When examining the relationship between off-line motor learning and performance on the executive function tests for the participants with stroke, there was a significant positive correlation between the off-line motor learning score and performance on the TMT D-KEFS (r = 0.652, P = 0.005) (Figure 1) which indicates that better performance on the TMT is associated with a higher magnitude of off-line motor learning (a lower score on the TMT indicates that less time was required to complete the test and a more negative off-line learning score indicates a larger magnitude of improvement on the tracking task from practice to the retention testing). There were nonsignificant negligible or weak correlations between the off-line motor learning score and performance on the Stroop Test, VFT, and d2 test (Table 3). For the control group, there were no significant correlations between off-line motor learning and performance on the executive function tests (Table 3). The PSG variables of interest showed no significant associations with performance on any of the 4 executive function tests (Table 4).
In the regression analysis, the 4 executive function tests were used as the predictor variables for off-line motor learning score for the stroke group. The overall model was significant (P = 0.041), explaining 54% of the variance in the off-line learning score (R2 = 0.539) (Table 5). The only executive function test that had a significant contribution in the model was the TMT D-KEFS (P = 0.013). Stepwise linear regression showed that the TMT D-KEFS was the only variable that predicts off-line motor learning (P = 0.005) and explained 43% (R2 = 0.425) of the variance in the off-line motor learning score. The model remained significant after controlling for condition 4 (motor speed) of the TMT D-KEFS (P = 0.008). We further considered the 2 individuals who demonstrated the largest magnitude of change on the tracking task (−7.44° and −5.77°). Notably, the person with the largest magnitude was the youngest individual in the sample (41 years of age) and the other individual was 52 years of age (which is below the mean of the sample). The stepwise linear regression was repeated with age added as a control. The TMT D-KEFS remained a significant predictor of off-line motor learning (P = 0.034) and explained 40.3% (R2 = 0.403) of the variance in off-line motor learning.
This study is the first to demonstrate that better performance on the TMT D-KEFS is associated with increased magnitude of off-line motor skill learning in individuals with chronic stroke. Furthermore, performance on the TMT D-KEFS was shown to be a significant independent predictor of off-line motor learning in individuals with chronic stroke even after controlling for age. This study advances the body of knowledge of what factors mediate off-line motor learning in people with chronic stroke.
An interesting finding in this study is that performance on the TMT D-KEFS was not associated with any of the sleep parameters or self-reported sleep quality. This lack of association is in contrast to the results from Siccoli et al,18 who found increased time spent in N3, and REM sleep was associated with better cognitive function (including executive function) in both the subacute and chronic stages poststroke. The discrepancy in findings may be due to a difference in calculation of the reported outcomes. Another reason why no association was found between performance on the TMT D-KEFS and sleep parameters or self-reported sleep quality in our study may be that participants with stroke in our study sample have on average good sleep quality (the mean Pittsburg Sleep Quality Index score for the stroke group is <5; a score >5 indicates poor sleep quality31), and none of the participants with stroke included in the study had untreated sleep disorders. Therefore, in the absence of poor sleep quality or sleep disorders, detecting an association between executive function and the sleep variables may be difficult. Another possibility is that the performance on the TMT D-KEFS may be associated with sleep parameters at certain parts of the night (ie, at the first half of the night in which N3 is predominant or the second half of the night in which N2 is predominant34), which was not analyzed for our study.
Because this study did not include a group that had a testing schedule to allow for assessing the association between executive function performance and motor learning independent of sleep, it is possible that the performance on the TMT D-KEFS might be associated with improved execution of the motor task whether the period between testing and retesting included sleep or being awake. However, we believe this unlikely as prior studies found that sleep enhanced off-line motor learning in individuals with chronic stroke, but a similar period of being awake did not.1,2 Therefore, sleep appears necessary to enhance learning off-line (with no further practice) in people with stroke.
A limitation of this study is the small sample size, which might affect the interpretation of the results. In addition, the findings of this study can be generalized to only those individuals with stroke with minimal to no cognitive impairments as the mean score on the Mini-Mental State Examination to assess global cognitive status was high (mean, 29.4 ± 0.71), and there were no differences in performance on the executive function tests between the individuals with stroke and the control participants (Table 2). It is important to note that changes in executive function typically occur with normal aging,35,36 and variability in executive function ability is typical in people who would be considered cognitively normal.35,37,38 Furthermore, the individuals with stroke in this study on average had good sleep quality (Pittsburg Sleep Quality Index global score is <5), which is contrary to what would be expected in the general stroke population.20,39,40 The fact that the individuals with stroke in this study have good sleep quality limits the understanding of how sleep disturbances would impact the ability to perform and learn a motor task through its association with attention and set-shifting. Future studies should investigate the association between poor sleep quality, executive function, and motor learning in individuals with chronic stroke.
The findings of this study have important clinical implications. In healthy adults, the performance on the TMT D-KEFS is associated with the performance of activities of daily living and overall physical function.41–43 Attention and set-shifting are important factors that allow an individual to effectively and rapidly adapt to different environmental situations, hence, the association with functional performance. Furthermore, functional neuroimaging studies have demonstrated that performance on the TMT highly correlates with frontal cortical regions that are involved in motor control.44,45 Poor performance on the TMT was associated with lower independent functional outcomes,46 predicts poorer driving abilities,47 and predicts mortality in individuals with stroke.48 In the current study, the finding that executive function predicts off-line motor learning may influence the ability to perform or learn motor skills necessary to perform activities of daily living and could potentially impact motor recovery following stroke.
Because of the impact of executive function on motor learning, physical therapists and rehabilitation clinicians should consider screening attentional and set-shifting abilities in individuals poststroke. For example, the TMT D-KEFS could be used to screen for attentional and set-shifting abilities in individuals poststroke. Performance on the TMT D-KEFS may indicate capacity for motor skill learning, which could influence goal-setting and prognosis. Future studies are needed to determine whether executive function is associated with off-line learning of more functionally relevant tasks or whether addressing executive function deficits impacts motor learning and motor recovery following stroke.
The findings of this study demonstrate that certain executive function processes (attention and set-shifting) predict off-line motor learning in individuals with chronic stroke. Clinicians should consider screening executive function abilities specifically attention and set-shifting in individuals following stroke. Future research should explore whether rehabilitation treatment plans that facilitate off-line motor learning and executive functioning favorably enhance functional recovery poststroke.
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