Elsevier

Brain Stimulation

Volume 7, Issue 4, July–August 2014, Pages 532-540
Brain Stimulation

Transcranial Direct Current Stimulation (tDCS)/Transcranial Alternating Current Stimulation (tACS)
Original Article
Effects of Different Electrical Brain Stimulation Protocols on Subcomponents of Motor Skill Learning

https://doi.org/10.1016/j.brs.2014.04.005Get rights and content

Abstract

Background

Noninvasive electrical brain stimulation (NEBS) with transcranial direct current (tDCS) or random noise stimulation (tRNS) applied to the primary motor cortex (M1) can augment motor learning.

Objective

We tested whether different types of stimulation alter particular aspects of learning a tracing task over three consecutive days, namely skill acquisition (online/within session effects) or consolidation (offline/between session effects).

Methods

Motor training on a tracing task over three consecutive days was combined with different types and montages of stimulation (tDCS, tRNS).

Results

Unilateral M1 stimulation using tRNS as well as unilateral and bilateral M1 tDCS all enhanced motor skill learning compared to sham stimulation. In all groups, this appeared to be driven by online effects without an additional offline effect. Unilateral tDCS resulted in large skill gains immediately following the onset of stimulation, while tRNS exerted more gradual effects. Control stimulation of the right temporal lobe did not enhance skill learning relative to sham.

Conclusions

The mechanisms of action of tDCS and tRNS are likely different. Hence, the time course of skill improvement within sessions could point to specific and temporally distinct interactions with the physiological process of motor skill learning. Exploring the parameters of NEBS on different tasks and in patients with brain injury will allow us to maximize the benefits of NEBS for neurorehabilitation.

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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    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.

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