Applying Anodal Transcranial Direct Current Stimulation at BA6 During Repetitive Practice Enhances Motor Learning by Improving Encoding and Post-Practice Consolidation

Abstract

Understanding how the structure of practice influences the consolidation and long-term retention of motor skills is important to maximize learning. Learning multiple motor sequences simultaneously is facilitated by using an interleaved as opposed to repetitive training schedule typically manifest as superior consolidation and long-term retention. Recent neural imaging data has highlighted the importance of earlier and more consistent recruitment of the BA6 region, in particular the supplementary motor area (SMA) and dorsal premotor area (PMd), during IP compared to repetitive practice (RP). Indeed, the emergence of greater functional connectivity of dorsal premotor region (PMd) during IP has been reported to be predictive of subsequent learning gains. The primary aim of this work was to modify the cortical activity at SMA (Experiment 1) and PMd (Experiment 2) during RP and IP using anodal or cathodal transcranial direct current stimulation (tDCS). The expectation was that increasing activity at these neural regions during RP should enhance offline gain. Conversely, down-regulating the cortical activity at these neural sites during IP should disrupt the expect learning benefit associated with this practice format. Participants were exposed to anodal tDCS at SMA (Exp1) and PMd (Exp2) of 2 mA during approximately 20-min of RP format or cathodal tDCS at these same sites while experiencing RP. Performance of three motor sequences was assessed in a RP format prior to any practice and immediately after practice, as well as 6-hr, 24-hr, and 72-hr after the completion of RP or IP. No stimulation was present during any of the test blocks. As expected, there was a robust learning benefit from IP manifest as superior early consolidation during the initial 6-hr after practice and further performance enhancement likely a result of more effective sleep-mediated consolidation. Applying anodal tDCS during RP at SMA (Experiment 1) led to increased offline gain both from superior early time-dependent as well as enhanced sleep-mediated consolidation. Administering anodal tDCS at PMd during RP (Experiment 2) also offered a learning benefit but surfaced from improved encoding during practice rather than from a change in post-practice consolidation processes. Cathodal stimulation at either SMA or PMd during IP failed to change the behavioral outcomes associated with their sham counterparts. These data then suggest that adequate activation of both neural regions, SMA complex and PMd, is important for skill acquisition but despite being neighboring neural sites within BA6 the specific contribution of each site to the evolution of novel motor memories is quite distinct.