Size of error affects cerebellar contributions to motor learning

Abstract

Small errors may affect the process of learning in a fundamentally different way than large errors. For example, adapting reaching movements in response to a small perturbation produces generalization patterns that are different from large perturbations. Are distinct neural mechanisms engaged in response to large versus small errors? Here, we examined the motor learning process in patients with severe degeneration of the cerebellum. Consistent with earlier reports, we found that the patients were profoundly impaired in adapting their motor commands during reaching movements in response to large, sudden perturbations. However, when the same magnitude perturbation was imposed gradually over many trials, the patients showed marked improvements, uncovering a latent ability to learn from errors. On sudden removal of the perturbation, the patients exhibited aftereffects that persisted much longer than did those in healthy controls. That is, despite cerebellar damage, the brain maintained the ability to learn from small errors and the motor memory that resulted from this learning was strongly resistant to change. Of note was the fact that on completion of learning, the motor output of the cerebellar patients remained distinct from healthy controls in terms of its temporal characteristics. Therefore cerebellar degeneration impaired the ability to learn from large-magnitude errors, but had a lesser impact on learning from small errors. The neural basis of motor learning in response to small and large errors appears to be distinct.

Fig. 1.

Study protocol and performance of typical subjects. A: subjects participated in 2 experiments: abrupt and gradual introduction of a force field. They held the handle of a lightweight robotic arm and made shooting movements to a target, crossing it, and hitting a virtual pillow beyond the target. In the first 170 trials the robot produced a null field (no forces). In the subsequent 240 trials, a curl force field was introduced (field A or field B), perturbing the hand perpendicular to its direction of motion. The gray bars represent “error-clamp” trials during which the robot produced a stiff channel, guiding the hand to the target. These error-clamp trials allowed us to measure the subject's motor output perpendicular to the direction of motion. Vertical dashed lines indicate brief set breaks. B: representative trajectories from the end of the null and the beginning and end of the adaptation periods for an individual subject from the control, mild (#9), and severe (#6) groups. The movement starts at (0,0) and the target is at (0,10).

Fig. 2.

Performance during the adaptation block. A and B: angular error at the end of the movement (means ± SE) for each group during abrupt and gradual training. Set breaks are indicated by the numbered tick marks on the x-axis. Bin size is 2 trials for the trials immediately following set break and 6 trials for the remainder of the block. C: average angular error at the end of the movement (means ± SE) during the last 6 field trials when the force field was at full strength in both the abrupt and gradual conditions. Control and mild patients perform comparably in the 2 conditions. Severe patients showed an improvement in performance in the gradual condition. D: average peak speed (means ± SE) during the last 6 trials when the field was at full strength in both the abrupt and the gradual conditions. E: average peak speed (means ± SE) for the severe patients during abrupt and gradual training. Bin size is 2 trials for the trials immediately following set break and 6 trials for the remainder of the block.

Fig. 3.

Motor output in error-clamp trials at end of adaptation. A: force output, represented as percentage of perturbation (which normalizes for movement speed), during the last 2 error-clamp trials of the adaptation phase for the control, mild, and severe groups. B: average movement duration and peak force (% perturbation) during the last 2 error-clamp trials of training. C: peak force (% perturbation) during the last 2 error-clamp trials of the adaptation phase plotted as a function of ataxia score for mild and severe patients (top: abrupt and gradual; bottom: within-subject difference between abrupt and gradual). In the abrupt condition, severity predicts performance in the error-clamp trials.

Fig. 4.

Motor output in postadaptation error-clamp block. A–C: maximum force output during the error-clamp trials in the post-adaptation retention block (means ± SE). Bin size is 6 trials. D: fragility of the memory. The change in force output from the beginning to the end of the post-adaptation block, expressed as percentage reduction from the first 6 trials to the last 6 trials. The changes are shown as means ± SE. In the gradual condition, the severe patients had less percentage loss of motor output than that of control and mild patients.

Fig. 5.

Aftereffects during the final null block of trials. A–C: angular error at the end of the movement (means ± SE) during the null washout trials. Bin size is 8 trials. The control and mild groups demonstrated aftereffects in both abrupt and gradual conditions. The severe group showed significant aftereffects only in the gradual condition. (The total number of trials does not add up to 80 because there were also error-clamp trials in this data set, which are not shown.)

Fig. 6.

Overcompensation for the force perturbation. A and B: angular error at 100 ms (means ± SE) for each subgroup during abrupt and gradual training. Bin size is 2 trials immediately following set break and 6 trials for the remainder of the block. C: average angular error at 100 ms (means ± SE) during the last 6 trials when the field was at full strength in both abrupt and gradual conditions. Controls showed overcompensation in both conditions. The severe patients did not show significant overcompensation in either condition.