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Functional and Structural Plasticity Co-express in a Left Premotor Region During Early Bimanual Skill Learning.

ABSTRACT: Introduction: Motor skill learning already triggers the functional reorganization of regional brain activity after short periods of training. Recent studies suggest that microstructural change may emerge at similar timescales, but the spatiotemporal profiles of functional and structural plasticity have rarely been traced in parallel. Recently, we demonstrated that 5 days of endoscopic skill training induces changes in task-related brain activity in the ventral premotor cortex (PMv) and other areas of the frontoparietal grasping network. Here, we analyzed microstructural data, collected during the same experiment to investigate if microstructural plasticity overlaps temporally and spatially with the training-induced changes in task-related brain activity. Materials and Methods: Thirty-nine students were divided into a full-routine group (n = 20), that underwent three endoscopy training sessions in the MR-scanner as well as a 5-day virtual reality (VR)-endoscopy training and a brief-routine group (n = 19), that only performed the in-scanner endoscopy training sessions. Diffusion Tensor Imaging (DTI)-derived fractional anisotropy (FA) and resting-state functional magnetic resonance imaging (rs-fMRI) were collected at baseline, after the first and after the last VR-training session. Results: The full-routine group showed significant FA changes in a left-hemispheric subcortical cluster underlying the PMv region, for which we previously demonstrated functional plasticity during endoscopy training in the same sample. Functional (task-related fMRI) and structural (FA) changes showed the largest change from the first to the second scan, suggesting similar temporal dynamics. In the full-routine group, the FA change in the subcortical cluster underlying the left PMv scaled positively with the individual improvement in endoscopic surgery. Conclusion: Microstructural white-matter plasticity mirrors the spatiotemporal profile of task-dependent plasticity during a 5-day course of endoscopy skill training. The observed similarities motivate future research on the interplay between functional and structural plasticity during early skill acquisition.

SUBMITTER: Irmen F

PROVIDER: S-EPMC7456840 | biostudies-literature | 2020

REPOSITORIES: biostudies-literature

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Functional and Structural Plasticity Co-express in a Left Premotor Region During Early Bimanual Skill Learning.

Irmen Friederike F Karabanov Anke Ninija AN Bögemann Sophie Alida SA Andersen Kasper Winther KW Madsen Kristoffer Hougaard KH Bisgaard Thue T Dyrby Tim B TB Siebner Hartwig Roman HR

Frontiers in human neuroscience 20200814

<b>Introduction</b>: Motor skill learning already triggers the functional reorganization of regional brain activity after short periods of training. Recent studies suggest that microstructural change may emerge at similar timescales, but the spatiotemporal profiles of functional and structural plasticity have rarely been traced in parallel. Recently, we demonstrated that 5 days of endoscopic skill training induces changes in task-related brain activity in the ventral premotor cortex (PMv) and ot ...[more]

PMID: 32922275

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Project description:Using robotic devices might improve recovery post-stroke, but the optimal way to apply robotic assistance has yet to be determined. The current study aimed to investigate whether training under the robotic active-assisted mode improves bimanual motor skill learning (biMSkL) more than training under the active mode in stroke patients. Twenty-six healthy individuals (HI) and 23 chronic hemiparetic stroke patients with a detectable lesion on MRI or CT scan, who demonstrated motor deficits in the upper limb, were randomly allocated to two parallel groups. The protocol included a two-day training on a new bimanual cooperative task, LIFT-THE-TRAY, under either the active or active-assisted modes (where assistance decreased in a pre-determined stepwise fashion) with the bimanual version of the REAplan® robotic device. The hypothesis was that the active-assisted mode would result in greater biMSkL than the active mode. The biMSkL was quantified by a speed-accuracy trade-off (SAT) before (T1) and immediately after (T2) training on days 1 and 2 (T3 and T4). The change in SAT after 2 days of training (T4/T1) indicated that both HI and stroke patients learned and retained the bimanual cooperative task. After 2 days of training, the active-assisted mode did not improve biMSkL more than the active mode (T4/T1) in HI nor stroke patients. Whereas HI generalized the learned bimanual skill to different execution speeds in both the active and active-assisted subgroups, the stroke patients generalized the learned skill only in the active subgroup. Taken together, the active-assisted mode, applied in a pre-determined stepwise decreasing fashion, did not improve biMSkL more than the active mode in HI and stroke subjects. Stroke subjects might benefit more from robotic assistance when applied "as-needed." This study was approved by the local ethical committee (Comité d'éthique médicale, CHU UCL Namur, Mont-Godinne, Yvoir, Belgium; Internal number: 54/2010, EudraCT number: NUB B039201317382) on July 14, 2016 and was registered with ClinicalTrials.gov (Identifier: NCT03974750) on June 5, 2019.

Project description:BackgroundSince a stroke can impair bimanual activities, enhancing bimanual cooperation through motor skill learning may improve neurorehabilitation. Therefore, robotics and neuromodulation with transcranial direct current stimulation (tDCS) are promising approaches. To date, tDCS has failed to enhance bimanual motor control after stroke possibly because it was not integrating the hypothesis that the undamaged hemisphere becomes the major poststroke hub for bimanual control.ObjectiveWe tested the following hypotheses: (I) In patients with chronic hemiparetic stroke training on a robotic device, anodal tDCS applied over the primary motor cortex of the undamaged hemisphere enhances bimanual motor skill learning compared to sham tDCS. (II) The severity of impairment correlates with the effect of tDCS on bimanual motor skill learning. (III) Bimanual motor skill learning is less efficient in patients than in healthy individuals (HI).MethodsA total of 17 patients with chronic hemiparetic stroke and 7 healthy individuals learned a complex bimanual cooperation skill on the REAplan® neurorehabilitation robot. The bimanual speed/accuracy trade-off (biSAT), bimanual coordination (biCo), and bimanual force (biFOP) scores were computed for each performance. In patients, real/sham tDCS was applied in a crossover, randomized, double-blind approach.ResultsCompared to sham, real tDCS did not enhance bimanual motor skill learning, retention, or generalization in patients, and no correlation with impairment was noted. The healthy individuals performed better than patients on bimanual motor skill learning, but generalization was similar in both groups.ConclusionA short motor skill learning session with a robotic device resulted in the retention and generalization of a complex skill involving bimanual cooperation. The tDCS strategy that would best enhance bimanual motor skill learning after stroke remains unknown.Clinical trial registrationhttps://clinicaltrials.gov/ct2/show/NCT02308852, identifier: NCT02308852.

Dataset Information

Functional and Structural Plasticity Co-express in a Left Premotor Region During Early Bimanual Skill Learning.

Publications

Functional and Structural Plasticity Co-express in a Left Premotor Region During Early Bimanual Skill Learning.

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