Distinguishing Distinct Neural Systems for Proximal vs Distal Upper Extremity Motor Control After Acute Stroke.


Journal

Neurology
ISSN: 1526-632X
Titre abrégé: Neurology
Pays: United States
ID NLM: 0401060

Informations de publication

Date de publication:
25 07 2023
Historique:
received: 27 11 2022
accepted: 31 03 2023
pmc-release: 25 07 2024
medline: 26 7 2023
pubmed: 3 6 2023
entrez: 2 6 2023
Statut: ppublish

Résumé

The classic and singular pattern of distal greater than proximal upper extremity motor deficits after acute stroke does not account for the distinct structural and functional organization of circuits for proximal and distal motor control in the healthy CNS. We hypothesized that separate proximal and distal upper extremity clinical syndromes after acute stroke could be distinguished and that patterns of neuroanatomical injury leading to these 2 syndromes would reflect their distinct organization in the intact CNS. Proximal and distal components of motor impairment (upper extremity Fugl-Meyer score) and strength (Shoulder Abduction Finger Extension score) were assessed in consecutively recruited patients within 7 days of acute stroke. Partial correlation analysis was used to assess the relationship between proximal and distal motor scores. Functional outcomes including the Box and Blocks Test (BBT), Barthel Index (BI), and modified Rankin scale (mRS) were examined in relation to proximal vs distal motor patterns of deficit. Voxel-based lesion-symptom mapping was used to identify regions of injury associated with proximal vs distal upper extremity motor deficits. A total of 141 consecutive patients (49% female) were assessed 4.0 ± 1.6 (mean ± SD) days after stroke onset. Separate proximal and distal upper extremity motor components were distinguishable after acute stroke ( These results highlight that proximal and distal upper extremity motor systems can be selectively injured by acute stroke, with dissociable deficits and functional consequences. Our findings emphasize how disruption of distinct motor systems can contribute to separable components of poststroke upper extremity hemiparesis.

Sections du résumé

BACKGROUND AND OBJECTIVES
The classic and singular pattern of distal greater than proximal upper extremity motor deficits after acute stroke does not account for the distinct structural and functional organization of circuits for proximal and distal motor control in the healthy CNS. We hypothesized that separate proximal and distal upper extremity clinical syndromes after acute stroke could be distinguished and that patterns of neuroanatomical injury leading to these 2 syndromes would reflect their distinct organization in the intact CNS.
METHODS
Proximal and distal components of motor impairment (upper extremity Fugl-Meyer score) and strength (Shoulder Abduction Finger Extension score) were assessed in consecutively recruited patients within 7 days of acute stroke. Partial correlation analysis was used to assess the relationship between proximal and distal motor scores. Functional outcomes including the Box and Blocks Test (BBT), Barthel Index (BI), and modified Rankin scale (mRS) were examined in relation to proximal vs distal motor patterns of deficit. Voxel-based lesion-symptom mapping was used to identify regions of injury associated with proximal vs distal upper extremity motor deficits.
RESULTS
A total of 141 consecutive patients (49% female) were assessed 4.0 ± 1.6 (mean ± SD) days after stroke onset. Separate proximal and distal upper extremity motor components were distinguishable after acute stroke (
DISCUSSION
These results highlight that proximal and distal upper extremity motor systems can be selectively injured by acute stroke, with dissociable deficits and functional consequences. Our findings emphasize how disruption of distinct motor systems can contribute to separable components of poststroke upper extremity hemiparesis.

Identifiants

pubmed: 37268437
pii: WNL.0000000000207417
doi: 10.1212/WNL.0000000000207417
pmc: PMC10435065
doi:

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, U.S. Gov't, Non-P.H.S. Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

e347-e357

Subventions

Organisme : NICHD NIH HHS
ID : R01 HD093694
Pays : United States

Commentaires et corrections

Type : CommentIn

Informations de copyright

Written work prepared by employees of the Federal Government as part of their official duties is, under the U.S. Copyright Act, a “work of the United States Government” for which copyright protection under Title 17 of the United States Code is not available. As such, copyright does not extend to the contributions of employees of the Federal Government.

