Brain plasticity related to the consolidation of motor sequence learning and motor adaptation

Abstract

This study aimed to investigate, through functional MRI (fMRI), the neuronal substrates associated with the consolidation process of two motor skills: motor sequence learning (MSL) and motor adaptation (MA). Four groups of young healthy individuals were assigned to either (i) a night/sleep condition, in which they were scanned while practicing a finger sequence learning task or an eight-target adaptation pointing task in the evening (test) and were scanned again 12 h later in the morning (retest) or (ii) a day/awake condition, in which they were scanned on the MSL or the MA tasks in the morning and were rescanned 12 h later in the evening. As expected and consistent with the behavioral results, the functional data revealed increased test-retest changes of activity in the striatum for the night/sleep group compared with the day/awake group in the MSL task. By contrast, the results of the MA task did not show any difference in test-retest activity between the night/sleep and day/awake groups. When the two MA task groups were combined, however, increased test-retest activity was found in lobule VI of the cerebellar cortex. Together, these findings highlight the presence of both functional and structural dissociations reflecting the off-line consolidation processes of MSL and MA. They suggest that MSL consolidation is sleep dependent and reflected by a differential increase of neural activity within the corticostriatal system, whereas MA consolidation necessitates either a period of daytime or sleep and is associated with increased neuronal activity within the corticocerebellar system.

Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.

(A) Experimental design. In orange, the day/awake group was tested and retested in the scanner while staying awake during the 12-h delay between sessions. In blue, the night/sleep group was tested around 9:00 PM and slept in the laboratory while polysomnographic measures were recorded and retested approximately 2 h after waking up, around 9:00 AM. (B) Illustrations of the apparatus and order of finger presses used in the motor sequence learning (MSL) task, as well as the setup and performance of a representative block of trials in the motor adaptation (MA) task.

Fig. 2.

Behavioral results. (A) Behavioral results of the MSL task. Performance of the two groups across blocks in both immediate and retest sessions are illustrated. (B) Illustration of the groups’ performance at the individual sequence level, with each curve representing a session. (Upper) The performance for the day/awake group. (Lower) The night/sleep group. (C) Behavioral results for the MA task. The y axis represents the ratio of DS relative to the time taken to reach each target. Left graph shows averaged subject’s performance for each cycle. Right graph shows performance on each individual movement to a single target. Each curve represents a session. Savings occurred within the first four cycles of the retest session. Yet there was no significant interaction or between-group differences (night/sleep vs. day/awake) with respect to the amount of savings, and thus the results of both groups were pooled together to look at test–retest differences (consolidation).

Fig. 3.

(A) Functional data related to the MSL task. (Upper) Brain regions showing greater activity in the retest, compared with the immediate posttraining test session for the night/sleep group over the day/awake group. The functional data are presented over an average of the anatomical scans (n = 23) acquired in the whole group of subjects. (Lower) Bar graph of beta values from the local maxima in the right putamen. (B) Imaging results for the MA task shown on the averaged brain (n = 24). (Upper Left) Results of both day/awake and night/sleep groups combined, showing an increase of activity from the immediate posttraining to the retest session in lobule VI of the right cerebellum. (Upper Right) Results of the correlation analysis between the increase in activity from the immediate posttraining test to the retest session and the amount of savings observed in each subject. (Lower) Plot graph depicting a positive correlation between the amount of savings (x axis) and the strength of BOLD signal (y axis) in lobule VI of the right cerebellum (x = 36, y = −60, z = −21).