PLoS One. 2017 Apr 13;12(4):e0175296. doi: 10.1371/journal.pone.0175296.

Enhancing consolidation of a rotational visuomotor adaptation task through acute exercise.

Ferrer-Uris B1, Busquets A1, Lopez-Alonso V2, Fernandez-Del-Olmo M2, Angulo-Barroso R1,3.

1 Institut Nacional d’Educació Física de Catalunya, University of Barcelona, Barcelona, Spain.

2 Facultade de Ciencias do Deporte e a Educación Física (INEF Galicia), University of A Coruña, A Coruña, Spain.

3 Kinesiology, California State University, Northridge, Northridge CA, United States of America.

 

Abstract

We assessed the effect of a single bout of intense exercise on the adaptation and consolidation of a rotational visuomotor task, together with the effect of the order of exercise presentation relative to the learning task. Healthy adult participants (n = 29) were randomly allocated to one of three experimental groups: (1) exercise before task practice, (2) exercise after task practice, and (3) task practice only. After familiarization with the learning task, participants undertook a baseline practice set. Then, four 60° clockwise rotational sets were performed, comprising an adaptation set and three retention sets at 1 h, 24 h, and 7 days after the adaptation set. Depending on the experimental group, exercise was presented before or after the adaptation sets. We found that error reduction during adaptation was similar regardless of when exercise was presented. During retention, significant error reduction was found in the retention set at 1 h for both exercise groups, but this enhancement was not present during subsequent retention sets, with no differences present between exercise groups. We conclude that an acute bout of intense exercise could positively affect retention, although the order in which exercise is presented does not appear to influence its benefits during the early stages of consolidation.

PMID: 28406936 PMCID: PMC5391069 DOI: 10.1371/journal.pone.0175296

 

Supplementary information

Exercise has been associated with multiple benefits, including cognitive stimulation and learning enhancements. The present study focused on the benefits of an intense acute exercise bout on adult learning of a perceptual-motor adaptation task. The question posed was: Can a short bout of intense exercise (13 min at 60-85% effort) reduce the errors made on a joystick manipulation task in adults? During motor learning two phases are usually defined (Krakauer & Shadmehr, 2006). First, a process named adaptation occurs where an improvement in skill performance is observed as a response to the initial practice (first set of skill practice). In our case, a reduction of errors made would be observed. During the adaptation phase, the formation of an internal model of the skill is assumed, which presents a rather unstable state initially being susceptible to interferences (Krakauer, Ghez, & Ghilardi, 2005). Following this adaptation phase, a consolidation of the internal model might occur in absence of skill practice. During the consolidation phase, the internal model becomes more stable and resistant to possible interferences. Because of this consolidation process, the skill will become perdurable and therefore it may be possible to recall the skill after some time without practicing it. In our case, a successful consolidation phase would mean that the reduction of errors in the joystick manipulation task would persist even when a time period with no additional practice has elapsed.

Usually, the adaptation phase (first set of practice) is studied via the analysis of skill performance improvements across practice trials (Magill & Anderson, 2014). To do so, performance variables, like errors, during the adaptation trials are plotted, and analyzed through the so called learning curves. Learning curves usually show an initial rapid learning rate during the initial practice trials, followed by a slower learning rate during the later practice trials. So, in our case, the errors are rapidly reduced in the initial adaptation trials, while lesser reduction of errors are seen in the later adaptation trials.

Consolidation of the formed internal model of the skill is usually assessed by the performance during retention tests (additional sets of testing with minimal practice). Retention tests consist of evaluations of skill performance done after a time interval from skill adaptation where no additional practice is performed (Magill & Anderson, 2014). Typically the time interval between adaptation and retention tests ranges from one hour to several days. In our case, we used 1h, 24 h, and 7 days. Good performance during a retention test, that is, reduction or minimal errors in our case, may indicate that consolidation of the motor skill has occurred to some degree. Furthermore, two other procedures are also usually used to explore if consolidation has occurred: analysis of “Savings” and “Offline gains” (Urbain, Houyoux, Albouy, & Peigneux, 2014). Savings are usually assessed by comparing the initial performance during the adaptation phase of learning the skill to the initial trials during the retention test. Savings may represent the amount of performance improvement from the start of the skill practice to the recall of the skill after a non-practice period. On the other hand, offline gains are usually assessed by comparing the performance during the later trials during the adaptation phase to the initial trials during the retention test. Offline gains may represent the amount of performance retained after a non-practice period.

