Cargando…

Motor learning in developmental coordination disorder: behavioral and neuroimaging study

Developmental coordination disorder (DCD) is characterized by motor learning deficits that are poorly understood within whole-body activities context. Here we present results of one of the largest non-randomized interventional trials combining brain imaging and motion capture techniques to examine m...

Descripción completa

Detalles Bibliográficos
Autores principales: Al-Yahya, Emad, Esser, Patrick, Weedon, Benjamin D., Joshi, Shawn, Liu, Yan-Ci, Springett, Daniella N., Salvan, Piergiorgio, Meaney, Andy, Collett, Johnny, Inacio, Mario, Delextrat, Anne, Kemp, Steve, Ward, Tomas, Izadi, Hooshang, Johansen-Berg, Heidi, Ayaz, Hasan, Dawes, Helen
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10323432/
https://www.ncbi.nlm.nih.gov/pubmed/37425016
http://dx.doi.org/10.3389/fnins.2023.1187790
_version_ 1785068957999300608
author Al-Yahya, Emad
Esser, Patrick
Weedon, Benjamin D.
Joshi, Shawn
Liu, Yan-Ci
Springett, Daniella N.
Salvan, Piergiorgio
Meaney, Andy
Collett, Johnny
Inacio, Mario
Delextrat, Anne
Kemp, Steve
Ward, Tomas
Izadi, Hooshang
Johansen-Berg, Heidi
Ayaz, Hasan
Dawes, Helen
author_facet Al-Yahya, Emad
Esser, Patrick
Weedon, Benjamin D.
Joshi, Shawn
Liu, Yan-Ci
Springett, Daniella N.
Salvan, Piergiorgio
Meaney, Andy
Collett, Johnny
Inacio, Mario
Delextrat, Anne
Kemp, Steve
Ward, Tomas
Izadi, Hooshang
Johansen-Berg, Heidi
Ayaz, Hasan
Dawes, Helen
author_sort Al-Yahya, Emad
collection PubMed
description Developmental coordination disorder (DCD) is characterized by motor learning deficits that are poorly understood within whole-body activities context. Here we present results of one of the largest non-randomized interventional trials combining brain imaging and motion capture techniques to examine motor skill acquisition and its underpinning mechanisms in adolescents with and without DCD. A total of 86 adolescents with low fitness levels (including 48 with DCD) were trained on a novel stepping task for a duration of 7 weeks. Motor performance during the stepping task was assessed under single and dual-task conditions. Concurrent cortical activation in the prefrontal cortex (PFC) was measured using functional near-infrared spectroscopy (fNIRS). Additionally, structural and functional magnetic resonance imaging (MRI) was conducted during a similar stepping task at the beginning of the trial. The results indicate that adolescents with DCD performed similarly to their peers with lower levels of fitness in the novel stepping task and demonstrated the ability to learn and improve motor performance. Both groups showed significant improvements in both tasks and under single- and dual-task conditions at post-intervention and follow-up compared to baseline. While both groups initially made more errors in the Stroop task under dual-task conditions, at follow-up, a significant difference between single- and dual-task conditions was observed only in the DCD group. Notably, differences in prefrontal activation patterns between the groups emerged at different time points and task conditions. Adolescents with DCD exhibited distinct prefrontal activation responses during the learning and performance of a motor task, particularly when complexity was increased by concurrent cognitive tasks. Furthermore, a relationship was observed between MRI brain structure and function measures and initial performance in the novel stepping task. Overall, these findings suggest that strategies that address task and environmental complexities, while simultaneously enhancing brain activity through a range of tasks, offer opportunities to increase the participation of adolescents with low fitness in physical activity and sports.
format Online
Article
Text
id pubmed-10323432
institution National Center for Biotechnology Information
language English
publishDate 2023
publisher Frontiers Media S.A.
record_format MEDLINE/PubMed
spelling pubmed-103234322023-07-07 Motor learning in developmental coordination disorder: behavioral and neuroimaging study Al-Yahya, Emad Esser, Patrick Weedon, Benjamin D. Joshi, Shawn Liu, Yan-Ci Springett, Daniella N. Salvan, Piergiorgio Meaney, Andy Collett, Johnny Inacio, Mario Delextrat, Anne Kemp, Steve Ward, Tomas Izadi, Hooshang Johansen-Berg, Heidi Ayaz, Hasan Dawes, Helen Front Neurosci Neuroscience Developmental coordination disorder (DCD) is characterized by motor learning deficits that are poorly understood within whole-body activities context. Here we present results of one of the largest non-randomized interventional trials combining brain imaging and motion capture techniques to examine motor skill acquisition and its underpinning mechanisms in adolescents with and without DCD. A total of 86 adolescents with low fitness levels (including 48 with DCD) were