Abstract
The basal ganglia are known to play a crucial role in movement execution, but their importance for motor skill learning remains unclear. Obstacles to our understanding include the lack of a universally accepted definition of motor skill learning (definition confound), and difficulties in distinguishing learning deficits from execution impairments (performance confound). We studied how healthy subjects and subjects with a basal ganglia disorder learn fast accurate reaching movements. We addressed the definition and performance confounds by: (1) focusing on an operationally defined core element of motor skill learning (speed-accuracy learning), and (2) using normal variation in initial performance to separate movement execution impairment from motor learning abnormalities. We measured motor skill learning as performance improvement in a reaching task with a speed-accuracy trade-off. We compared the performance of subjects with Huntington's disease (HD), a neurodegenerative basal ganglia disorder, to that of premanifest carriers of the HD mutation and of control subjects. The initial movements of HD subjects were less skilled (slower and/or less accurate) than those of control subjects. To factor out these differences in initial execution, we modeled the relationship between learning and baseline performance in control subjects. Subjects with HD exhibited a clear learning impairment that was not explained by differences in initial performance. These results support a role for the basal ganglia in both movement execution and motor skill learning.
Highlights
While the basal ganglia have long been implicated in motor learning (Knowlton et al, 1996; Yin and Knowlton, 2006), their role in this type of learning remains incompletely understood
In this study we examined the role of the basal ganglia in motor skill learning
Two important features of the present study were its emphasis on how to define and measure motor skill learning, and on how to disambiguate motor execution impairment from motor learning abnormalities. We focused on these aspects in order to address longstanding limitations in our knowledge of basal ganglia function due to, respectively, variation in definitions of motor skill learning and the confounding effect of movement impairment on motor learning
Summary
While the basal ganglia have long been implicated in motor learning (Knowlton et al, 1996; Yin and Knowlton, 2006), their role in this type of learning remains incompletely understood. A large number of studies on motor learning in patients with either of two basal ganglia disorders [Parkinson’s disease (PD) and Huntington’s disease (HD)] have yielded mixed results. These studies, reviewed in the Discussion, include demonstrations of both disrupted and intact motor learning in patients with PD and patients with HD. Some of the difficulty in interpreting previous studies stems from the fact that the term “motor learning” has been used to refer to different types of learning, including motor adaptation, sequence learning, and motor skill learning (Krakauer and Mazzoni, 2011). The basal ganglia are important for normal execution of well-rehearsed movements (Marsden, 1982), and normal learning may be masked or impeded by impaired execution
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