Impact of Parkinson's disease and dopaminergic medication on adaptation to explicit and implicit visuomotor perturbations

Abstract

The capacity to learn new visuomotor associations is fundamental to adaptive motor behavior. Evidence suggests visuomotor learning deficits in Parkinson's disease (PD). However, the exact nature of these deficits and the ability of dopamine medication to improve them are under-explored. Previous studies suggested that learning driven by large and small movement errors engaged distinct neural mechanisms. Here, we investigated whether PD patients have a generalized impairment in visuomotor learning or selective deficits in learning from large explicit errors which engages cognitive strategies or small imperceptible movement errors involving primarily implicit learning processes. Visuomotor learning skills of non-medicated and medicated patients were assessed in two reaching tasks in which the size of visuospatial errors experienced during learning was manipulated using a novel three-dimensional virtual reality environment. In the explicit perturbation task, the visuomotor perturbation was applied suddenly resulting in large consciously detected initial spatial errors, whereas in the implicit perturbation task, the perturbation was gradually introduced in small undetectable steps such that subjects never experienced large movement errors. A major finding of this study was that PD patients in non-medicated and medicated conditions displayed slower learning rates and smaller adaptation magnitudes than healthy subjects in the explicit perturbation task, but performance similar to healthy controls in the implicit perturbation task. Also, non-medicated patients showed an average reduced deadaptation relative to healthy controls when exposed to the large errors produced by the sudden removal of the perturbation in both the explicit and implicit perturbation tasks. Although dopaminergic medication consistently improved motor signs, it produced a variable impact on learning the explicit perturbation and deadaptation and unexpectedly worsened performance in some patients. Considered together, these results indicate that PD selectively impairs the ability to learn from large consciously detected visuospatial errors. This finding suggests that basal ganglia-related circuits are important neural structures for adaptation to sudden perturbations requiring awareness and high-cost action selection. Dopaminergic treatment may selectively compromise the ability to learn from large explicit movement errors for reasons that remain to be elucidated.