In the present study, the effects of an intense exercise bout on learning of a joystick manipulation motor skill were analyzed in three experimental groups: (1) Exercise prior to the motor skill adaptation, EX-rVMA group; (2) exercise after the motor skill adaptation, rVMA-EX group; (3) and a no-exercise group as control, CON group.  Exercise effects on motor learning, both adaptation and consolidation, were assessed via analysis of the learning curves, and via analysis of the retention test performance, respectively. We also analyzed the possible relation between the adaptation and consolidation processes via Pearson correlation analysis between the initial adaptation and initial retention (i.e. Savings), and later adaptation and initial retention (i.e. Offline gains).

In addition to postulating that exercise can improve motor learning in adults, other studies suggest that motor learning may be affected by multiple factors for instance fitness level. Therefore, the role of fitness level was studied via Pearson correlation analysis as a possible factor moderating motor learning during the adaptation and retention tests. These analyses were performed using estimated VO2max through the 20 meter shuttle run test (Léger, Mercier, Gadoury, & Lambert, 1988) as a measure of fitness level and the initial movement angular errors (IDE) during the task trials (lower initial angular errors indicated better skill performance). IDE was used as a representation of the movement motor planning, which is usually used as indicator of the state of the internal model of the skill (Contreras-Vidal, Bo, Boudreau, & Clark, 2005).

Analysis of the effects of exercise on the overall learning curve

During the analysis of the exercise effect on the overall learning curve, quasi-identical learning curves were observed among the three experimental groups, meaning that exercise had a null effect on the adaptation rate of the skill (Figure 1). That is, the intense exercise bout of 13 minutes was not effective in further reducing the errors produced during the adaptation phase. A possible explanation for the null effect of exercise on motor adaptation could be related to the exercise intensity (McMorris & Hale, 2012). Previous studies have observed greater exercise benefits on short-term memory and cognitive stimulation when the exercise intensity was moderate. In contrast, high exercise intensity seems to cause no cognitive stimulation. Furthermore, other studies examining the effects of intense exercise on motor learning have also observed a null effect of exercise on motor adaptation, possibly due to some level of fatigue induced by the exercise bout which could have hindered potential exercise benefits during the adaptation phase (Roig, Skriver, Lundbye-Jensen, Kiens, & Nielsen, 2012).

 

 

Figure 1. Comparison of the learning curves during the adaptation phase among the three experimental groups. Trials during adaptation were grouped in epochs of 8 trials and fitted to a double exponential curve for analysis purposes. Similar learning curves and rate of learning were observed among the three experimental groups during the adaptation of the motor task. Abbreviations: CON = no-exercise group; EX–rVMA = learning task after exercise group; rVMA–EX = learning task before exercise group; IDE = initial movement angular error.

 

 

Correlational analyses of “Savings” and  “Offline gains”

When exercise effects were analyzed during the retention sets of the learning task, improvements were observed during the first retention test, performed 1 hour after the adaptation of the skill, for both exercise groups (for a detailed description of these results see Ferrer-Uris, Busquets, Lopez-Alonso, Fernandez-del-Olmo, & Angulo-Barroso, 2017). Therefore, one could say that a short bout of 13 minutes of intense exercise better maintains the performance level of the joystick task (less errors) for those adults that exercised either before or after the adaptation phase. Figure 2 represents groups’ performance at the start and end of the adaptation phase of the learning task along with the starting performance during three retention tests performed during the study.

 

 

Figure 2. Error values among groups during the initial and later adaptation trials and initial retention trials of the learning task.  Initial movement angular error values (mean and SD) are shown for the learning task during the first and last 32 trials of the adaptation and the first 32 trials during the retention tests of the motor task. Abbreviations: CON = no-exercise group; EX–rVMA = learning task after exercise group; rVMA–EX = learning task before exercise group; IDE = initial movement angular error; RT = retention test (performed at 1 h, 24 h and 7 days after the task adaptation).

 

Savings and Offline gains were analyzed using the first retention test (RT1h) initial trials and the initial adaptation trials or later adaptation trials, respectively. Savings correlational analysis revealed that initial performance during the adaptation of the motor task presented no correlation with the initial retention performance (r = 0.239; p = 0.212) (Figure 3). These “Savings” results may indicate that savings cannot be inferred from the initial performance on the task and, thus, we cannot predict final performance (retention) of participants by observing their initial performance during the adaptation. However, when we evaluated the offline gains by exploring the correlation between the later adaptation trials and the initial retention performance, a positive moderate significant correlation was found (for a detailed description of these results see Ferrer-Uris et al., 2017). This positive correlation indicated that while saving can’t be predicted, offline gains may be partially explained by the performance reached at the end of the adaptation. Therefore, reaching a good performance level during the later adaptation phase may be relevant in order to consolidate and recall the motor skill. Therefore, retention performance can be partly inferred from performance at the end of adaptation.

