Dissociable causal roles of dorsolateral prefrontal cortex and primary motor cortex as a function of motor skill expertise

Abstract

Established models of motor skill learning posit that early stages of learning are dominated by an attentionally demanding, effortful mode of control supported by associative corticostriatal circuits involving the dorsolateral prefrontal cortex (DLPFC). As expertise develops, automatic and “effortless” performance coincides with a transition to a reliance on sensorimotor circuits that include primary motor cortex (M1). However, the dynamics of how control evolves during the transition from novice to expert are currently unclear. This lack of clarity is due, in part, to the fact that most motor learning studies comprise a limited number of training sessions and rely on correlative techniques such as neuroimaging. Here, we train human participants on a discrete motor sequencing task over the course of six weeks, followed by an assessment of the causal roles of DLPFC and M1 at varying levels of expertise. We use repetitive transcranial magnetic stimulation to transiently disrupt activity in these regions immediately prior to performance in separate sessions. Our results confirm the dissociable importance of DLPFC and M1 as expertise develops. DLPFC stimulation leads to larger behavioral deficits for novice skills than expert skills, while M1 stimulation leads to relatively larger deficits as expertise develops. However, our results also reveal that prefrontal disruption causes performance deficits at all levels of expertise. These findings challenge existing models and indicate an evolving rather than a strictly diminishing role for DLPFC throughout learning.