Elsevier

Neuropsychologia

Volume 94, 8 January 2017, Pages 84-95
Neuropsychologia

Task-specificity of unilateral anodal and dual-M1 tDCS effects on motor learning

https://doi.org/10.1016/j.neuropsychologia.2016.12.002Get rights and content

Highlights

  • Participants acquire proficiency in three separate motor tasks.

  • Motor learning is maintained over 28 days.

  • Anodal and dual-M1 tDCS enhance and sustain motor learning more than sham.

  • The evolution of tDCS effects is specific to electrode montage and task demands.

Abstract

Task-specific effects of transcranial direct current stimulation (tDCS) on motor learning were investigated in 30 healthy participants. In a sham-controlled, mixed design, participants trained on 3 different motor tasks (Purdue Pegboard Test, Visuomotor Grip Force Tracking Task and Visuomotor Wrist Rotation Speed Control Task) over 3 consecutive days while receiving either unilateral anodal over the right primary motor cortex (M1), dual-M1 or sham stimulation. Retention sessions were administered 7 and 28 days after the end of training. In the Purdue Pegboard Test, both anodal and dual-M1 stimulation reduced average completion time approximately equally, an improvement driven by online learning effects and maintained for about 1 week. The Visuomotor Grip Force Tracking Task and the Visuomotor Wrist Rotation Speed Control Task were associated with an advantage of dual-M1 tDCS in consolidation processes both between training sessions and when testing at long-term retention; both were maintained for at least 1 month. This study demonstrates that M1-tDCS enhances and sustains motor learning with different electrode montages. Stimulation-induced effects emerged at different learning phases across the tasks, which strongly suggests that the influence of tDCS on motor learning is dynamic with respect to the functional recruitment of the distributed motor system at the time of stimulation. Divergent findings regarding M1-tDCS effects on motor learning may partially be ascribed to task-specific consequences and the effects of offline consolidation.

Introduction

The performance of nearly any voluntary motor task can improve with repetition and practice. Motor skill learning occurs not only during practice (online gains), but also between practice sessions (offline gains) (Müller et al., 2002, Robertson et al., 2005). Skill changes that occur offline are stabilised and enhanced through the process of consolidation, which can occur shortly after the end of training (Muellbacher et al., 2002). Following consolidation, motor skills can be maintained over longer periods of time and become increasingly automatic (retention). Rate and magnitude of skill acquisition are also highly task-specific, depending on complexity and nature of the task (e.g. Carey et al., 2005; Kuriyama et al., 2004).

In recent years, non-invasive neurostimulation studies have enhanced our comprehension of how brain areas are recruited across different learning phases and task demands. The primary motor cortex (M1) is known to modulate motor output and encode movement parameters, but there is increasing evidence to suggest that M1 is more acutely involved in the acquisition of motor skills (Galea et al., 2011, Matsuzaka et al., 2007, Ungerleider et al., 2002). It is well documented that transcranial direct current stimulation (tDCS), with the anode over the M1 and the cathode over the contralateral supraorbital area, in combination with motor training results in greater motor performance gains compared with no stimulation. This has been reported across a range of motor tasks, measuring movement speed, accuracy and/or a change in movement kinematics. Some are broad clinical tests of hand function such as the Jebsen-Taylor Hand Function Test (Boggio et al., 2006, Williams et al., 2010), but most isolate a specific motor skill such as the serial reaction time task (SRTT) (Kang and Paik, 2011, Kantak et al., 2012, Nitsche et al., 2003), finger-sequencing tasks (Stagg et al., 2011, Vines et al., 2008b), ballistic thumb movements (Bortoletto et al., 2015, Galea and Celnik, 2009), maximal pinch force (Tanaka et al., 2009) and the sequential visual isometric pinch task (SVIPT) (Reis et al., 2013, Reis et al., 2009, Schambra et al., 2011).

These studies among others (e.g. Karni et al., 1995) support a prominent role of M1 in fast online performance gains. The aim of the present study was to stimulate M1 using tDCS over multiple motor learning sessions and different motor tasks. Only a few tDCS studies have probed the involvement of M1 in post-session motor learning processes. In one such study, Kantak et al. (2012) found that anodal tDCS applied to M1 during a SRTT improved online performance of a practised sequence and offline skill maintenance when tested the following day. In contrast, other studies found motor learning mediated by offline gains only. Reis et al. (2009) applied anodal tDCS during the SVIPT over the course of 5 days and participants showed significant learning between sessions, but not during sessions. Improvements were maintained at long-term retention 3 months later. These divergent findings may be explained by differences in the motor tasks applied and/or differences in training duration.

Recent evidence indicates that anodal tDCS to M1 may influence motor learning processes in a task-specific manner. Namely, Saucedo Marquez et al. (2013) compared the effects of tDCS on the acquisition of the finger-sequencing task and the adapted SVIPT over 3 consecutive days. While online and offline gains were reported for the finger-sequencing task, the SVIPT showed a learning effect only at retention, 1 week after the last training session. It was suggested that anodal tDCS necessarily has a stronger influence on neuronal firing rates in the area under the electrodes, which are functionally more relevant to some task demands than others. Since active stimulation of both motor cortices simultaneously (dual-M1 tDCS) has been associated with an increase in functional connectivity from intracortical areas to areas under the anode (Lindenberg et al., 2013, Sehm et al., 2013), this could have advantageous effects on tasks implicating more remote areas.