 

 

Figure 3. Savings: Correlation between initial angular error (IDE) at the start of the adaptation and the start of the RT1h of the learning task. IDE mean errors were calculated at the start of the adaptation (AD; first 32 trials, 4 epochs) and at the start of the first retention test (RT1h; 32 trials, 4 epochs). Performance at the start of the adaptation and at the start of the first retention test was not correlated.

 

Fitness level as moderator of exercise effects on motor learning

It has been postulated that good fitness level may enhance learning capacity (Herting & Nagel, 2013).  Given this potential relationship, correlational analysis between participants’ estimated VO2max and their performance during the adaptation and retention tests of the motor task were explored for a subsample of adults who did not exercise. No significant correlation was observed between fitness level and any of the task test performance (see Table 1 for results). Lack of a significant correlation between the task performance and participants’ fitness level could be an indication that fitness level has no moderating effect on motor learning. However, we have to take into account that only active participants were included in the present study and, therefore, the sample of this study was quite homogenous. Therefore, it may be possible that the results obtained in this study regarding the moderator effect of fitness level on motor learning were affected by the exclusion of sedentary, low-fit participants and highly trained individuals. Future research comparing motor learning between high-fit and low-fit individuals should address this topic.

 

Table 1. Results of the Pearson correlation test for the fitness level (estimated VO2max) and the task initial angular error (IDE) during adaptation and retention tests

Abbreviations: AD= adaptation; RT = retention test (performed at 1 h, 24 h and 7 days after the task adaptation).

 

Highlights:

  • Effects of acute intense exercise on adult’s motor learning (adaptation and consolidation phases) were examined
  • Intense exercise enhanced the short-term motor consolidation of a rotational perceptual-motor task
  • Exercise and learning task presentation order had similar positive effects on exercise-induced consolidation of the task
  • Exercise had no effect on the learning curve and learning ratio of the motor task during the adaptation phase
  • Analyses of “Savings” and “Offline gains” indicated that what matters is one’s level of performance at the end of the adaptation phase and not at the beginning
  • Participant’s fitness level seemed to have no moderating effect on motor learning in a sample composed of homogenously fit participants

 

References:

Contreras-Vidal, J. L., Bo, J., Boudreau, J. P., & Clark, J. E. (2005). Development of visuomotor representations for hand movement in young children. Experimental Brain Research, 162(2), 155–64. https://doi.org/10.1007/s00221-004-2123-7

Ferrer-Uris, B., Busquets, A., Lopez-Alonso, V., Fernandez-del-Olmo, M., & Angulo-Barroso, R. (2017). Enhancing consolidation of a rotational visuomotor adaptation task through acute exercise. PLOS ONE, 12(4), 1–18. https://doi.org/10.1371/journal.pone.0175296

Herting, M. M., & Nagel, B. J. (2013). Differences in brain activity during a verbal associative memory encoding task in high- and low-fit adolescents. Journal of Cognitive Neuroscience, 25(4), 595–612. https://doi.org/10.1162/jocn_a_00344

Krakauer, J. W., Ghez, C., & Ghilardi, M. F. (2005). Adaptation to visuomotor transformations: consolidation, interference, and forgetting. The Journal of Neuroscience : The Official Journal of the Society for Neuroscience, 25(2), 473–8. https://doi.org/10.1523/JNEUROSCI.4218-04.2005

Krakauer, J. W., & Shadmehr, R. (2006). Consolidation of motor memory. Trends in Neurosciences, 29(1), 58–64. https://doi.org/10.1016/j.tins.2005.10.003

Léger, L. a, Mercier, D., Gadoury, C., & Lambert, J. (1988). The multistage 20 metre shuttle run test for aerobic fitness. Journal of Sports Sciences, 6(2), 93–101. https://doi.org/10.1080/02640418808729800

Magill, R. A., & Anderson, D. (2014). Motor learning and control : concepts and applications (10th ed). New York : McGraw-Hill. Retrieved from http://cataleg.ub.edu/record=b2091819~S1*spi

McMorris, T., & Hale, B. J. (2012). Differential effects of differing intensities of acute exercise on speed and accuracy of cognition: A meta-analytical investigation. Brain and Cognition, 80(3), 338–351. https://doi.org/10.1016/j.bandc.2012.09.001

Roig, M., Skriver, K., Lundbye-Jensen, J., Kiens, B., & Nielsen, J. B. (2012). A single bout of exercise improves motor memory. PloS One, 7(9), e44594. https://doi.org/10.1371/journal.pone.0044594

Urbain, C., Houyoux, E., Albouy, G., & Peigneux, P. (2014). Consolidation through the looking-glass: sleep-dependent proactive interference on visuomotor adaptation in children. Journal of Sleep Research, 23(1), 44–52. https://doi.org/10.1111/jsr.12082