Basal ganglia and cortical networks for sequential ordering and rhythm of complex movements

Voluntary actions require the concurrent engagement and coordinated control of complex temporal (e.g., rhythm) and ordinal motor processes. Using high-resolution functional magnetic resonance imaging (fMRI) and multi-voxel pattern analysis (MVPA), we sought to determine the degree to which these com...

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Main Authors: Bednark, Jeffery G., Campbell, Megan E. J., Cunnington, Ross
Format: Online
Language:English
Published: Frontiers Media S.A. 2015
Online Access:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4515550/
id pubmed-4515550
recordtype oai_dc
spelling pubmed-45155502015-08-17 Basal ganglia and cortical networks for sequential ordering and rhythm of complex movements Bednark, Jeffery G. Campbell, Megan E. J. Cunnington, Ross Neuroscience Voluntary actions require the concurrent engagement and coordinated control of complex temporal (e.g., rhythm) and ordinal motor processes. Using high-resolution functional magnetic resonance imaging (fMRI) and multi-voxel pattern analysis (MVPA), we sought to determine the degree to which these complex motor processes are dissociable in basal ganglia and cortical networks. We employed three different finger-tapping tasks that differed in the demand on the sequential temporal rhythm or sequential ordering of submovements. Our results demonstrate that sequential rhythm and sequential order tasks were partially dissociable based on activation differences. The sequential rhythm task activated a widespread network centered around the supplementary motor area (SMA) and basal-ganglia regions including the dorsomedial putamen and caudate nucleus, while the sequential order task preferentially activated a fronto-parietal network. There was also extensive overlap between sequential rhythm and sequential order tasks, with both tasks commonly activating bilateral premotor, supplementary motor, and superior/inferior parietal cortical regions, as well as regions of the caudate/putamen of the basal ganglia and the ventro-lateral thalamus. Importantly, within the cortical regions that were active for both complex movements, MVPA could accurately classify different patterns of activation for the sequential rhythm and sequential order tasks. In the basal ganglia, however, overlapping activation for the sequential rhythm and sequential order tasks, which was found in classic motor circuits of the putamen and ventro-lateral thalamus, could not be accurately differentiated by MVPA. Overall, our results highlight the convergent architecture of the motor system, where complex motor information that is spatially distributed in the cortex converges into a more compact representation in the basal ganglia. Frontiers Media S.A. 2015-07-27 /pmc/articles/PMC4515550/ /pubmed/26283945 http://dx.doi.org/10.3389/fnhum.2015.00421 Text en Copyright © 2015 Bednark, Campbell and Cunnington. http://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 and reproduction in other forums is permitted, provided the original author(s) or licensor 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.
repository_type Open Access Journal
institution_category Foreign Institution
institution US National Center for Biotechnology Information
building NCBI PubMed
collection Online Access
language English
format Online
author Bednark, Jeffery G.
Campbell, Megan E. J.
Cunnington, Ross
spellingShingle Bednark, Jeffery G.
Campbell, Megan E. J.
Cunnington, Ross
Basal ganglia and cortical networks for sequential ordering and rhythm of complex movements
author_facet Bednark, Jeffery G.
Campbell, Megan E. J.
Cunnington, Ross
author_sort Bednark, Jeffery G.
title Basal ganglia and cortical networks for sequential ordering and rhythm of complex movements
title_short Basal ganglia and cortical networks for sequential ordering and rhythm of complex movements
title_full Basal ganglia and cortical networks for sequential ordering and rhythm of complex movements
title_fullStr Basal ganglia and cortical networks for sequential ordering and rhythm of complex movements
title_full_unstemmed Basal ganglia and cortical networks for sequential ordering and rhythm of complex movements
title_sort basal ganglia and cortical networks for sequential ordering and rhythm of complex movements
description Voluntary actions require the concurrent engagement and coordinated control of complex temporal (e.g., rhythm) and ordinal motor processes. Using high-resolution functional magnetic resonance imaging (fMRI) and multi-voxel pattern analysis (MVPA), we sought to determine the degree to which these complex motor processes are dissociable in basal ganglia and cortical networks. We employed three different finger-tapping tasks that differed in the demand on the sequential temporal rhythm or sequential ordering of submovements. Our results demonstrate that sequential rhythm and sequential order tasks were partially dissociable based on activation differences. The sequential rhythm task activated a widespread network centered around the supplementary motor area (SMA) and basal-ganglia regions including the dorsomedial putamen and caudate nucleus, while the sequential order task preferentially activated a fronto-parietal network. There was also extensive overlap between sequential rhythm and sequential order tasks, with both tasks commonly activating bilateral premotor, supplementary motor, and superior/inferior parietal cortical regions, as well as regions of the caudate/putamen of the basal ganglia and the ventro-lateral thalamus. Importantly, within the cortical regions that were active for both complex movements, MVPA could accurately classify different patterns of activation for the sequential rhythm and sequential order tasks. In the basal ganglia, however, overlapping activation for the sequential rhythm and sequential order tasks, which was found in classic motor circuits of the putamen and ventro-lateral thalamus, could not be accurately differentiated by MVPA. Overall, our results highlight the convergent architecture of the motor system, where complex motor information that is spatially distributed in the cortex converges into a more compact representation in the basal ganglia.
publisher Frontiers Media S.A.
publishDate 2015
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4515550/
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