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Quantitative evaluation of human cerebellum-dependent motor learning through prism adaptation of hand-reaching movement.

ABSTRACT: The cerebellum plays important roles in motor coordination and learning. However, motor learning has not been quantitatively evaluated clinically. It thus remains unclear how motor learning is influenced by cerebellar diseases or aging, and is related with incoordination. Here, we present a new application for testing human cerebellum-dependent motor learning using prism adaptation. In our paradigm, the participant wearing prism-equipped goggles touches their index finger to the target presented on a touchscreen in every trial. The whole test consisted of three consecutive sessions: (1) 50 trials with normal vision (BASELINE), (2) 100 trials wearing the prism that shifts the visual field 25° rightward (PRISM), and (3) 50 trials without the prism (REMOVAL). In healthy subjects, the prism-induced finger-touch error, i.e., the distance between touch and target positions, was decreased gradually by motor learning through repetition of trials. We found that such motor learning could be quantified using the "adaptability index (AI)", which was calculated by multiplying each probability of [acquisition in the last 10 trials of PRISM], [retention in the initial five trials of REMOVAL], and [extinction in the last 10 trials of REMOVAL]. The AI of cerebellar patients less than 70 years old (mean, 0.227; n = 62) was lower than that of age-matched healthy subjects (0.867, n = 21; p < 0.0001). While AI did not correlate with the magnitude of dysmetria in ataxic patients, it declined in parallel with disease progression, suggesting a close correlation between the impaired cerebellar motor leaning and the dysmetria. Furthermore, AI decreased with aging in the healthy subjects over 70 years old compared with that in the healthy subjects less than 70 years old. We suggest that our paradigm of prism adaptation may allow us to quantitatively assess cerebellar motor learning in both normal and diseased conditions.

SUBMITTER: Hashimoto Y

PROVIDER: S-EPMC4364988 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Modulation of frontal midline theta (fm?) is observed during error commission, but little is known about the role of theta oscillations in correcting motor behaviours. We investigate EEG activity of healthy partipants executing a reaching task under variable degrees of prism-induced visuo-motor distortion and visual occlusion of the initial arm trajectory. This task introduces directional errors of different magnitudes. The discrepancy between predicted and actual movement directions (i.e. the error), at the time when visual feedback (hand appearance) became available, elicits a signal that triggers on-line movement correction. Analysis were performed on 25 EEG channels. For each participant, the median value of the angular error of all reaching trials was used to partition the EEG epochs into high- and low-error conditions. We computed event-related spectral perturbations (ERSP) time-locked either to visual feedback or to the onset of movement correction. ERSP time-locked to the onset of visual feedback showed that fm? increased in the high- but not in the low-error condition with an approximate time lag of 200 ms. Moreover, when single epochs were sorted by the degree of motor error, fm? started to increase when a certain level of error was exceeded and, then, scaled with error magnitude. When ERSP were time-locked to the onset of movement correction, the fm? increase anticipated this event with an approximate time lead of 50 ms. During successive trials, an error reduction was observed which was associated with indices of adaptations (i.e., aftereffects) suggesting the need to explore if theta oscillations may facilitate learning. To our knowledge this is the first study where the EEG signal recorded during reaching movements was time-locked to the onset of the error visual feedback. This allowed us to conclude that theta oscillations putatively generated by anterior cingulate cortex activation are implicated in error processing in semi-naturalistic motor behaviours.

Project description:Practice of movement in virtual-reality and other artificially altered environments has been proposed as a method for rehabilitation following neurological injury and for training new skills in healthy humans. For such training to be useful, there must be transfer of learning from the artificial environment to the performance of desired skills in the natural environment. Therefore an important assumption of such methods is that practice in the altered environment engages the same learning and plasticity mechanisms that are required for skill performance in the natural environment. We test the hypothesis that transfer of learning may fail because the learning and plasticity mechanism that adapts to the altered environment is different from the learning mechanism required for improvement of motor skill. In this paper, we propose that a model that separates skill learning and environmental adaptation is necessary to explain the learning and aftereffects that are observed in virtual reality experiments. In particular, we studied the condition where practice in the altered environment should lead to correct skill performance in the original environment. Our 2-mechanism model predicts that aftereffects will still be observed when returning to the original environment, indicating a lack of skill transfer from the artificial environment to the original environment. To illustrate the model prediction, we tested 10 healthy participants on the interaction between a simple overlearned motor skill (straight hand movements to targets in different directions) and an artificially altered visuomotor environment (rotation of visual feedback of the results of movement). As predicted by the models, participants show adaptation to the altered environment and after-effects on return to the baseline environment even when practice in the altered environment should have led to correct skill performance. The presence of aftereffect under all conditions that involved changes in environment demonstrates separation of environmental adaptation and skill learning. Our results support the existence of two distinct learning modules with different adaptation properties. Therefore we suggest that adaptation to an altered environment may not be useful for training new skills.

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Quantitative evaluation of human cerebellum-dependent motor learning through prism adaptation of hand-reaching movement.

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