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

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@article{f37d05e12c954190aee22949bba4850c,
title = "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.",
keywords = "endoscopy, grasping network, motor learning, plasticity, sensorimotor",
author = "Friederike Irmen and Karabanov, {Anke Ninija} and B{\"o}gemann, {Sophie Alida} and Andersen, {Kasper Winther} and Madsen, {Kristoffer Hougaard} and Thue Bisgaard and Dyrby, {Tim B} and Siebner, {Hartwig Roman}",
note = "Copyright {\textcopyright} 2020 Irmen, Karabanov, B{\"o}gemann, Andersen, Madsen, Bisgaard, Dyrby and Siebner.",
year = "2020",
month = aug,
day = "14",
doi = "10.3389/fnhum.2020.00310",
language = "English",
volume = "14",
pages = "1--11",
journal = "Frontiers in Human Neuroscience",
issn = "1662-5161",
publisher = "Frontiers Research Foundation",

}

RIS

TY - JOUR

T1 - Functional and Structural Plasticity Co-express in a Left Premotor Region During Early Bimanual Skill Learning

AU - Irmen, Friederike

AU - Karabanov, Anke Ninija

AU - Bögemann, Sophie Alida

AU - Andersen, Kasper Winther

AU - Madsen, Kristoffer Hougaard

AU - Bisgaard, Thue

AU - Dyrby, Tim B

AU - Siebner, Hartwig Roman

N1 - Copyright © 2020 Irmen, Karabanov, Bögemann, Andersen, Madsen, Bisgaard, Dyrby and Siebner.

PY - 2020/8/14

Y1 - 2020/8/14

N2 - 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.

AB - 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.

KW - endoscopy

KW - grasping network

KW - motor learning

KW - plasticity

KW - sensorimotor

UR - http://www.scopus.com/inward/record.url?scp=85089997334&partnerID=8YFLogxK

U2 - 10.3389/fnhum.2020.00310

DO - 10.3389/fnhum.2020.00310

M3 - Journal article

C2 - 32922275

VL - 14

SP - 1

EP - 11

JO - Frontiers in Human Neuroscience

JF - Frontiers in Human Neuroscience

SN - 1662-5161

M1 - 310

ER -

ID: 60881912