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Auteurs

David J Lin (DJ)

From the Center for Neurotechnology and Neurorecovery (D.J.L., R.H., J.A.D., S.M., H.J., K.S.E., K.R., L.R.H.), Department of Neurology, Massachusetts General Hospital, Harvard Medical School; Division of Neurocritical Care (D.J.L., L.R.H.), Department of Neurology; Stroke Service (D.J.L., S.P.F., L.H.S., L.R.H.), Department of Neurology, Massachusetts General Hospital, Boston; VA RR&D Center for Neurorestoration and Neurotechnology (D.J.L., L.R.H.), Rehabilitation R&D Service, Department of VA Medical Center, Providence, RI; Division of Neurocritical Care (S.B.S.), Department of Neurology, Brigham and Women's Hospital, Harvard Medical School; Department of Occupational Therapy (H.J., K.S.E.), MGH Institute of Health Professions, Boston, MA; Department of Rehabilitation (P.B.), Exercise and Nutrition Sciences, University of Cincinnati College of Allied Health Sciences, OH; Department of Biostatistics (J.G.), Columbia University Mailman School of Public Health, New York, NY; Department of Occupational Therapy (J.R.), Massachusetts General Hospital, Boston; School of Engineering (L.R.H.), Brown University, Providence, RI; and Department of Neurology (S.C.C.), University of California, Los Angeles, California Rehabilitation Hospital. dlin7@mgh.harvard.edu.

Richard Hardstone (R)

From the Center for Neurotechnology and Neurorecovery (D.J.L., R.H., J.A.D., S.M., H.J., K.S.E., K.R., L.R.H.), Department of Neurology, Massachusetts General Hospital, Harvard Medical School; Division of Neurocritical Care (D.J.L., L.R.H.), Department of Neurology; Stroke Service (D.J.L., S.P.F., L.H.S., L.R.H.), Department of Neurology, Massachusetts General Hospital, Boston; VA RR&D Center for Neurorestoration and Neurotechnology (D.J.L., L.R.H.), Rehabilitation R&D Service, Department of VA Medical Center, Providence, RI; Division of Neurocritical Care (S.B.S.), Department of Neurology, Brigham and Women's Hospital, Harvard Medical School; Department of Occupational Therapy (H.J., K.S.E.), MGH Institute of Health Professions, Boston, MA; Department of Rehabilitation (P.B.), Exercise and Nutrition Sciences, University of Cincinnati College of Allied Health Sciences, OH; Department of Biostatistics (J.G.), Columbia University Mailman School of Public Health, New York, NY; Department of Occupational Therapy (J.R.), Massachusetts General Hospital, Boston; School of Engineering (L.R.H.), Brown University, Providence, RI; and Department of Neurology (S.C.C.), University of California, Los Angeles, California Rehabilitation Hospital.

Julie A DiCarlo (JA)

From the Center for Neurotechnology and Neurorecovery (D.J.L., R.H., J.A.D., S.M., H.J., K.S.E., K.R., L.R.H.), Department of Neurology, Massachusetts General Hospital, Harvard Medical School; Division of Neurocritical Care (D.J.L., L.R.H.), Department of Neurology; Stroke Service (D.J.L., S.P.F., L.H.S., L.R.H.), Department of Neurology, Massachusetts General Hospital, Boston; VA RR&D Center for Neurorestoration and Neurotechnology (D.J.L., L.R.H.), Rehabilitation R&D Service, Department of VA Medical Center, Providence, RI; Division of Neurocritical Care (S.B.S.), Department of Neurology, Brigham and Women's Hospital, Harvard Medical School; Department of Occupational Therapy (H.J., K.S.E.), MGH Institute of Health Professions, Boston, MA; Department of Rehabilitation (P.B.), Exercise and Nutrition Sciences, University of Cincinnati College of Allied Health Sciences, OH; Department of Biostatistics (J.G.), Columbia University Mailman School of Public Health, New York, NY; Department of Occupational Therapy (J.R.), Massachusetts General Hospital, Boston; School of Engineering (L.R.H.), Brown University, Providence, RI; and Department of Neurology (S.C.C.), University of California, Los Angeles, California Rehabilitation Hospital.

