Transcranial Direct Current Stimulation (tDCS)/Transcranial Alternating Current Stimulation (tACS)Original ArticleEffects of Different Electrical Brain Stimulation Protocols on Subcomponents of Motor Skill Learning
Introduction
A substantial portion of our lives is spent learning new motor skills: from walking to writing, driving and sports. Motor skills are the primary mechanism for interaction with the world around us; hence, defective motor skills resulting from neurological diseases are a severe impairment. Noninvasive electrical brain stimulation (NEBS) applied transcranially to the motor cortex (M1) has been shown to improve motor skill learning in healthy individuals [1], [2] and in chronic stroke patients [3], [4], [5]. Transcranial direct current stimulation (tDCS) with an anode over M1 and a cathode over the contralateral supraorbital area, in combination with motor training resulted in greater skill gains compared to sham in healthy subjects. Using tasks of different complexity, experiments have shown both within session (online) improvements in a single-day [6], [7], as well as between session (offline) improvements observed with multi-session training [8], [9]. In an attempt to maximize stimulation benefits, recent studies utilized a bilateral M1 montage, with an anode over the M1 contralateral and a cathode ipsilateral to the training hand. The basic idea of this approach is the modulation of interhemispheric inhibition [10], [11], [12], that is strengthening the facilitatory effect on one M1 with anodal tDCS, while reducing the inhibitory influence of the other M1 by cathodal tDCS [12], [13].
While tDCS uses a direct current flowing in one direction necessitating an anode and cathode with potentially different local effects, transcranial random noise stimulation (tRNS) uses an alternating current with a randomly changing frequency and current direction, removing anode/cathode-specific effects. High frequency tRNS (100–640 Hz) applied to M1 has also been shown to facilitate implicit motor sequence learning [14]. Both anodal tDCS and tRNS enhance M1 excitability [14], [15], [16], although it is likely there are differences in the mechanism of action of a constant current versus changing currents applied to the cortex [17], [18]. It has been suggested that the concept of stochastic resonance may apply to all forms of NEBS: stimulation-induced noise introduced to a neuronal system may provide a signal processing benefit in the brain by altering the signal-to-noise ratio [19], [20]. While synchronization with task–relevant activity may play a particular role for tRNS, additional homeostatic mechanisms induced by a constant noise input may apply for tDCS [19], [21]. Despite the huge amount of separate investigations of tDCS and tRNS effects assessed in a single session, there are only two direct comparisons between these stimulation types: For visuomotor learning, neither tRNS nor anodal tDCS applied to M1 combined with a brief single training session improved learning relative to sham stimulation [22]. On an orientation discrimination task Pirulli et al. [23] found the effect of stimulation type applied to the visual cortex varied depending on the timing of stimulation, with tRNS more effective if applied during practice, whereas tDCS induced better discrimination when applied before practice. However, these results directly contrast with results from the motor learning domain, where anodal tDCS applied to M1 before learning a serial reaction time task was found to inhibit or leave unaffected subsequent learning [7], [24], showing NEBS effects are current type, site and task specific.
Given that these studies probed aspects of learning in a single session and one was not directly related to motor learning, it is currently unknown whether tDCS and tRNS would exert distinct effects onto specific subcomponents of motor skill learning, i.e. within session (online) improvements or between session (offline) effects, only assessable when training for more than one session. Disentangling how different forms of NEBS interact with the stages of the learning process is of great value both for understanding the mechanisms of motor skill learning as well as to maximize clinical benefits of NEBS. Here, we directly contrast the effects of tDCS and tRNS on repeated motor learning sessions in an exploratory study to test the efficacy of these different stimulation types.
Section snippets
Methods and materials
This study was in accordance with the Declaration of Helsinki amended by the 59th WMA General Assembly, Seoul, October 2008 and was approved by the local Ethics Committee of the University of Freiburg.
Demographics
91 healthy German-speaking participants took part in the experiment. One participant was excluded from analysis (including demographics) due to an error in stimulation parameters (tDCS:M1-SO group). No further participants were excluded. All participants tolerated the stimulation well. 8 subjects out of 90 reported mild headache after stimulation on day 1 only; this is likely to be caused by TMS rather than NEBS, as they did not reoccur on day 2 (no TMS), and 2 of these 8 were in the sham
Discussion
Motor cortex electrical stimulation accelerates prolonged motor skill learning with different tDCS montages as well as with tRNS. Enhancement of overall learning is mainly driven by online (within session) improvements. No significant differences are found between tDCS and tRNS. Non-M1 stimulation does not significantly enhance motor skill learning, confirming the key role of the primary motor cortex in motor skill learning and region specific effects of stimulation.
Conclusion
NEBS applied to M1 enhances motor skill learning over multiple sessions; on the tracing task this appears to be due to strengthening of skill acquisition within session when training the nondominant hand. Strikingly, the direct comparison of different stimulation protocols revealed no clear advantage of a particular stimulation type or montage with regard to overall learning. Hence, as long as M1 is targeted, current type and electrical field distribution within the brain seem to have a
Acknowledgments
Thanks to Mark Nieuwenstein for comments on an earlier version of the manuscript and to Michel Rijntjes for helpful comments on the task design.
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2022, Entertainment ComputingCitation Excerpt :TDCS was applied immediately prior to the motor task and participants had to perform the exoskeleton-based training for the left arm. Another task that included upper limb, non-dominant hand, in combination with tDCS, was presented in [35]. M1 region was stimulated for 20 min and in the end, there was a significantly increased motor skill learning compared to the sham.
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2021, Behavioural Brain ResearchCitation Excerpt :Therefore, performing tRNS with motor training may improve the responsiveness of the M1 and enhance the effect of motor training. In fact, several previous studies have shown that tRNS performed during motor training improved motor function in an, a visuomotor tracking task, and a force control task compared to a sham stimulation [19,26]. In summary, previous studies have indicated that tRNS to the M1 increases corticospinal excitability, and that tRNS alone or during motor training improves motor function compared to motor training alone.
Improving consolidation by applying anodal transcranial direct current stimulation at primary motor cortex during repetitive practice
2021, Neurobiology of Learning and MemoryCitation Excerpt :This was true for the performance change between the baseline and immediate post-training tests in the absence of stimulation as well as during ongoing performance in the presence of anodal stimulation throughout repetitive practice. This outcome was not entirely surprising as evidence of online improvement from anodal tDCS at M1 being combined with physical practice is mixed with some studies revealing enhancement (Nitsche et al., 2003; Reis et al., 2009; Stagg and Nitsche, 2011; Kantak et al., 2012; Cuypers et al., 2013; Karok and Witney, 2013; Saucedo Marquez et al., 2013; Prichard et al., 2014; Waters-Metenier et al., 2014; Ciechanski and Kirton, 2017), whereas others failed to reveal any benefit (Amadi et al., 2015; Reis et al., 2015; Ammann et al., 2016). It’s worth noting that the present work focused on the administration of anodal tDCS concurrent with the acquisition of multiple novel skills as opposed to just a single skill as was the case in most previous studies.
Financial disclosures: All authors of this manuscript report no biomedical financial interests or potential conflicts of interest.
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These authors contributed equally.