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Motor learning without moving: Proprioceptive and predictive hand localization after passive visuoproprioceptive discrepancy training.

ABSTRACT: An accurate estimate of limb position is necessary for movement planning, before and after motor learning. Where we localize our unseen hand after a reach depends on felt hand position, or proprioception, but in studies and theories on motor adaptation this is quite often neglected in favour of predicted sensory consequences based on efference copies of motor commands. Both sources of information should contribute, so here we set out to further investigate how much of hand localization depends on proprioception and how much on predicted sensory consequences. We use a training paradigm combining robot controlled hand movements with rotated visual feedback that eliminates the possibility to update predicted sensory consequences ('exposure training'), but still recalibrates proprioception, as well as a classic training paradigm with self-generated movements in another set of participants. After each kind of training we measure participants' hand location estimates based on both efference-based predictions and afferent proprioceptive signals with self-generated hand movements ('active localization') as well as based on proprioception only with robot-generated movements ('passive localization'). In the exposure training group, we find indistinguishable shifts in passive and active hand localization, but after classic training, active localization shifts more than passive, indicating a contribution from updated predicted sensory consequences. Both changes in open-loop reaches and hand localization are only slightly smaller after exposure training as compared to after classic training, confirming that proprioception plays a large role in estimating limb position and in planning movements, even after adaptation. (data: https://doi.org/10.17605/osf.io/zfdth, preprint: https://doi.org/10.1101/384941).

SUBMITTER: Mostafa AA

PROVIDER: S-EPMC6715176 | biostudies-other | 2019

REPOSITORIES: biostudies-other

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Motor learning without moving: Proprioceptive and predictive hand localization after passive visuoproprioceptive discrepancy training.

Mostafa Ahmed A AA 't Hart Bernard Marius BM Henriques Denise Y P DYP

PloS one 20190829 8

An accurate estimate of limb position is necessary for movement planning, before and after motor learning. Where we localize our unseen hand after a reach depends on felt hand position, or proprioception, but in studies and theories on motor adaptation this is quite often neglected in favour of predicted sensory consequences based on efference copies of motor commands. Both sources of information should contribute, so here we set out to further investigate how much of hand localization depends o ...[more]

PMID: 31465524

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Project description:ObjectiveNumerous reports advocate that training of the proprioceptive sense is a viable behavioral therapy for improving impaired motor function. However, there is little agreement of what constitutes proprioceptive training and how effective it is. We therefore conducted a comprehensive, systematic review of the available literature in order to provide clarity to the notion of training the proprioceptive system.MethodsFour major scientific databases were searched. The following criteria were subsequently applied: (1) A quantified pre- and post-treatment measure of proprioceptive function. (2) An intervention or training program believed to influence or enhance proprioceptive function. (3) Contained at least one form of treatment or outcome measure that is indicative of somatosensory function. From a total of 1284 articles, 51 studies fulfilled all criteria and were selected for further review.ResultsOverall, proprioceptive training resulted in an average improvement of 52% across all outcome measures. Applying muscle vibration above 30 Hz for longer durations (i.e., min vs. s) induced outcome improvements of up to 60%. Joint position and target reaching training consistently enhanced joint position sense (up to 109%) showing an average improvement of 48%. Cortical stroke was the most studied disease entity but no clear evidence indicated that proprioceptive training is differentially beneficial across the reported diseases.ConclusionsThere is converging evidence that proprioceptive training can yield meaningful improvements in somatosensory and sensorimotor function. However, there is a clear need for further work. Those forms of training utilizing both passive and active movements with and without visual feedback tended to be most beneficial. There is also initial evidence suggesting that proprioceptive training induces cortical reorganization, reinforcing the notion that proprioceptive training is a viable method for improving sensorimotor function.

