Cerebellar Direct Current Stimulation Enhances On-Line Motor Skill Acquisition through an Effect on Accuracy

Abstract

The cerebellum is involved in the update of motor commands during error-dependent learning. Transcranial direct current stimulation (tDCS), a form of noninvasive brain stimulation, has been shown to increase cerebellar excitability and improve learning in motor adaptation tasks. Although cerebellar involvement has been clearly demonstrated in adaptation paradigms, a type of task that heavily relies on error-dependent motor learning mechanisms, its role during motor skill learning, a behavior that likely involves errordependent as well as reinforcement and strategic mechanisms, is not completely understood. Here, in humans, we delivered cerebellar tDCS to modulate its activity during novel motor skill training over the course of 3 d and assessed gains during training (on-line effects), between days (off-line effects), and overall improvement. We found that excitatory anodal tDCS applied over the cerebellum increased skill learning relative to sham and cathodal tDCS specifically by increasing on-line rather than off-line learning. Moreover, the larger skill improvement in the anodal group was predominantly mediated by reductions in error rate rather than changes in movement time. These results have important implications for using cerebellar tDCS as an intervention to speed up motor skill acquisition and to improve motor skill accuracy, as well as to further our understanding of cerebellar function.

Effects of tDCS on motor learning and memory formation: A consensus and critical position paper

“…Interestingly, there were larger offline declines in the anodal tDCS group possibly due to a reduction in memory stability or that there was more accumulated knowledge to be lost. Despite this, the overall skill gains remained larger at one week follow up (Cantarero et al, 2015). Other previous work has shown a significant online learning enhancement effect of anodal tDCS over M1 for early training sessions only (Reis et al, 2009).…”

“…In particular, the larger gains were driven to a greater extent by reductions in error rates as opposed to changes in movement time. This suggests that specific task constraints may play a role in determining the motor network areas of interest (Cantarero et al, 2015). For example, anodal tDCS applied over the cerebellum concurrently with training for a task with very precise timing requirements enhanced offline improvement, as opposed to online learning as observed in prior studies (Wessel et al, 2016).…”

“…In contrast, anodal tDCS delivered over PMd showed no online effects relative to sham, but in fact impaired retention at 24 hours. Finally, Cantarero et al (2015) showed that applying anodal tDCS over the ipsilateral cerebellum during skill learning (SVIPT task) in young healthy individuals augmented online skill acquisition via a reduction in error rates (Cantarero et al, 2015). This effect appeared to be robust, as it was present in every session for three consecutive days (the duration of the study).…”

“…Several studies, a majority of which have focused on sequence learning, have investigated offline motor skill learning and retention over multiple (typically at least three) days of training (Table 2) (Cantarero et al, 2015;Naros et al, 2016;Reis et al, 2015;Reis et al, 2009;Saucedo-Marquez, Zhang, Swinnen, Meesen, & Wenderoth, 2013;Schambra et al, 2011;Waters-Metenier et al, 2014). Reis and colleagues (2009) found that anodal tDCS applied to M1 concurrently with training over five consecutive days resulted in significant enhancement of offline skill gains and retention compared with sham in the sequential visual isometric pinchforce task (SVIPT) (Reis et al, 2009).…”

Taking the brakes off the learning curve

“…Previous studies using both inhibitory and excitatory stimulation of the cerebellar hemisphere reported impaired motor execution during non-repetitive, adaptation tasks (Miall and Christensen 2004;Miall et al 2007;Galea et al 2011;Jayaram et al 2011;Li Voti et al 2014;Cantarero et al 2015;Herzfeld et al 2014). This is not in contradiction with our own pattern of results, since different circuits might carry out the sensorimotor adaptation (in which online error monitoring is important) and the explicit sequence learning (in which extraction of the pattern is key).…”