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Motor deficits correlate with resting state motor network connectivity in patients with brain tumours

While a tumour in or abutting primary motor cortex leads to motor weakness, how tumours elsewhere in the frontal or parietal lobes affect functional connectivity in a weak patient is less clear. We hypothesized that diminished functional connectivity in a distributed network of motor centres would c...

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Autores principales: Otten, Marc L., Mikell, Charles B., Youngerman, Brett E., Liston, Conor, Sisti, Michael B., Bruce, Jeffrey N., Small, Scott A., McKhann, Guy M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2012
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3326259/
https://www.ncbi.nlm.nih.gov/pubmed/22408270
http://dx.doi.org/10.1093/brain/aws041
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author Otten, Marc L.
Mikell, Charles B.
Youngerman, Brett E.
Liston, Conor
Sisti, Michael B.
Bruce, Jeffrey N.
Small, Scott A.
McKhann, Guy M.
author_facet Otten, Marc L.
Mikell, Charles B.
Youngerman, Brett E.
Liston, Conor
Sisti, Michael B.
Bruce, Jeffrey N.
Small, Scott A.
McKhann, Guy M.
author_sort Otten, Marc L.
collection PubMed
description While a tumour in or abutting primary motor cortex leads to motor weakness, how tumours elsewhere in the frontal or parietal lobes affect functional connectivity in a weak patient is less clear. We hypothesized that diminished functional connectivity in a distributed network of motor centres would correlate with motor weakness in subjects with brain masses. Furthermore, we hypothesized that interhemispheric connections would be most vulnerable to subtle disruptions in functional connectivity. We used task-free functional magnetic resonance imaging connectivity to probe motor networks in control subjects and patients with brain tumours (n = 22). Using a control dataset, we developed a method for automated detection of key nodes in the motor network, including the primary motor cortex, supplementary motor area, premotor area and superior parietal lobule, based on the anatomic location of the hand-motor knob in the primary motor cortex. We then calculated functional connectivity between motor network nodes in control subjects, as well as patients with and without brain masses. We used this information to construct weighted, undirected graphs, which were then compared to variables of interest, including performance on a motor task, the grooved pegboard. Strong connectivity was observed within the identified motor networks between all nodes bilaterally, and especially between the primary motor cortex and supplementary motor area. Reduced connectivity was observed in subjects with motor weakness versus subjects with normal strength (P < 0.001). This difference was driven mostly by decreases in interhemispheric connectivity between the primary motor cortices (P < 0.05) and between the left primary motor cortex and the right premotor area (P < 0.05), as well as other premotor area connections. In the subjects without motor weakness, however, performance on the grooved pegboard did not relate to interhemispheric connectivity, but rather was inversely correlated with connectivity between the left premotor area and left supplementary motor area, for both the left and the right hands (P < 0.01). Finally, two subjects who experienced severe weakness following surgery for their brain tumours were followed longitudinally, and the subject who recovered showed reconstitution of her motor network at follow-up. The subject who was persistently weak did not reconstitute his motor network. Motor weakness in subjects with brain tumours that do not involve primary motor structures is associated with decreased connectivity within motor functional networks, particularly interhemispheric connections. Motor networks become weaker as the subjects become weaker, and may become strong again during motor recovery.
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spelling pubmed-33262592012-04-16 Motor deficits correlate with resting state motor network connectivity in patients with brain tumours Otten, Marc L. Mikell, Charles B. Youngerman, Brett E. Liston, Conor Sisti, Michael B. Bruce, Jeffrey N. Small, Scott A. McKhann, Guy M. Brain Original Articles While a tumour in or abutting primary motor cortex leads to motor weakness, how tumours elsewhere in the frontal or parietal lobes affect functional connectivity in a weak patient is less clear. We hypothesized that diminished functional connectivity in a distributed network of motor centres would correlate with motor weakness in subjects with brain masses. Furthermore, we hypothesized that interhemispheric connections would be most vulnerable to subtle disruptions in functional connectivity. We used task-free functional magnetic resonance imaging connectivity to probe motor networks in control subjects and patients with brain tumours (n = 22). Using a control dataset, we developed a method for automated detection of key nodes in the motor network, including the primary motor cortex, supplementary motor area, premotor area and superior parietal lobule, based on the anatomic location of the hand-motor knob in the primary motor cortex. We then calculated functional connectivity between motor network nodes in control subjects, as well as patients with and without brain masses. We used this information to construct weighted, undirected graphs, which were then compared to variables of interest, including performance on a motor task, the grooved pegboard. Strong connectivity was observed within the identified motor networks between all nodes bilaterally, and especially between the primary motor cortex and supplementary motor area. Reduced connectivity was observed in subjects with motor weakness versus subjects with normal strength (P < 0.001). This difference was driven mostly by decreases in interhemispheric connectivity between the primary motor cortices (P < 0.05) and between the left primary motor cortex and the right premotor area (P < 0.05), as well as other premotor area connections. In the subjects without motor weakness, however, performance on the grooved pegboard did not relate to interhemispheric connectivity, but rather was inversely correlated with connectivity between the left premotor area and left supplementary motor area, for both the left and the right hands (P < 0.01). Finally, two subjects who experienced severe weakness following surgery for their brain tumours were followed longitudinally, and the subject who recovered showed reconstitution of her motor network at follow-up. The subject who was persistently weak did not reconstitute his motor network. Motor weakness in subjects with brain tumours that do not involve primary motor structures is associated with decreased connectivity within motor functional networks, particularly interhemispheric connections. Motor networks become weaker as the subjects become weaker, and may become strong again during motor recovery. Oxford University Press 2012-04 2012-02-08 /pmc/articles/PMC3326259/ /pubmed/22408270 http://dx.doi.org/10.1093/brain/aws041 Text en © The Author (2012). Published by Oxford University Press on behalf of the Guarantors of Brain. http://creativecommons.org/licenses/by-nc/3.0 This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/3.0), which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Original Articles
Otten, Marc L.
Mikell, Charles B.
Youngerman, Brett E.
Liston, Conor
Sisti, Michael B.
Bruce, Jeffrey N.
Small, Scott A.
McKhann, Guy M.
Motor deficits correlate with resting state motor network connectivity in patients with brain tumours
title Motor deficits correlate with resting state motor network connectivity in patients with brain tumours
title_full Motor deficits correlate with resting state motor network connectivity in patients with brain tumours
title_fullStr Motor deficits correlate with resting state motor network connectivity in patients with brain tumours
title_full_unstemmed Motor deficits correlate with resting state motor network connectivity in patients with brain tumours
title_short Motor deficits correlate with resting state motor network connectivity in patients with brain tumours
title_sort motor deficits correlate with resting state motor network connectivity in patients with brain tumours
topic Original Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3326259/
https://www.ncbi.nlm.nih.gov/pubmed/22408270
http://dx.doi.org/10.1093/brain/aws041
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