Project description:BackgroundNeurological injuries such as stroke often differentially impair hand motor and somatosensory function, as well as the interplay between the two, which leads to limitations in performing activities of daily living. However, it is challenging to identify which specific aspects of sensorimotor function are impaired based on conventional clinical assessments that are often insensitive and subjective. In this work we propose and validate a set of robot-assisted assessments aiming at disentangling hand proprioceptive from motor impairments, and capturing their interrelation (sensorimotor impairments).MethodsA battery of five complementary assessment tasks was implemented on a one degree-of-freedom end-effector robotic platform acting on the index finger metacarpophalangeal joint. Specifically, proprioceptive impairments were assessed using a position matching paradigm. Fast target reaching, range of motion and maximum fingertip force tasks characterized motor function deficits. Finally, sensorimotor impairments were assessed using a dexterous trajectory following task. Clinical feasibility (duration), reliability (intra-class correlation coefficient ICC, smallest real difference SRD) and validity (Kruskal-Wallis test, Spearman correlations [Formula: see text] with Fugl-Meyer Upper Limb Motor Assessment, kinesthetic Up-Down Test, Box & Block Test) of robotic tasks were evaluated with 36 sub-acute stroke subjects and 31 age-matched neurologically intact controls.ResultsEighty-three percent of stroke survivors with varied impairment severity (mild to severe) could complete all robotic tasks (duration: <15 min per tested hand). Further, the study demonstrated good to excellent reliability of the robotic tasks in the stroke population (ICC>0.7, SRD<30%), as well as discriminant validity, as indicated by significant differences (p-value<0.001) between stroke and control subjects. Concurrent validity was shown through moderate to strong correlations ([Formula: see text]=0.4-0.8) between robotic outcome measures and clinical scales. Finally, robotic tasks targeting different deficits (motor, sensory) were not strongly correlated with each other ([Formula: see text]0.32, p-value>0.1), thereby presenting complementary information about a patient's impairment profile.ConclusionsThe proposed robot-assisted assessments provide a clinically feasible, reliable, and valid approach to distinctly characterize impairments in hand proprioceptive and motor function, along with the interaction between the two. This opens new avenues to help unravel the contributions of unique aspects of sensorimotor function in post-stroke recovery, as well as to contribute to future developments towards personalized, assessment-driven therapies.

Project description:This study examined the trainability of the proprioceptive sense and explored the relationship between proprioception and motor learning. With vision blocked, human learners had to perform goal-directed wrist movements relying solely on proprioceptive/haptic cues to reach several haptically specified targets. One group received additional somatosensory movement error feedback in form of vibro-tactile cues applied to the skin of the forearm. We used a haptic robotic device for the wrist and implemented a 3-day training regimen that required learners to make spatially precise goal-directed wrist reaching movements without vision. We assessed whether training improved the acuity of the wrist joint position sense. In addition, we checked if sensory learning generalized to the motor domain and improved spatial precision of wrist tracking movements that were not trained. The main findings of the study are: First, proprioceptive acuity of the wrist joint position sense improved after training for the group that received the combined proprioceptive/haptic and vibro-tactile feedback (VTF). Second, training had no impact on the spatial accuracy of the untrained tracking task. However, learners who had received VTF significantly reduced their reliance on haptic guidance feedback when performing the untrained motor task. That is, concurrent VTF was highly salient movement feedback and obviated the need for haptic feedback. Third, VTF can be also provided by the limb not involved in the task. Learners who received VTF to the contralateral limb equally benefitted. In conclusion, somatosensory training can significantly enhance proprioceptive acuity within days when learning is coupled with vibro-tactile sensory cues that provide feedback about movement errors. The observable sensory improvements in proprioception facilitates motor learning and such learning may generalize to the sensorimotor control of the untrained motor tasks. The implications of these findings for neurorehabilitation are discussed.

Project description:BACKGROUND:A large number of robotic or gravity-supporting devices have been developed for rehabilitation of upper extremity post-stroke. Because these devices continuously monitor performance data during training, they could potentially help to develop predictive models of the effects of motor training on recovery. However, during training with such devices, patients must become adept at using the new "tool" of the exoskeleton, including learning the new forces and visuomotor transformations associated with the device. We thus hypothesized that the changes in performance during extensive training with a passive, gravity-supporting, exoskeleton device (the Armeo Spring) will follow an initial fast phase, due to learning to use the device, and a slower phase that corresponds to reduction in overall arm impairment. Of interest was whether these fast and slow processes were related. METHODS:To test the two-process hypothesis, we used mixed-effect exponential models to identify putative fast and slow changes in smoothness of arm movements during 80 arm reaching tests performed during 20 days of exoskeleton training in 53 individuals with post-acute stroke. RESULTS:In line with our hypothesis, we found that double exponential models better fit the changes in smoothness of arm movements than single exponential models. In contrast, single exponential models better fit the data for a group of young healthy control subjects. In addition, in the stroke group, we showed that smoothness correlated with a measure of impairment (the upper extremity Fugl Meyer score - UEFM) at the end, but not at the beginning, of training. Furthermore, the improvement in movement smoothness due to the slow component, but not to the fast component, strongly correlated with the improvement in the UEFM between the beginning and end of training. There was no correlation between the change of peaks due to the fast process and the changes due to the slow process. Finally, the improvement in smoothness due to the slow, but not the fast, component correlated with the number of days since stroke at the onset of training - i.e. participants who started exoskeleton training sooner after stroke improved their smoothness more. CONCLUSIONS:Our results therefore demonstrate that at least two processes are involved in in performance improvements measured during mechanized training post-stroke. The fast process is consistent with learning to use the exoskeleton, while the slow process independently reflects the reduction in upper extremity impairment.

Dataset Information

Motor learning without moving: Proprioceptive and predictive hand localization after passive visuoproprioceptive discrepancy training.

Publications

Motor learning without moving: Proprioceptive and predictive hand localization after passive visuoproprioceptive discrepancy training.

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