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Chronic musculoskeletal impairment is associated with alterations in brain regions responsible for the production and perception of movement

KEY POINTS: Massive irreparable rotator cuff tear was used as a model to study the impact of chronic pain and motor impairment on the motor systems of the human brain using magnetic resonance imaging. Patients show markers of lower grey/white matter integrity and lower functional connectivity compar...

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Autores principales: Conboy, Veronica, Edwards, Carl, Ainsworth, Roberta, Natusch, Douglas, Burcham, Claire, Danisment, Buse, Khot, Sharmila, Seymour, Richard, Larcombe, Stephanie J., Tracey, Irene, Kolasinski, James
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8132184/
https://www.ncbi.nlm.nih.gov/pubmed/33675033
http://dx.doi.org/10.1113/JP281273
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author Conboy, Veronica
Edwards, Carl
Ainsworth, Roberta
Natusch, Douglas
Burcham, Claire
Danisment, Buse
Khot, Sharmila
Seymour, Richard
Larcombe, Stephanie J.
Tracey, Irene
Kolasinski, James
author_facet Conboy, Veronica
Edwards, Carl
Ainsworth, Roberta
Natusch, Douglas
Burcham, Claire
Danisment, Buse
Khot, Sharmila
Seymour, Richard
Larcombe, Stephanie J.
Tracey, Irene
Kolasinski, James
author_sort Conboy, Veronica
collection PubMed
description KEY POINTS: Massive irreparable rotator cuff tear was used as a model to study the impact of chronic pain and motor impairment on the motor systems of the human brain using magnetic resonance imaging. Patients show markers of lower grey/white matter integrity and lower functional connectivity compared with control participants in regions responsible for movement and the perception of visual movement and body shape. An independent cohort of patients showed relative deficits in the perception of visual motion and hand laterality compared with an age‐matched control group. These data support the hypothesis that the structure and function of the motor control system differs in patients who have experienced chronic motor impairment. This work also raises a new hypothesis, supported by neuroimaging and behaviour, that a loss of motor function could also be associated with off‐target effects, namely a reduced ability to perceive motion and body form. ABSTRACT: Changes in the way we move can induce changes in the brain, yet we know little of such plasticity in relation to musculoskeletal diseases. Here we use massive irreparable rotator cuff tear as a model to study the impact of chronic motor impairment and pain on the human brain. Cuff tear destabilises the shoulder, impairing upper‐limb function in overhead and load‐bearing tasks. We used neuroimaging and behavioural testing to investigate how brain structure and function differed in cuff tear patients and controls (imaging: 21 patients, age 76.3 ± 7.68; 18 controls, age 74.9 ± 6.59; behaviour: 13 patients, age 75.5 ± 10.2; 11 controls, age 73.4 ± 5.01). We observed lower grey matter density and cortical thickness in cuff tear patients in the postcentral gyrus, inferior parietal lobule, temporal‐parietal junction and the pulvinar – areas implicated in somatosensation, reach/grasp and body form perception. In patients we also observed lower functional connectivity between the motor network and the middle temporal visual cortex (MT), a region involved in visual motion perception. Lower white matter integrity was observed in patients in the inferior fronto‐occipital/longitudinal fasciculi. We investigated the cognitive domains associated with the brain regions identified. Patients exhibited relative impairment in visual body judgements and the perception of biological/global motion. These data support our initial hypothesis that cuff tear is associated with differences in the brain's motor control regions in comparison with unaffected individuals. Moreover, our combination of neuroimaging and behavioural data raises a new hypothesis that chronic motor impairment is associated with an altered perception of visual motion and body form.