trained on a novel stepping task for a duration of 7 weeks. Motor performance during the stepping task was assessed under single and dual-task conditions. Concurrent cortical activation in the prefrontal cortex (PFC) was measured using functional near-infrared spectroscopy (fNIRS). Additionally, structural and functional magnetic resonance imaging (MRI) was conducted during a similar stepping task at the beginning of the trial. The results indicate that adolescents with DCD performed similarly to their peers with lower levels of fitness in the novel stepping task and demonstrated the ability to learn and improve motor performance. Both groups showed significant improvements in both tasks and under single- and dual-task conditions at post-intervention and follow-up compared to baseline. While both groups initially made more errors in the Stroop task under dual-task conditions, at follow-up, a significant difference between single- and dual-task conditions was observed only in the DCD group. Notably, differences in prefrontal activation patterns between the groups emerged at different time points and task conditions. Adolescents with DCD exhibited distinct prefrontal activation responses during the learning and performance of a motor task, particularly when complexity was increased by concurrent cognitive tasks. Furthermore, a relationship was observed between MRI brain structure and function measures and initial performance in the novel stepping task. Overall, these findings suggest that strategies that address task and environmental complexities, while simultaneously enhancing brain activity through a range of tasks, offer opportunities to increase the participation of adolescents with low fitness in physical activity and sports. Frontiers Media S.A. 2023-06-22 /pmc/articles/PMC10323432/ /pubmed/37425016 http://dx.doi.org/10.3389/fnins.2023.1187790 Text en Copyright © 2023 Al-Yahya, Esser, Weedon, Joshi, Liu, Springett, Salvan, Meaney, Collett, Inacio, Delextrat, Kemp, Ward, Izadi, Johansen-Berg, Ayaz and Dawes. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Neuroscience
Al-Yahya, Emad
Esser, Patrick
Weedon, Benjamin D.
Joshi, Shawn
Liu, Yan-Ci
Springett, Daniella N.
Salvan, Piergiorgio
Meaney, Andy
Collett, Johnny
Inacio, Mario
Delextrat, Anne
Kemp, Steve
Ward, Tomas
Izadi, Hooshang
Johansen-Berg, Heidi
Ayaz, Hasan
Dawes, Helen
Motor learning in developmental coordination disorder: behavioral and neuroimaging study
title Motor learning in developmental coordination disorder: behavioral and neuroimaging study
title_full Motor learning in developmental coordination disorder: behavioral and neuroimaging study
title_fullStr Motor learning in developmental coordination disorder: behavioral and neuroimaging study
title_full_unstemmed Motor learning in developmental coordination disorder: behavioral and neuroimaging study
title_short Motor learning in developmental coordination disorder: behavioral and neuroimaging study
title_sort motor learning in developmental coordination disorder: behavioral and neuroimaging study
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10323432/
https://www.ncbi.nlm.nih.gov/pubmed/37425016
http://dx.doi.org/10.3389/fnins.2023.1187790
work_keys_str_mv AT alyahyaemad motorlearningindevelopmentalcoordinationdisorderbehavioralandneuroimagingstudy
AT esserpatrick motorlearningindevelopmentalcoordinationdisorderbehavioralandneuroimagingstudy
AT weedonbenjamind motorlearningindevelopmentalcoordinationdisorderbehavioralandneuroimagingstudy
AT joshishawn motorlearningindevelopmentalcoordinationdisorderbehavioralandneuroimagingstudy
AT liuyanci motorlearningindevelopmentalcoordinationdisorderbehavioralandneuroimagingstudy
AT springettdaniellan motorlearningindevelopmentalcoordinationdisorderbehavioralandneuroimagingstudy
AT salvanpiergiorgio motorlearningindevelopmentalcoordinationdisorderbehavioralandneuroimagingstudy
AT meaneyandy motorlearningindevelopmentalcoordinationdisorderbehavioralandneuroimagingstudy
AT collettjohnny motorlearningindevelopmentalcoordinationdisorderbehavioralandneuroimagingstudy
AT inaciomario motorlearningindevelopmentalcoordinationdisorderbehavioralandneuroimagingstudy
AT delextratanne motorlearningindevelopmentalcoordinationdisorderbehavioralandneuroimagingstudy
AT kempsteve motorlearningindevelopmentalcoordinationdisorderbehavioralandneuroimagingstudy
AT wardtomas motorlearningindevelopmentalcoordinationdisorderbehavioralandneuroimagingstudy
AT izadihooshang motorlearningindevelopmentalcoordinationdisorderbehavioralandneuroimagingstudy
AT johansenbergheidi motorlearningindevelopmentalcoordinationdisorderbehavioralandneuroimagingstudy
AT ayazhasan motorlearningindevelopmentalcoordinationdisorderbehavioralandneuroimagingstudy
AT daweshelen motorlearningindevelopmentalcoordinationdisorderbehavioralandneuroimagingstudy