Improving consolidation by applying anodal transcranial direct current stimulation at primary motor cortex during repetitive practice
Introduction
Competent motor behavior resulting from skill acquisition is the foundation of most human daily activity. Acquisition of motor skills and the associated neuroplastic changes that occur are dependent on exposure to extensive practice. Practice however should be organized to optimize its effectiveness (Wright et al., 2014). In this regard, interleaved practice has been reported to foster superior long-term retention compared to repetitive practice when multiple novel motor skill are being acquired simultaneously (Shea and Morgan, 1979, Lage et al., 2015, Wright et al., 2016). Interleaved practice is characterized by a frequent change in task demands for the learner across practice trials by being required to execute a different motor skill on each trial. Conversely, repetitive practice involves the repeated execution of the same motor task for a pre-determined number of trials before facing practice of other to-be-learned motor tasks. The retention benefit from interleaved practice is manifest as stable performance during the initial wake hours after practice with further improvement overnight. In contrast, following repetitive practice, significant forgetting occurs immediately after practice is complete with no gain in performance overnight (Wright et al., 2016, Kim and Wright, 2020). These data suggest that interleaved practice fosters effective post-practice consolidation, a process that has been described as critical to the establishment of a robust motor memory (McGaugh, 2000).
Muellbacher et al. (2002) proposed that M1 plays a crucial role in consolidation of motor skills based on the finding that performance improvement of a relatively simple pinch-force task is attenuated by administering 1-Hz repetitive transcranial magnetic stimulation (rTMS) at M1 for 15-min immediately after practice, but not when applied to occipital or dorsolateral prefrontal regions. The interference from rTMS is eliminated if applied approximately 6-hr after practice suggesting early consolidation of new learning is impacted. Modulation of post-practice consolidation can also be mediated via the administration of transcranial direct current stimulation (tDCS) (Buch et al., 2017, Stagg et al., 2018). Importantly, for the present work, application of anodal tDCS at M1 during practice has been shown to facilitate human motor learning by influencing consolidation. Specifically, Reis et al. (2009) had individuals practice a sequential force-pinch skill over the course of five days in the presence of either anodal or sham tDCS at M1. A significant benefit from stimulation during practice was manifest offline. That is, performance enhancement from the application of anodal tDCS at M1 emerged during the intervals between practice sessions and remained for some time after training was over. These data were further elaborated by Reis et al. (2015) noting that similar offline gain is observed following the passage of sufficient time in the absence of sleep (~15-min to 3-h following stimulation).
Since the efficacy of post-practice consolidation has been linked to the long-term retention benefits of interleaved practice, it is possible that the relative greater recruitment of M1 during interleaved practice accounts, at least in part, for the effectiveness of this practice format compared to repetitive practice. Indeed, data are available revealing differential involvement of M1 during interleaved and repetitive practice. Specifically, (a) activity at M1 during response preparation is greater during interleaved practice and correlates with off-line learning for individuals exposed to this schedule of practice (Cross et al., 2007, Wymbs and Grafton, 2009), (b) M1 excitability at the time of retention is greater following interleaved practice and the additional excitability is related to the performance differences between repetitive & interleaved practice at the time of test (Lin et al., 2011), (c) applying supra-threshold single pulse TMS at M1 after interleaved practice trials attenuates the offline gain commonly observed following this type of practice (Lin et al., 2008, Lin et al., 2010), and (d) stronger task-related functional connectivity later in training between the right dorsal premotor area and M1 during interleaved practice is associated with the subsequent retention advantage exhibited by interleaved practice participants (Lin et al., 2013). On the basis of these data, the present study was designed to examine if modifying activity at M1 during repetitive practice, via the application anodal tDCS, can change online and offline performance for individuals that encounter this type of training.
