Stimulating the cerebellum affects visuomotor adaptation but not intermanual transfer of learning

Abstract

When systematic movement errors occur, the brain responds with a systematic change in motor behavior. This type of adaptive motor learning can transfer intermanually; adaptation of movements of the right hand in response to training with a perturbed visual signal (visuomotor adaptation) may carry over to the left hand. While visuomotor adaptation has been studied extensively, it is unclear whether the cerebellum, a structure involved in adaptation, is important for intermanual transfer as well. We addressed this question with three experiments in which subjects reached with their right hands as a 30° visuomotor rotation was introduced. Subjects received anodal or sham transcranial direct current stimulation on the trained (experiment 1) or untrained (experiment 2) hemisphere of the cerebellum, or, for comparison, motor cortex (M1). After the training period, subjects reached with their left hand, without visual feedback, to assess intermanual transfer of learning aftereffects. Stimulation of the right cerebellum caused faster adaptation, but none of the stimulation sites affected transfer. To ascertain whether cerebellar stimulation would increase transfer if subjects learned faster as well as a larger amount, in experiment 3 anodal and sham cerebellar groups experienced a shortened training block such that the anodal group learned more than sham. Despite the difference in adaptation magnitude, transfer was similar across these groups, although smaller than in experiment 1. Our results suggest that intermanual transfer of visuomotor learning does not depend on cerebellar activity and that the number of movements performed at plateau is an important predictor of transfer.

Figure 1. Experimental protocol

A. Experimental setup. Subjects were seated in front of a digitizing tablet and computer monitor, wearing goggles to prevent seeing their hands. Subjects held a digitizing pen and made rapid shooting movements on the tablet to make a cursor on the screen (small yellow dot) move from the center home position (white square) through a target (large white dot) that appeared in one of 8 positions (grey dots; not visible to subject). B. Representation of the back of the brain with locations of anodal tDCS stimulation on the trained and untrained cerebellum and M1 (red and blue electrodes respectively). C. Experiment 1 and 2 protocol. Subjects performed 10 blocks of trials. Bold type: continuous visual error feedback was present. Italics: no visual feedback. The final row indicates number of trials in each block. tDCS was on throughout Blocks 5 and 6, over the trained or untrained hemisphere. In Block 6 (Adaptation), a 30° clockwise rotation was introduced to the cursor, such that subjects experienced large clockwise errors and had to adjust their movements to compensate. D. Experiment 3 protocol. Identical to Experiment 1, except Block 6 (Adaptation) was only 64 trials.

Figure 2. Experiment 1 results

Anodal tDCS on the trained hemisphere of cerebellum or M1 does not increase intermanual transfer. SH_TRAINED (black) and M1_TRAINED (blue) tDCS had similar effects on error angle throughout the entire session. CB_TRAINED (red) tDCS, however, increased the speed of learning in the Adaptation block. Inset bars represent averages and standard error of epochs 6–7 for Adaptation and 2–11 for the four Post-adaptation blocks, with baselines subtracted. *Post-hoc tests showed Adaptation in the CB_TRAINED group was significantly different from SH_TRAINED and M1_TRAINED. **Please note that all groups showed significant transfer of aftereffects in Post 1 (ANOVA_RM on un-subtracted data, effect of time, p < 0.01).

Figure 3. Experiment 2 results

Anodal tDCS on the untrained hemisphere of cerebellum or M1 does not increase intermanual transfer. SH_UNTRAINED (black), CB_UNTRAINED (red), and M1_UNTRAINED (blue) tDCS had similar effects on error angle in Adaptation. Inset bars represent averages and standard error of epochs 6–7 for Adaptation and 2–11 for the four Post-adaptation blocks, with baselines subtracted. **All groups showed significant transfer of aftereffects in Post 1 (ANOVA_RM on un-subtracted data, effect of time, p < 0.001).

Figure 4. Experiment 3 results

Faster and greater extent of adaptation caused by anodal tDCS on trained cerebellum does not influence intermanual transfer. Inset bars represent averages and standard error of epoch 8 for Adaptation and 2–11 for the four Post-adaptation blocks, with baselines subtracted. *By the end of an Adaptation block of 64 trials, subjects with AN_TRAINED (red) tDCS had learned significantly more than subjects with SH_TRAINED (black) tDCS. However, these effects did not alter transfer to the left hand. **Both groups showed significant transfer of aftereffects in Post 1 (ANOVA_RM on un-subtracted data, effect of time, p < 0.001).

Figure 5. Comparison of plateau length and transfer in Experiments 1 and 3

AIn the Adaptation block, subjects performed more trials at plateau in Experiment 1 than in Experiment 3. *Significant effect of Adaptation block duration on plateau length (2-way ANOVA effect of Adaptation block duration F_(1,44) = 112.8, p < 0.001). B. Subjects also transferred more in Experiment 1 than in Experiment 3. **Significant interaction of Adaption block duration and time (2-way ANOVA_RM on un-subtracted data in Post 1 vs. Base 4 showed an experiment by time interaction F_(1,91) = 4.75, p = 0.035).