Neural substrates underlying motor skill learning in chronic hemiparetic stroke patients
Motor skill learning is critical in post-stroke motor recovery, but little is known about its underlying neural substrates. Recently, using a new visuomotor skill learning paradigm involving a speed/accuracy trade-off in healthy individuals we identified three subpopulations based on their behaviora...
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doaj-805843bd76614199ab34b5e4818a234f2020-11-25T03:32:28ZengFrontiers Media S.A.Frontiers in Human Neuroscience1662-51612015-06-01910.3389/fnhum.2015.00320136212Neural substrates underlying motor skill learning in chronic hemiparetic stroke patientsStephanie eLefebvre0Stephanie eLefebvre1Laurence eDricot2Patrice eLaloux3Patrice eLaloux4wojciech eGradkowski5wojciech eGradkowski6Philippe eDesfontaines7Frédéric eEvrard8Andre ePeeters9Jacques eJamart10Yves eVandermeeren11Yves eVandermeeren12Yves eVandermeeren13Université catholique de Louvain, CHU Dinant-Godinne UCL NamurUniversité catholique de Louvain (UCL), Institute of NeuroScience (IoNS)Université catholique de Louvain (UCL), Institute of NeuroScience (IoNS)Université catholique de Louvain, CHU Dinant-Godinne UCL NamurUniversité catholique de Louvain (UCL), Institute of NeuroScience (IoNS)ImagilysWarsaw University of TechnologyCHC, Site Saint-JosephClinique Saint-PierreCliniques Universitaires Saint Luc UCLCHU Dinant-Godinne UCL NamurUniversité catholique de Louvain, CHU Dinant-Godinne UCL NamurUniversité catholique de Louvain (UCL), Institute of NeuroScience (IoNS)Université catholique de LouvainMotor skill learning is critical in post-stroke motor recovery, but little is known about its underlying neural substrates. Recently, using a new visuomotor skill learning paradigm involving a speed/accuracy trade-off in healthy individuals we identified three subpopulations based on their behavioral trajectories: fitters (in whom improvement in speed or accuracy coincided with deterioration in the other parameter), shifters (in whom speed and/or accuracy improved without degradation of the other parameter), and non-learners. We aimed to identify the neural substrates underlying the first stages of motor skill learning in chronic hemiparetic stroke patients and to determine whether specific neural substrates were recruited in shifters versus fitters. During functional magnetic resonance imaging (fMRI), 23 patients learned the visuomotor skill with their paretic upper limb. In the whole-group analysis, correlation between activation and motor skill learning was restricted to the dorsal prefrontal cortex of the damaged hemisphere (DLPFCdamh: r=-0.82) and the dorsal premotor cortex (PMddamh: r=0.70); the correlations was much lesser (-0.16<r>0.25) in the other regions of interest. In a subgroup analysis, significant activation was restricted to bilateral posterior parietal cortices of the fitters and did not correlate with motor skill learning. Conversely, in shifters significant activation occurred in the primary sensorimotor cortexdamh and supplementary motor areadamh and in bilateral PMd where activation changes correlated significantly with motor skill learning (r=0.91). Finally, resting-state activity acquired before learning showed a higher functional connectivity in the salience network of shifters compared with fitters (qFDR<0.05). These data suggest a neuroplastic compensatory reorganization of brain activity underlying the first stages of motor skill learning with the paretic upper limb in chronic hemiparetic stroke patients, with a key role of bilateral PMdhttp://journal.frontiersin.org/Journal/10.3389/fnhum.2015.00320/fullStrokefMRINeurorehabilitationpremotor cortexmotor skill learningResting-state fMRI |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Stephanie eLefebvre Stephanie eLefebvre Laurence eDricot Patrice eLaloux Patrice eLaloux wojciech eGradkowski wojciech eGradkowski Philippe eDesfontaines Frédéric eEvrard Andre ePeeters Jacques eJamart Yves eVandermeeren Yves eVandermeeren Yves eVandermeeren |
spellingShingle |
Stephanie eLefebvre Stephanie eLefebvre Laurence eDricot Patrice eLaloux Patrice eLaloux wojciech eGradkowski wojciech eGradkowski Philippe eDesfontaines Frédéric eEvrard Andre ePeeters Jacques eJamart Yves eVandermeeren Yves eVandermeeren Yves eVandermeeren Neural substrates underlying motor skill learning in chronic hemiparetic stroke patients Frontiers in Human Neuroscience Stroke fMRI Neurorehabilitation premotor cortex motor skill learning Resting-state fMRI |
author_facet |
Stephanie eLefebvre Stephanie eLefebvre Laurence eDricot Patrice eLaloux Patrice eLaloux wojciech eGradkowski wojciech eGradkowski Philippe eDesfontaines Frédéric eEvrard Andre ePeeters Jacques eJamart Yves eVandermeeren Yves eVandermeeren Yves eVandermeeren |
author_sort |
Stephanie eLefebvre |
title |
Neural substrates underlying motor skill learning in chronic hemiparetic stroke patients |
title_short |
Neural substrates underlying motor skill learning in chronic hemiparetic stroke patients |
title_full |
Neural substrates underlying motor skill learning in chronic hemiparetic stroke patients |
title_fullStr |
Neural substrates underlying motor skill learning in chronic hemiparetic stroke patients |
title_full_unstemmed |
Neural substrates underlying motor skill learning in chronic hemiparetic stroke patients |
title_sort |
neural substrates underlying motor skill learning in chronic hemiparetic stroke patients |
publisher |
Frontiers Media S.A. |
series |
Frontiers in Human Neuroscience |
issn |
1662-5161 |
publishDate |
2015-06-01 |
description |
Motor skill learning is critical in post-stroke motor recovery, but little is known about its underlying neural substrates. Recently, using a new visuomotor skill learning paradigm involving a speed/accuracy trade-off in healthy individuals we identified three subpopulations based on their behavioral trajectories: fitters (in whom improvement in speed or accuracy coincided with deterioration in the other parameter), shifters (in whom speed and/or accuracy improved without degradation of the other parameter), and non-learners. We aimed to identify the neural substrates underlying the first stages of motor skill learning in chronic hemiparetic stroke patients and to determine whether specific neural substrates were recruited in shifters versus fitters. During functional magnetic resonance imaging (fMRI), 23 patients learned the visuomotor skill with their paretic upper limb. In the whole-group analysis, correlation between activation and motor skill learning was restricted to the dorsal prefrontal cortex of the damaged hemisphere (DLPFCdamh: r=-0.82) and the dorsal premotor cortex (PMddamh: r=0.70); the correlations was much lesser (-0.16<r>0.25) in the other regions of interest. In a subgroup analysis, significant activation was restricted to bilateral posterior parietal cortices of the fitters and did not correlate with motor skill learning. Conversely, in shifters significant activation occurred in the primary sensorimotor cortexdamh and supplementary motor areadamh and in bilateral PMd where activation changes correlated significantly with motor skill learning (r=0.91). Finally, resting-state activity acquired before learning showed a higher functional connectivity in the salience network of shifters compared with fitters (qFDR<0.05). These data suggest a neuroplastic compensatory reorganization of brain activity underlying the first stages of motor skill learning with the paretic upper limb in chronic hemiparetic stroke patients, with a key role of bilateral PMd |
topic |
Stroke fMRI Neurorehabilitation premotor cortex motor skill learning Resting-state fMRI |
url |
http://journal.frontiersin.org/Journal/10.3389/fnhum.2015.00320/full |
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