Bihemispheric Transcranial Direct Current Stimulation Enhances Effector-Independent Representations of Motor Synergy and Sequence Learning

Abstract

Complex manual tasks-everything from buttoning up a shirt to playing the piano-fundamentally involve two components: (1) generating specific patterns of muscle activity (here, termed "synergies"); and (2) stringing these into purposeful sequences. Although transcranial direct current stimulation (tDCS) of the primary motor cortex (M1) has been found to increase the learning of motor sequences, it is unknown whether it can similarly facilitate motor synergy learning. Here, we determined the effects of tDCS on the learning of motor synergies using a novel hand configuration task that required the production of difficult muscular activation patterns. Bihemispheric tDCS was applied to M1 of healthy, right-handed human participants during 4 d of repetitive left-hand configuration training in a double-blind design. tDCS augmented synergy learning, leading subsequently to faster and more synchronized execution. This effect persisted for at least 4 weeks after training. Qualitatively similar tDCS-associated improvements occurred during training of finger sequences in a separate subject cohort. We additionally determined whether tDCS only improved the acquisition of motor memories for specific synergies/sequences or whether it also facilitated more general parts of the motor representations, which could be transferred to novel movements. Critically, we observed that tDCS effects generalized to untrained hand configurations and untrained finger sequences (i.e., were nonspecific), as well as to the untrained hand (i.e., were effector-independent). Hence, bihemispheric tDCS may be a promising adjunct to neurorehabilitative training regimes, in which broad transfer to everyday tasks is highly desirable.

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

“…-pressing a keyboard key or button), while the required sequence of actions are typically complex in structure (between 8-15 items in length with controls on smaller intra-sequence patterns). Alternatively, the SVIPT requires execution of a precision pinch force action that is more difficult to elicit than a key-press (Waters-Metenier, Husain, Wiestler, & Diedrichsen, 2014). Thus, there is a greater emphasis placed upon accurate performance of the unit action within an explicit sequence context in the SVIPT than most variants of SFTTs.…”

“…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).…”

“…In addition to task-specific learning effects, these findings suggest that different learning processes interact with tDCS stimulation in non-additive ways as task complexity increases. Waters-Metenier et al (2014) looked at task-specific effects of bilateral M1 stimulation, in this case on the learning novel hand movement synergy patterns and finger tapping sequences (Waters-Metenier et al, 2014). In this case, tDCS improved both synergy and sequence learning with long-term retention of the effects persisting for at least 4 weeks following training.…”

“…The authors conclude that the effects of anodal tDCS over M1 on sequential motor learning may depend on learning stages (Dayan & Cohen, 2011) and be to some extent task-or montage-specific and that multiple tDCS sessions present advantages over single session applications on both finger tapping and SVIPT tasks. Similarly, the effects on long-term retention might be task specific with different retention effects reported in the finger tapping versus SVIPT tasks Reis et al, 2009;Saucedo-Marquez et al, 2013;Waters-Metenier et al, 2014). Of note, the relatively small number of studies fitting the inclusion criteria is a primary example of the challenges faced when attempting to perform quantitative reviews of tDCS effects on motor learning (Antal, Keeser, Priori, Padberg, & Nitsche, 2015;Nitsche, Bikson, & Bestmann, 2015).…”

“…Similarly, the issue of generalization is of clear relevance to rehabilitation and remains a major challenge. In addition to investigating the efficacy of tDCS in enhancing specific quantitative features of skill learning, improving our understanding of the effects of tDCS on generalization of learning across different skills will also be an important scientific endeavor (Waters-Metenier et al, 2014).…”