Dual-M1 tDCS has been under investigation as a powerful strategy to modulate motor performance (Vines et al., 2008a, Karok and Witney, 2013, Koyama et al., 2015, Waters-Metenier et al., 2014). Dual-M1 tDCS, with the anode over M1 and the cathode of the contralateral M1, is thought to induce up- and down-regulation of respective M1 cortical excitability (Karok and Witney, 2013, Mordillo Mateos et al., 2012, Williams et al., 2010). This has been shown to enhance motor learning in healthy subjects (e.g. Vines et al., 2008a) and to facilitate motor performance in stroke patients (e.g. Lindenberg et al., 2010). The exact mechanisms underlying dual-M1 stimulation effects on motor system activity are still incompletely understood. However, it appears to be more than a mere add-on of the anodal and cathodal currents. Resting-state and task-related functional magnetic resonance imaging (fMRI) studies examining the influence of tDCS on network activity found a decrease in interhemispheric functional projections in the conventional anodal and the dual-M1 condition, with only dual-M1 tDCS associated with increases in functional intracortical projections (Lindenberg et al., 2013, Sehm et al., 2013). Therefore, the currents may spread and activate the larger network, which suggests that dual-M1 stimulation effects could be manifested differently across different motor tasks.

The present study aimed to investigate task-specificity effects of unilateral anodal and dual-M1 electrode montages across various motor learning phases. In a sham-controlled, mixed-design, participants received motor training on three different tasks over three consecutive days while receiving either unilateral anodal, dual-M1 or sham tDCS. Two retention sessions, 7 days after the end of training and 28 days after the end of training, assessed how any performance changes are maintained over time. Participants trained on the Purdue Pegboard Test (PPT), a Visuomotor Grip Force Tracking Task and a Visuomotor Wrist Rotation Speed Control Task.

Based on previous research, we predicted that active tDCS would generally show enhanced motor learning compared to sham. We expected fast online gains in the PPT with marginal differences between electrode montages (Kidgell et al., 2013). We hypothesized slow and sustained motor learning effects with the Visuomotor Grip Force Tracking Task and the Visuomotor Wrist Rotation Speed Control Task, likely driven by offline gains (Reis et al., 2009, Saucedo Marquez et al., 2013, Waters-Metenier et al., 2014). Since dual-M1 tDCS is associated with different patterns of activation when compared with anodal tDCS (Lindenberg et al., 2013, Sehm et al., 2013), we expected different rates of skill acquisition in these tasks following multiple stimulation sessions.

Section snippets

Participants

Thirty healthy young adults (15 females; mean age 27.0 years±5.4 SD) participated in this study. All participants were right-handed, as determined by the Edinburgh Handedness Inventory (Oldfield, 1971) and were screened to be medically and neurologically healthy by a medical history questionnaire. The experimental protocol was performed in accordance with the revised Declaration of Helsinki and approved by the Faculty of Health Sciences Research Ethics Committee, Trinity College Dublin, Ireland.

Results

All participants tolerated the experiment well with no adverse effects reported from stimulation. There were no group differences in self-reported level of fatigue (F8,76=1.33, p>0.05), sleep (F8,76=0.64, p>0.05) or attention (F8,76=1.62, p>0.05). The sensation from tDCS was generally rated as more painful in the sham group (average 2.1±1.3 out of 7 painful) compared to the anodal (1.23±0.5) and the dual-M1 group (1.57±1.0), but not significantly so (F2,27 =3.01, p>0.05). In keeping with this,

Discussion

The findings from the present study indicate that M1-tDCS induces lasting motor learning with different electrode montages. While each of the three experimental tasks were associated with overall online learning within the first session, stimulation effects were found at or after the second training day only, most notably following dual-M1 stimulation. These tDCS-induced effects appear to emerge at different learning phases, which suggests that they are adaptive to the functional requirements

Funding sources

Support for this work was provided by the Irish Research Council's EMBARK Initiative (409.G30568).

Conflict of interest

The authors declare that they have no conflict of interest.

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      Based on some studies in this review, which verified the bihemispheric tDCS effect on bimanual tasks (Pixa et al., 2017a, 2017b), the application of stimulation before, and not during the motor task practice may have compromised the tDCS effect in the study by Gao et al. (2021). Flix-Diez et al. (2021), unlike four other studies (Ciechanski and Kirton, 2016; Cole, Dukelow, et al., 2018; Cole, Giuffre, et al., 2018; Karok et al., 2017), did not show an anodal M1 tDCS effect during the PPT task learning. When comparing the characteristics of this study with the study by Karok et al. (2017), who also analyzed the PTT task in adults, it appears that the latter study used higher electrical current intensity (1.5 mA), shorter time stimulation (15 min), fewer practice sessions (3 sessions), and the non-preferred member during learning.

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