was counterbalanced across participants. See [1] for further information. (B) A schematic showing the sequence of a trial: fixation point appears, followed by the two alternative choice targets and then by the Glass pattern. Participants reported their decision as soon as it was made. A tone occurred at the end of correct trials and no sound occurred for incorrect trials. (C) Proportion of leftward (positive) choices is plotted against the orientation strength for 12 age- and sex- matched healthy participants. The grey points and lines show the data and the logistic fits in the equal prior trials (50:50) whereas the black arrows and lines show the data for unequal positive prior trials (75:25, upward arrow) or the unequal negative prior (25:75, downward arrow). (D) Same as in (C) for 12 medicated people with Parkinson’s disease. (E) Parameter estimates for the starting point of evidence accumulation in the first and second half of the session for the healthy participants of (C). Grey bars: starting point for the equal prior; black bars: starting point for the unequal prior. A positive starting point indicates that the process starts closer to the decision boundary associated with the more frequent orientation. A negative starting point indicates that the process starts closer to the opposite boundary, inconsistent with the prior. (F) Same as in (E) for the group of people with PD shown in (D). (G) Same as in (E) for the drift rate offset. A positive value of the drift rate offset indicates that the process drifts towards the bound associated with the more frequent choice according to the priors. (H) Same as in (F) for the drift rate offset. Error bars are ±SEM. Adapted from [1] with permission.

BOX 1; Figure I. Drift Diffusion Model Schematic

(A) In two choice tasks, noisy sensory evidence is accumulated over time (blue line), and a decision is made when the evdience crosses one of the two decision bounds (black lines). In the absence of a bias, evidence accumulation begins at the center of the two bounds, referred to as the starting point (red dot). The distance between the starting point of evidence accumulation and the bound is the amount of evidence required for a decision, also referred to as a decision threshold. The average rate at which evidence accumulates is referred to as the drift rate and reflects the strength of the sensory evidence. For example, when the orientation signal in the Glass pattern is strong, decisions are fast and likely to be accurate, as reflected by the positive drift rate (green arrow). In contrast, when the orientation signal in the Glass pattern is weak, evidence accimulates slowly and can lead to innacuracies (black dashed arrow). The gray arrow indicates advancing time. (B) Adjusting the starting point toward one bound (red dot), translates to less evidence required to reach that decision and choosing that option more frequently, similar to adjusting a decision criterion to be more liberal in signal detection theory. (C) Changes in the drift rate offset (angle between black dashed line and green solid line) results in faster evidence accumuation which also results in one of the options being chosen more frequently. Adapted with permission from [1].

BOX 2; Figure II. Freezing of Gait (FoG) in PD – A Clinical Example of the Importance of Priors

(A) Normal gait in the presence of congruent visual and vestibular signals. Green boxes indicate steps leading to normal gait production. (B) In the presence of conflicting sensory cues, indicated by the black box and the red outlined box, prior information (upward green arrow) can resolve the conflict in a healthy individual and result only in a normal and transient slowing of gait. (C) In PD, the failure of the ability to integrate prior information (red upward arrow) may lead to an impaired ability to adjust the decision criterion and thus suboptimal decisions and FoG.