Sydney Mckiernan (S)

From the Center for Neurotechnology and Neurorecovery (D.J.L., R.H., J.A.D., S.M., H.J., K.S.E., K.R., L.R.H.), Department of Neurology, Massachusetts General Hospital, Harvard Medical School; Division of Neurocritical Care (D.J.L., L.R.H.), Department of Neurology; Stroke Service (D.J.L., S.P.F., L.H.S., L.R.H.), Department of Neurology, Massachusetts General Hospital, Boston; VA RR&D Center for Neurorestoration and Neurotechnology (D.J.L., L.R.H.), Rehabilitation R&D Service, Department of VA Medical Center, Providence, RI; Division of Neurocritical Care (S.B.S.), Department of Neurology, Brigham and Women's Hospital, Harvard Medical School; Department of Occupational Therapy (H.J., K.S.E.), MGH Institute of Health Professions, Boston, MA; Department of Rehabilitation (P.B.), Exercise and Nutrition Sciences, University of Cincinnati College of Allied Health Sciences, OH; Department of Biostatistics (J.G.), Columbia University Mailman School of Public Health, New York, NY; Department of Occupational Therapy (J.R.), Massachusetts General Hospital, Boston; School of Engineering (L.R.H.), Brown University, Providence, RI; and Department of Neurology (S.C.C.), University of California, Los Angeles, California Rehabilitation Hospital.

Samuel B Snider (SB)

From the Center for Neurotechnology and Neurorecovery (D.J.L., R.H., J.A.D., S.M., H.J., K.S.E., K.R., L.R.H.), Department of Neurology, Massachusetts General Hospital, Harvard Medical School; Division of Neurocritical Care (D.J.L., L.R.H.), Department of Neurology; Stroke Service (D.J.L., S.P.F., L.H.S., L.R.H.), Department of Neurology, Massachusetts General Hospital, Boston; VA RR&D Center for Neurorestoration and Neurotechnology (D.J.L., L.R.H.), Rehabilitation R&D Service, Department of VA Medical Center, Providence, RI; Division of Neurocritical Care (S.B.S.), Department of Neurology, Brigham and Women's Hospital, Harvard Medical School; Department of Occupational Therapy (H.J., K.S.E.), MGH Institute of Health Professions, Boston, MA; Department of Rehabilitation (P.B.), Exercise and Nutrition Sciences, University of Cincinnati College of Allied Health Sciences, OH; Department of Biostatistics (J.G.), Columbia University Mailman School of Public Health, New York, NY; Department of Occupational Therapy (J.R.), Massachusetts General Hospital, Boston; School of Engineering (L.R.H.), Brown University, Providence, RI; and Department of Neurology (S.C.C.), University of California, Los Angeles, California Rehabilitation Hospital.

Hannah Jacobs (H)

From the Center for Neurotechnology and Neurorecovery (D.J.L., R.H., J.A.D., S.M., H.J., K.S.E., K.R., L.R.H.), Department of Neurology, Massachusetts General Hospital, Harvard Medical School; Division of Neurocritical Care (D.J.L., L.R.H.), Department of Neurology; Stroke Service (D.J.L., S.P.F., L.H.S., L.R.H.), Department of Neurology, Massachusetts General Hospital, Boston; VA RR&D Center for Neurorestoration and Neurotechnology (D.J.L., L.R.H.), Rehabilitation R&D Service, Department of VA Medical Center, Providence, RI; Division of Neurocritical Care (S.B.S.), Department of Neurology, Brigham and Women's Hospital, