Evaluating the Abnormality of Bilateral Motor Cortex Activity in Subacute Stroke Patients Executing a Unimanual Motor Task With Increasing Demand on Precision

Abnormal contralesional M1 activity is consistently reported in patients with compromised upper limb and hand function after stroke. The underlying mechanisms and functional implications of this activity are not clear, which hampers the development of treatment strategies targeting this brain area....

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Main Authors: Kate Pirog Revill, Deborah A. Barany, Isabelle Vernon, Stephanie Rellick, Alexandra Caliban, Julie Tran, Samir R. Belagaje, Fadi Nahab, Marc W. Haut, Cathrin M. Buetefisch
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-05-01
Series:Frontiers in Neurology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fneur.2022.836716/full
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author Kate Pirog Revill
Deborah A. Barany
Isabelle Vernon
Stephanie Rellick
Alexandra Caliban
Julie Tran
Samir R. Belagaje
Fadi Nahab
Marc W. Haut
Marc W. Haut
Marc W. Haut
Cathrin M. Buetefisch
Cathrin M. Buetefisch
Cathrin M. Buetefisch
author_facet Kate Pirog Revill
Deborah A. Barany
Isabelle Vernon
Stephanie Rellick
Alexandra Caliban
Julie Tran
Samir R. Belagaje
Fadi Nahab
Marc W. Haut
Marc W. Haut
Marc W. Haut
Cathrin M. Buetefisch
Cathrin M. Buetefisch
Cathrin M. Buetefisch
author_sort Kate Pirog Revill
collection DOAJ
description Abnormal contralesional M1 activity is consistently reported in patients with compromised upper limb and hand function after stroke. The underlying mechanisms and functional implications of this activity are not clear, which hampers the development of treatment strategies targeting this brain area. The goal of the present study was to determine the extent to which contralesional M1 activity can be explained by the demand of a motor task, given recent evidence for increasing ipsilateral M1 activity with increasing demand in healthy age-matched controls. We hypothesized that higher activity in contralesional M1 is related to greater demand on precision in a hand motor task. fMRI data were collected from 19 patients with ischemic stroke affecting hand function in the subacute recovery phase and 31 healthy, right-handed, age-matched controls. The hand motor task was designed to parametrically modulate the demand on movement precision. Electromyography data confirmed strictly unilateral task performance by all participants. Patients showed significant impairment relative to controls in their ability to perform the task in the fMRI scanner. However, patients and controls responded similarly to an increase in demand for precision, with better performance for larger targets and poorer performance for smaller targets. Patients did not show evidence of elevated ipsilesional or contralesional M1 blood oxygenation level-dependent (BOLD) activation relative to healthy controls and mean BOLD activation levels were not elevated for patients with poorer performance relative to patients with better task performance. While both patients and healthy controls showed demand-dependent increases in BOLD activation in both ipsilesional/contralateral and contralesional/ipsilateral hemispheres, patients with stroke were less likely to show evidence of a linear relationship between the demand on precision and BOLD activation in contralesional M1 than healthy controls. Taken together, the findings suggest that task demand affects the BOLD response in contralesional M1 in patients with stroke, though perhaps less strongly than in healthy controls. This has implications for the interpretation of reported abnormal bilateral M1 activation in patients with stroke because in addition to contralesional M1 reorganization processes it could be partially related to a response to the relatively higher demand of a motor task when completed by patients rather than by healthy controls.
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spelling doaj.art-2a286e330a9a405291e57961c66a569d2022-12-22T00:24:14ZengFrontiers Media S.A.Frontiers in Neurology1664-22952022-05-011310.3389/fneur.2022.836716836716Evaluating the Abnormality of Bilateral Motor Cortex Activity in Subacute Stroke Patients Executing a Unimanual Motor Task With Increasing Demand on PrecisionKate Pirog Revill0Deborah A. Barany1Isabelle Vernon2Stephanie Rellick3Alexandra Caliban4Julie Tran5Samir R. Belagaje6Fadi Nahab7Marc W. Haut8Marc W. Haut9Marc W. Haut10Cathrin M. Buetefisch11Cathrin M. Buetefisch12Cathrin M. Buetefisch13Department of Psychology, Emory University, Atlanta, GA, United StatesDepartment of Neurology, Emory University, Atlanta, GA, United StatesDepartment of Neurology, Emory University, Atlanta, GA, United StatesDepartment of Behavioral Medicine and Psychiatry, Rockefeller Neuroscience Institute, West Virginia University, Morgantown, WV, United StatesDepartment of Neurology, Emory University, Atlanta, GA, United StatesDepartment of Neurology, Emory University, Atlanta, GA, United StatesDepartment of Neurology, Emory University, Atlanta, GA, United StatesDepartment of Neurology, Emory University, Atlanta, GA, United StatesDepartment of Behavioral Medicine and Psychiatry, Rockefeller Neuroscience Institute, West Virginia University, Morgantown, WV, United StatesDepartment of Neurology, Rockefeller Neuroscience Institute, West Virginia University, Morgantown, WV, United StatesDepartment of Radiology, Rockefeller Neuroscience Institute, West Virginia University, Morgantown, WV, United StatesDepartment of Neurology, Emory University, Atlanta, GA, United StatesDepartment of Rehabilitation Medicine, Emory University, Atlanta, GA, United StatesDepartment of Radiology, Emory University, Atlanta, GA, United StatesAbnormal contralesional M1 activity is consistently reported in patients with compromised upper limb and hand function after stroke. The underlying mechanisms and functional implications of this activity are not clear, which hampers the development of treatment strategies targeting this brain area. The goal of the present study was to determine the extent to which contralesional M1 activity can be explained by the demand of a motor task, given recent evidence for increasing ipsilateral M1 activity with increasing demand in healthy age-matched controls. We hypothesized that higher activity in contralesional M1 is related to greater demand on precision in a hand motor task. fMRI data were collected from 19 patients with ischemic stroke affecting hand function in the subacute recovery phase and 31 healthy, right-handed, age-matched controls. The hand motor task was designed to parametrically modulate the demand on movement precision. Electromyography data confirmed strictly unilateral task performance by all participants. Patients showed significant impairment relative to controls in their ability to perform the task in the fMRI scanner. However, patients and controls responded similarly to an increase in demand for precision, with better performance for larger targets and poorer performance for smaller targets. Patients did not show evidence of elevated ipsilesional or contralesional M1 blood oxygenation level-dependent (BOLD) activation relative to healthy controls and mean BOLD activation levels were not elevated for patients with poorer performance relative to patients with better task performance. While both patients and healthy controls showed demand-dependent increases in BOLD activation in both ipsilesional/contralateral and contralesional/ipsilateral hemispheres, patients with stroke were less likely to show evidence of a linear relationship between the demand on precision and BOLD activation in contralesional M1 than healthy controls. Taken together, the findings suggest that task demand affects the BOLD response in contralesional M1 in patients with stroke, though perhaps less strongly than in healthy controls. This has implications for the interpretation of reported abnormal bilateral M1 activation in patients with stroke because in addition to contralesional M1 reorganization processes it could be partially related to a response to the relatively higher demand of a motor task when completed by patients rather than by healthy controls.https://www.frontiersin.org/articles/10.3389/fneur.2022.836716/fullfMRIstrokemotor cortexhand functionmotor recovery-cerebral infarct
spellingShingle Kate Pirog Revill
Deborah A. Barany
Isabelle Vernon
Stephanie Rellick
Alexandra Caliban
Julie Tran
Samir R. Belagaje
Fadi Nahab
Marc W. Haut
Marc W. Haut
Marc W. Haut
Cathrin M. Buetefisch
Cathrin M. Buetefisch
Cathrin M. Buetefisch
Evaluating the Abnormality of Bilateral Motor Cortex Activity in Subacute Stroke Patients Executing a Unimanual Motor Task With Increasing Demand on Precision
Frontiers in Neurology
fMRI
stroke
motor cortex
hand function
motor recovery-cerebral infarct
title Evaluating the Abnormality of Bilateral Motor Cortex Activity in Subacute Stroke Patients Executing a Unimanual Motor Task With Increasing Demand on Precision
title_full Evaluating the Abnormality of Bilateral Motor Cortex Activity in Subacute Stroke Patients Executing a Unimanual Motor Task With Increasing Demand on Precision
title_fullStr Evaluating the Abnormality of Bilateral Motor Cortex Activity in Subacute Stroke Patients Executing a Unimanual Motor Task With Increasing Demand on Precision
title_full_unstemmed Evaluating the Abnormality of Bilateral Motor Cortex Activity in Subacute Stroke Patients Executing a Unimanual Motor Task With Increasing Demand on Precision
title_short Evaluating the Abnormality of Bilateral Motor Cortex Activity in Subacute Stroke Patients Executing a Unimanual Motor Task With Increasing Demand on Precision
title_sort evaluating the abnormality of bilateral motor cortex activity in subacute stroke patients executing a unimanual motor task with increasing demand on precision
topic fMRI
stroke
motor cortex
hand function
motor recovery-cerebral infarct
url https://www.frontiersin.org/articles/10.3389/fneur.2022.836716/full
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