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Randomized Controlled Trial
. 2018 Apr-May;32(4-5):295-308.
doi: 10.1177/1545968318769164. Epub 2018 Apr 22.

Transcranial Direct Current Stimulation Enhances Motor Skill Learning but Not Generalization in Chronic Stroke

Affiliations
Randomized Controlled Trial

Transcranial Direct Current Stimulation Enhances Motor Skill Learning but Not Generalization in Chronic Stroke

Manuela Hamoudi et al. Neurorehabil Neural Repair. 2018 Apr-May.

Abstract

Background: Motor training alone or combined with transcranial direct current stimulation (tDCS) positioned over the motor cortex (M1) improves motor function in chronic stroke. Currently, understanding of how tDCS influences the process of motor skill learning after stroke is lacking.

Objective: To assess the effects of tDCS on the stages of motor skill learning and on generalization to untrained motor function.

Methods: In this randomized, sham-controlled, blinded study of 56 mildly impaired chronic stroke patients, tDCS (anode over the ipsilesional M1 and cathode on the contralesional forehead) was applied during 5 days of training on an unfamiliar, challenging fine motor skill task (sequential visual isometric pinch force task). We assessed online and offline learning during the training period and retention over the following 4 months. We additionally assessed the generalization to untrained tasks.

Results: With training alone (sham tDCS group), patients acquired a novel motor skill. This skill improved online, remained stable during the offline periods and was largely retained at follow-up. When tDCS was added to training (real tDCS group), motor skill significantly increased relative to sham, mostly in the online stage. Long-term retention was not affected by tDCS. Training effects generalized to untrained tasks, but those performance gains were not enhanced further by tDCS.

Conclusions: Training of an unfamiliar skill task represents a strategy to improve fine motor function in chronic stroke. tDCS augments motor skill learning, but its additive effect is restricted to the trained skill.

Keywords: brain injury; motor cortex; neuroplasticity; neurotrophins; noninvasive brain stimulation.

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Conflict of interest statement

The authors declare that there is no conflict of interest.

Figures

Figure 1
Figure 1. Study design
A, Patients trained for five consecutive days and were then subjected to 5 follow-up visits. During training they received real (40µA/cm2) or sham tDCS for 20 minutes per day with the anode targeting the primary motor cortex (M1) of the affected hemisphere. A training session consisted of 5 blocks of 20 trials of the sequential visual isometric pinch force task (SVIPT). At the beginning of day 1, the end of day 5 and all follow-ups the Jebsen Taylor hand function test (JTT) and the Grooved Pegboard test (GPT) were also performed. The no-training/no-tDCS group performed only the generalization tasks without receiving training or tDCS. B, CONSORT flow diagram of the study. C, The summarized binary lesion overlay for each study group is shown, blue=sham tDCS, red=real tDCS, green= no-training/no-tDCS group. Color key (dark to bright) ranges from 1 to 6 patients. The majority of patients had an infarction mainly located along the pyramidal tract and particularly in the internal capsule. Stimulation groups were well matched for their lesion anatomy and volume. VLSM revealed no group differences.
Figure 2
Figure 2. Measures of motor skill learning during training and follow-up period
A, Skill learning curve over five training days (five blocks per day) and the follow-up period. The patients receiving real tDCS (red dots) showed significantly greater improvement of motor skill and outperform sham stimulated patients (blue dots) at all time points. The majority of acquired skill was retained after the end of training. At day 113, the real tDCS group showed greater remaining skill compared to sham tDCS. B, Higher total learning in the real tDCS group (red) was predominantly due to greater online (within session) learning. C, The proportion of skill retained at day 113 was similar in the two stimulation conditions, suggesting that real tDCS did not per se affect long-term retention. Significance: *p<0.05. All data are shown as group mean ± SEM.
Figure 3
Figure 3. Measures of generalization after SVIPT training and during the follow-up period
A, Grooved Pegboard test, paretic hand; Improvement measured by absolute change in accuracy relative to day 1; Both training groups show increased accuracy (a reduction in no. of errors is indicated by positive values), on all days, while the no-training/no-tDCS group shows less accuracy (i.e., trading accuracy for higher speed). The MANOVA revealed a significant effect of training compared to no training/no-tDCS, but no additional effect of real tDCS compared to sham tDCS. B, Grooved Pegboard test, paretic hand, Percent improvement in speed (total time to complete the test) relative to day 1. Both training groups and the no-training/no-tDCS group showed improvements in total time. There was no significant difference between trained and untrained patients or between sham and real tDCS stimulated patients. C, Jebsen Taylor test, paretic hand; Percent improvement in speed (total time to complete the full test) relative to day 1. The MANOVA revealed a significant effect of training compared to no- training/no-tDCS, independent of tDCS stimulation type. The no-training/no-tDCS group showed only minor improvements (repetition effects). D, The GPT accuracy change is plotted against the GPT speed change. Data from all time points were used for illustration of the lacking relationship between the two variables in the no-training/no-tDCS group, compared to the strong positive relationship in the two trained groups (indicating improvements in both variables). The real tDCS group shows the greatest improvements in accuracy for a given speed change. The ellipses indicate the 90% confidence interval per group, the lines represents the mean centered linear regression line per group. Significance: *p<0.05. All data except for panel C (single subject data) are shown as group mean ± SEM.
Figure 4
Figure 4. Analysis of cumulative learning probability and correlation of learning subcomponents
A, Compared to sham tDCS (blue), patients reached a minimum skill gain of 1 unit earlier, when training was combined with real tDCS (red). A skill gain of 1 unit represents the average level of skill reached by the sham tDCS group and was extrapolated from a predictive model. Note that the sham tDCS group is censored, i.e. the Kaplan Meier interval for the time to event (100% of patients reaching the criterion) is not known for this particular group. This happened because few patients did not reach a skill gain of 1 within the 25 training blocks. B, There was a strong negative correlation between online and offline learning during training across groups. Real tDCS (red circles and line) shifted the set point for occurrence of offline skill loss towards higher online learning compared to sham (blue squares and line).
Figure 5
Figure 5. Learning curves for the five training days and the follow-up period for movement time, error rate and movement smoothness
A, Movement time: both groups showed improvements in movement time; real tDCS significantly shortened movement time across sessions compared to sham tDCS; B, Error rate: both groups reduced the error rate over 5 days; no significant differences were found between real and sham tDCS; C, Movement smoothness: Real tDCS significantly enhanced movement smoothness across sessions compared to sham tDCS. All data are shown as group mean ± SEM.

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