Dissociating the roles of the cerebellum and motor cortex during adaptive learning: the motor cortex retains what the cerebellum learns

Abstract

Adaptation to a novel visuomotor transformation has revealed important principles regarding learning and memory. Computational and behavioral studies have suggested that acquisition and retention of a new visuomotor transformation are distinct processes. However, this dissociation has never been clearly shown. Here, participants made fast reaching movements while unexpectedly a 30-degree visuomotor transformation was introduced. During visuomotor adaptation, subjects received cerebellar, primary motor cortex (M1) or sham anodal transcranial direct current stimulation (tDCS), a noninvasive form of brain stimulation known to increase excitability. We found that cerebellar tDCS caused faster adaptation to the visuomotor transformation, as shown by a rapid reduction of movement errors. These findings were not present with similar modulation of visual cortex excitability. In contrast, tDCS over M1 did not affect adaptation, but resulted in a marked increase in retention of the newly learnt visuomotor transformation. These results show a clear dissociation in the processes of acquisition and retention during adaptive motor learning and demonstrate that the cerebellum and primary motor cortex have distinct functional roles. Furthermore, they show that is possible to enhance cerebellar function using tDCS.

Figure 1.

Schematic representation of the main experimental setup. (a) Experiment 1: 3 groups (n = 10 each; SHAM, CB, M1) participated in a similar protocol involving 6 blocks. Pre1, Pre2, Post1, and Post2 were all under veridical conditions (no visual perturbation). During Adapt1 and 2, subjects were exposed to a 30-degree CCW screen–cursor transformation. Anodal (CB, and M1) or SHAM tDCS (SHAM) was applied to either the ipsilateral cerebellar cortex (CB) or contralateral motor cortex (M1) during Pre2 and Adapt1 (approximately 15 min; shaded area). The numbers under each block represent the amount of trials, while the numbers in brackets indicate the approximate length of time in minutes for each block. (b) Experiment 2: 3 groups (n = 10 each; SHAM, CB, M1) experienced a similar protocol involving 6 blocks. Pre1 and 2 were under veridical conditions. During Adapt, subjects were exposed to a 30-degree CCW screen–cursor transformation. Anodal or SHAM tDCS was applied during Pre2 and Adapt to M1 or cerebellum. Post1, 2, and 3 all involved trials with no visual feedback. (c) Experiment 3: 2 groups (n = 8 each: CB, OC) experienced a similar first 3 blocks where anodal tDCS was applied during Pre2 and Adapt to either the cerebellum or OC. Before Pre1 (pre) and after Adapt (post), TMS was used to assess phosphene threshold, a measure of visual cortex excitability.

Figure 2.

Single subject data for experiment 1. A sample subject from the SHAM (black), CB (cerebellar anodal tDCS: red), and M1 (M1 anodal tDCS: blue) groups is shown. (a) Under veridical conditions, all groups made similar accurate movement trajectories toward each target (Pre2: epoch 12). (b) When initially exposed to the novel 30-degree CCW screen–cursor transformation (Adapt1: epoch 1), subjects show comparable error in their trajectories. (c) In comparison to the SHAM and M1 participants, the CB participant is able to display a reduced amount of error in their movement trajectories at approximately midpoint of the adaptation block (Adapt1: epoch 8).

Figure 3.

Group data for experiment 1. End point error (degrees) are shown during baseline (Pre1 and 2), adaptation (Adapt1 and 2), and deadaptation (Post1 and 2) for the SHAM (black), CB (red), and M1 (blue) groups (mean ± standard error of the mean [SEM] of 8 trial epochs). Positive values indicate counterclockwise deviation. The shaded area represents blocks in which tDCS was applied (Pre2 and Adapt1). Bar graphs insets indicate “mean end point error” in degrees (±SEM) for SHAM (black), CB (red), and M1 (blue) groups in each block. This was determined for each participant by averaging consecutive epochs (see Materials and Methods). For each block, separate 1-way ANOVAs compared these values across groups. *P < 0.009.

Figure 4.

Single participant data for experiment 2. A sample participant from the SHAM (black), CB (cerebellar anodal tDCS: red), and M1 (M1 anodal tDCS: blue) groups is shown. (a) Under veridical conditions, all groups made similar accurate movement trajectories toward each target (Pre2: epoch 12). (b) Similarly to experiment 1, the CB participant exhibits a reduced amount of error in their movement trajectories by epoch 8, which is not observed in both the SHAM and M1 participants (Adapt1: epoch 8). (c) Initially in the trials with no vision, all participants show a similar amount of error (Post1: epoch 1). (d) By the end of the no-vision blocks, the M1 participant displays a larger amount of movement error relative to the SHAM and CB participants indicative of increased retention (Post3: epoch 8).

Figure 5.

Group data for experiment 2. End point error (degrees) are shown during baseline (Pre1 and 2), adaptation (Adapt) and deadaptation with no visual feedback (Post1, 2, and 3) for the SHAM (black), CB (red), and M1 (blue) groups (mean ± standard error of the mean [SEM] of 8 trial epochs). Positive values indicate counterclockwise deviation. The shaded area represents blocks in which tDCS was applied (Pre2 and Adapt). Bar graphs insets indicate mean end point error in degrees (±SEM) for SHAM (black), CB (red), and M1 (blue) in each block. For each block, separate 1-way ANOVAs compared these values across groups. *P < 0.05.

Figure 6.

Group data for experiment 3. (a) End point error (degrees) are shown during baseline (Pre1 and 2) and adaptation (Adapt) for the OC (green) and CB (red) groups (mean ± standard error of the mean [SEM] of 8 trial epochs). Positive values indicate counterclockwise deviation. The shaded area represents blocks in which tDCS was applied (Pre2 and Adapt). Bar graph insets indicate mean end point error in degrees (±SEM) during adapt for OC (green), CB (red), and experiment 2 SHAM (black) conditions. For Adapt, an ANOVA compared these values between groups. (b) Changes in visual PTs as measured by TMS (% of stimulator output). These were assessed prior to Pre1 (pre) and after Adapt (post). An independent t-test compared these values (post–pre) between groups. *P < 0.05.