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spelling pubmed-81321842021-05-21 Chronic musculoskeletal impairment is associated with alterations in brain regions responsible for the production and perception of movement Conboy, Veronica Edwards, Carl Ainsworth, Roberta Natusch, Douglas Burcham, Claire Danisment, Buse Khot, Sharmila Seymour, Richard Larcombe, Stephanie J. Tracey, Irene Kolasinski, James J Physiol Neuroscience KEY POINTS: Massive irreparable rotator cuff tear was used as a model to study the impact of chronic pain and motor impairment on the motor systems of the human brain using magnetic resonance imaging. Patients show markers of lower grey/white matter integrity and lower functional connectivity compared with control participants in regions responsible for movement and the perception of visual movement and body shape. An independent cohort of patients showed relative deficits in the perception of visual motion and hand laterality compared with an age‐matched control group. These data support the hypothesis that the structure and function of the motor control system differs in patients who have experienced chronic motor impairment. This work also raises a new hypothesis, supported by neuroimaging and behaviour, that a loss of motor function could also be associated with off‐target effects, namely a reduced ability to perceive motion and body form. ABSTRACT: Changes in the way we move can induce changes in the brain, yet we know little of such plasticity in relation to musculoskeletal diseases. Here we use massive irreparable rotator cuff tear as a model to study the impact of chronic motor impairment and pain on the human brain. Cuff tear destabilises the shoulder, impairing upper‐limb function in overhead and load‐bearing tasks. We used neuroimaging and behavioural testing to investigate how brain structure and function differed in cuff tear patients and controls (imaging: 21 patients, age 76.3 ± 7.68; 18 controls, age 74.9 ± 6.59; behaviour: 13 patients, age 75.5 ± 10.2; 11 controls, age 73.4 ± 5.01). We observed lower grey matter density and cortical thickness in cuff tear patients in the postcentral gyrus, inferior parietal lobule, temporal‐parietal junction and the pulvinar – areas implicated in somatosensation, reach/grasp and body form perception. In patients we also observed lower functional connectivity between the motor network and the middle temporal visual cortex (MT), a region involved in visual motion perception. Lower white matter integrity was observed in patients in the inferior fronto‐occipital/longitudinal fasciculi. We investigated the cognitive domains associated with the brain regions identified. Patients exhibited relative impairment in visual body judgements and the perception of biological/global motion. These data support our initial hypothesis that cuff tear is associated with differences in the brain's motor control regions in comparison with unaffected individuals. Moreover, our combination of neuroimaging and behavioural data raises a new hypothesis that chronic motor impairment is associated with an altered perception of visual motion and body form. John Wiley and Sons Inc. 2021-03-23 2021-04-15 /pmc/articles/PMC8132184/ /pubmed/33675033 http://dx.doi.org/10.1113/JP281273 Text en © 2021 The Authors. The Journal of Physiology published by John Wiley & Sons Ltd on behalf of The Physiological Society https://creativecommons.org/licenses/by/4.0/This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
spellingShingle Neuroscience
Conboy, Veronica
Edwards, Carl
Ainsworth, Roberta
Natusch, Douglas
Burcham, Claire
Danisment, Buse
Khot, Sharmila
Seymour, Richard
Larcombe, Stephanie J.
Tracey, Irene
Kolasinski, James
Chronic musculoskeletal impairment is associated with alterations in brain regions responsible for the production and perception of movement
title Chronic musculoskeletal impairment is associated with alterations in brain regions responsible for the production and perception of movement
title_full Chronic musculoskeletal impairment is associated with alterations in brain regions responsible for the production and perception of movement
title_fullStr Chronic musculoskeletal impairment is associated with alterations in brain regions responsible for the production and perception of movement
title_full_unstemmed Chronic musculoskeletal impairment is associated with alterations in brain regions responsible for the production and perception of movement
title_short Chronic musculoskeletal impairment is associated with alterations in brain regions responsible for the production and perception of movement
title_sort chronic musculoskeletal impairment is associated with alterations in brain regions responsible for the production and perception of movement
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8132184/
https://www.ncbi.nlm.nih.gov/pubmed/33675033
http://dx.doi.org/10.1113/JP281273
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