To accomplish this goal, participants were assigned to one of three experimental groups that included two control conditions (Interleaved-Sham, Repetitive-Sham) that performed in the absence of real stimulation and a novel third group that involved the administration of anodal stimulation at M1 throughout repetitive practice (Repetitive-Anodal). In all conditions, motor sequence performance was evaluated during practice (i.e., online) as well as during delayed tests (i.e., offline) using total response time (TT) as the primary dependent variable (Kim et al., 2018). Individuals in the sham conditions were expected to mimic the outcomes commonly observed in previous studies addressing the influence of interleaved and repetitive practice for learning. Specifically, the repetitive practice participants were expected to reveal significant forgetting following the conclusion of practice. In contrast, interleaved practice was expected to support initial stable performance immediately after practice and further performance enhancement following overnight sleep (Shea and Morgan, 1979, Lage et al., 2015, Wright et al., 2016). Motor performance, following practice that was combined with anodal tDCS, was anticipated to improve offline gain resulting in the individuals assigned to Repetitive-Anodal outperforming their Repetitive-Sham counterparts during delayed test. The inclusion of tests administered 6-h as well as 24-h after practice offered the opportunity to assess if any offline benefits from anodal stimulation during repetitive practice are restricted to either early time-dependent and/or sleep-related improvements.
Section snippets
Participants
Participants were right-handed undergraduate students (N = 54, Males: 23, Females: 31) that received course credit for their participation. Individuals had no prior experience with the experimental tasks and were unaware of the specific purpose of the study. All individuals that participated in this study had no history of epilepsy, any known neurological disorder, no psychiatric history, were medication free during the previous 14-days prior to participation, had not used alcohol within
Baseline DSP task performance
Fig. 3 reveals that the performance of the discrete sequence production tasks (DSP) for the individuals assigned to each experimental group was similar prior to training (Repetitive-Sham, M = 3023 ms, SEM = 74 ms; Interleaved-Sham, M = 2947 ms, SEM = 86 ms; Repetitive-Anodal, M = 2983 ms, SEM = 93 ms).3 This was confirmed by the 3 (Group: Repetitive-Sham, Interleaved-Sham, Repetitive-Anodal) between-subject analysis of variance (ANOVA) for TT observed during
Revisiting the impact of repetitive and interleaved practice for online and offline gains
Repetitive practice has been reported to be very effective for inducing rapid online improvements but remains susceptible to these gains been lost rapidly after practice. In contrast, interleaved practice, while associated with slower gains online, has been shown to result in superior retention performance (Shea and Morgan, 1979, Wright et al., 2016). The present experiment extend previous examinations of practice organization by including multiple test periods during the first 24-h offering an
Conclusions and limitations
The present findings are consistent with the claim that increased recruitment of M1 during interleaved practice plays is a critical role in the retention advantage this practice format has over repetitive practice (Cross et al., 2007, Lin et al., 2008, Lin et al., 2010, Lin et al., 2011, Lin et al., 2013, Wymbs and Grafton, 2009). Supplementing repetitive practice with anodal tDCS at M1 throughout training resulted in offline gains congruent with those observed following interleaved practice.
Data availability statement
The datasets generated for this study are available upon reasonable request from corresponding author.
Ethics statement
The studies involving human participants were reviewed and approved by the Institutional Review Board at the Texas A&M University. The participants provided their written informed consent to participate in this study.
Author contributions
TK, DW designed the study and experimental protocol. TK and HK performed the experiment, collected the data, and analysed the data. TK drafted the manuscript. All authors contributed to critical writing and revision of the manuscript.
Funding
The author(s) received partial funding for this project from the Omar Smith Endowed Chair in Kinesiology awarded to the third author (DW).
CRediT authorship contribution statement
Taewon Kim: Writing - original draft, Writing - review & editing, Conceptualization, Investigation, Formal analysis, Project administration. Hakjoo Kim: Writing - review & editing, Investigation, Formal analysis. David L. Wright: Writing - review & editing, Conceptualization, Project administration, Funding acquisition.
Declaration of Competing Interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
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