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Brain connectivity during simulated balance in older adults with and without Parkinson's disease

Individuals with Parkinson’s disease often experience postural instability, a debilitating and largely treatment-resistant symptom. A better understanding of the neural substrates contributing to postural instability could lead to more effective treatments. Constraints of current functional neuroima...

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Autores principales: Pasman, Elizabeth P., McKeown, Martin J., Garg, Saurabh, Cleworth, Taylor W., Bloem, Bastiaan R., Inglis, J. Timothy, Carpenter, Mark G.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Elsevier 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8102637/
https://www.ncbi.nlm.nih.gov/pubmed/34215147
http://dx.doi.org/10.1016/j.nicl.2021.102676
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author Pasman, Elizabeth P.
McKeown, Martin J.
Garg, Saurabh
Cleworth, Taylor W.
Bloem, Bastiaan R.
Inglis, J. Timothy
Carpenter, Mark G.
author_facet Pasman, Elizabeth P.
McKeown, Martin J.
Garg, Saurabh
Cleworth, Taylor W.
Bloem, Bastiaan R.
Inglis, J. Timothy
Carpenter, Mark G.
author_sort Pasman, Elizabeth P.
collection PubMed
description Individuals with Parkinson’s disease often experience postural instability, a debilitating and largely treatment-resistant symptom. A better understanding of the neural substrates contributing to postural instability could lead to more effective treatments. Constraints of current functional neuroimaging techniques, such as the horizontal orientation of most MRI scanners (forcing participants to lie supine), complicates investigating cortical and subcortical activation patterns and connectivity networks involved in healthy and parkinsonian balance control. In this cross-sectional study, we utilized a newly-validated MRI-compatible balance simulator (based on an inverted pendulum) that enabled participants to perform balance-relevant tasks while supine in the scanner. We utilized functional MRI to explore effective connectivity underlying static and dynamic balance control in healthy older adults (n = 17) and individuals with Parkinson’s disease while on medication (n = 17). Participants performed four tasks within the scanner with eyes closed: resting, proprioceptive tracking of passive ankle movement, static balancing of the simulator, and dynamic responses to random perturbations of the simulator. All analyses were done in the participant's native space without spatial transformation to a common template. Effective connectivity between 57 regions of interest was computed using a Bayesian Network learning approach with false discovery rate set to 5%. The first 12 principal components of the connection weights, binomial logistic regression, and cross-validation were used to create 4 separate models: contrasting static balancing vs {rest, proprioception} and dynamic balancing vs {rest, proprioception} for both controls and individuals with Parkinson’s disease. In order to directly compare relevant connections between controls and individuals with Parkinson’s disease, we used connections relevant for predicting a task in either controls or individuals with Parkinson’s disease in logistic regression with Least Absolute Shrinkage and Selection Operator regularization. During dynamic balancing, we observed decreased connectivity between different motor areas and increased connectivity from the brainstem to several cortical and subcortical areas in controls, while individuals with Parkinson’s disease showed increased connectivity associated with motor and parietal areas, and decreased connectivity from brainstem to other subcortical areas. No significant models were found for static balancing in either group. Our results support the notion that dynamic balance control in individuals with Parkinson’s disease relies more on cortical motor areas compared to healthy older adults, who show a preference of subcortical control during dynamic balancing.
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spelling pubmed-81026372021-05-14 Brain connectivity during simulated balance in older adults with and without Parkinson's disease Pasman, Elizabeth P. McKeown, Martin J. Garg, Saurabh Cleworth, Taylor W. Bloem, Bastiaan R. Inglis, J. Timothy Carpenter, Mark G. Neuroimage Clin Regular Article Individuals with Parkinson’s disease often experience postural instability, a debilitating and largely treatment-resistant symptom. A better understanding of the neural substrates contributing to postural instability could lead to more effective treatments. Constraints of current functional neuroimaging techniques, such as the horizontal orientation of most MRI scanners (forcing participants to lie supine), complicates investigating cortical and subcortical activation patterns and connectivity networks involved in healthy and parkinsonian balance control. In this cross-sectional study, we utilized a newly-validated MRI-compatible balance simulator (based on an inverted pendulum) that enabled participants to perform balance-relevant tasks while supine in the scanner. We utilized functional MRI to explore effective connectivity underlying static and dynamic balance control in healthy older adults (n = 17) and individuals with Parkinson’s disease while on medication (n = 17). Participants performed four tasks within the scanner with eyes closed: resting, proprioceptive tracking of passive ankle movement, static balancing of the simulator, and dynamic responses to random perturbations of the simulator. All analyses were done in the participant's native space without spatial transformation to a common template. Effective connectivity between 57 regions of interest was computed using a Bayesian Network learning approach with false discovery rate set to 5%. The first 12 principal components of the connection weights, binomial logistic regression, and cross-validation were used to create 4 separate models: contrasting static balancing vs {rest, proprioception} and dynamic balancing vs {rest, proprioception} for both controls and individuals with Parkinson’s disease. In order to directly compare relevant connections between controls and individuals with Parkinson’s disease, we used connections relevant for predicting a task in either controls or individuals with Parkinson’s disease in logistic regression with Least Absolute Shrinkage and Selection Operator regularization. During dynamic balancing, we observed decreased connectivity between different motor areas and increased connectivity from the brainstem to several cortical and subcortical areas in controls, while individuals with Parkinson’s disease showed increased connectivity associated with motor and parietal areas, and decreased connectivity from brainstem to other subcortical areas. No significant models were found for static balancing in either group. Our results support the notion that dynamic balance control in individuals with Parkinson’s disease relies more on cortical motor areas compared to healthy older adults, who show a preference of subcortical control during dynamic balancing. Elsevier 2021-04-16 /pmc/articles/PMC8102637/ /pubmed/34215147 http://dx.doi.org/10.1016/j.nicl.2021.102676 Text en © 2021 The Author(s) https://creativecommons.org/licenses/by-nc-nd/4.0/This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
spellingShingle Regular Article
Pasman, Elizabeth P.
McKeown, Martin J.
Garg, Saurabh
Cleworth, Taylor W.
Bloem, Bastiaan R.
Inglis, J. Timothy
Carpenter, Mark G.
Brain connectivity during simulated balance in older adults with and without Parkinson's disease
title Brain connectivity during simulated balance in older adults with and without Parkinson's disease
title_full Brain connectivity during simulated balance in older adults with and without Parkinson's disease
title_fullStr Brain connectivity during simulated balance in older adults with and without Parkinson's disease
title_full_unstemmed Brain connectivity during simulated balance in older adults with and without Parkinson's disease
title_short Brain connectivity during simulated balance in older adults with and without Parkinson's disease
title_sort brain connectivity during simulated balance in older adults with and without parkinson's disease
topic Regular Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8102637/
https://www.ncbi.nlm.nih.gov/pubmed/34215147
http://dx.doi.org/10.1016/j.nicl.2021.102676
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