The effect of Parkinson's disease and Huntington's disease on human visuomotor learning

Abstract

Visuomotor adaptation is often driven by error-based (EB) learning in which signed errors update motor commands. There are, however, visuomotor tasks where signed errors are unavailable or cannot be mapped onto appropriate motor command changes, rendering EB learning ineffective; and yet, healthy subjects can learn in these EB learning-free conditions. While EB learning depends on cerebellar integrity, the neural bases of EB-independent learning are poorly understood. As basal ganglia are involved in learning mechanisms that are independent of signed error feedback, here we tested whether patients with basal ganglia lesions, including those with Huntington's disease and Parkinson's disease, would show impairments in a visuomotor learning task that prevents the use of EB learning. We employed two visuomotor throwing tasks that were similar, but were profoundly different in the resulting visual feedback. This difference was implemented through the introduction of either a lateral displacement of the visual field via a wedge prism (EB learning) or a horizontal reversal of the visual field via a dove prism (non-EB learning). Our results show that patients with basal ganglia degeneration had normal EB learning in the wedge prism task, but were profoundly impaired in the reversing prism task that does not depend on the signed error signal feedback. These results represent the first evidence that human visuomotor learning in the absence of EB feedback depends on the integrity of the basal ganglia.

Prism adaptation in Parkinson disease: comparing reaching to walking and freezers to non-freezers

“…These results align with previous reports of normal adaptation in PD (Fernandez-Ruiz et al 2003; Gutierrez-Garralda et al 2013; Stern et al 1988; Weiner et al 1983). In contrast, Contreras-Vidal and Buch noted that people with PD adapt pointing movements slower when exposed to a large kinematic distortion (Contreras-Vidal and Buch 2003).…”

“…This suggests that to some degree, the basal ganglia influence sensorimotor recalibration or spatial realignment (Fernandez-Ruiz et al 2003; Stern et al 1988). While after-effect magnitude is reduced in PD, the adaptation process itself is relatively preserved such that adaptation rates are similar between PD and healthy controls (Gutierrez-Garralda et al 2013; Stern et al 1988). Collectively, the data from individuals with PD or cerebellar damage suggest that the processes of adaptation and storage are likely controlled by distinct but interconnected neural processes.…”

Formation of a long-term memory for visuomotor adaptation following only a few trials of practice

“…A further piece of evidence in support of the recall hypothesis is that Parkinson's disease (PD) patients are typically unimpaired in initial adaptation to a perturbation (Stern et al 1988;Gutierrez-Garralda et al 2013;Leow et al 2013;Mongeon et al 2013) but show impaired savings during readaptation (Marinelli et al 2009;Bédard and Sanes 2011;Leow et al 2013). This dissociation suggests that initial adaptation and savings depend on different processes.…”

Task errors contribute to implicit remapping in sensorimotor adaptation

“…Neuropsychological evidence in humans supports the hypothesis that implicit acquisition of a new sensorimotor map is sensitive to reward. For example, when the neurotransmitter required for processing reward, dopamine, is deficient in Parkinson’s disease, post-adaptation aftereffects are also reduced (Stern et al , 1988; Contreras-Vidal & Buch, 2003; Fernandez-Ruiz et al , 2003; Gutierrez-Garralda et al , 2013; Roemmich et al , 2014). Withdrawing dopamine medication in Parkinson’s disease patients further reduces the size of the aftereffect (Roemmich et al , 2014), demonstrating a role for dopamine reward signals in implicit remapping.…”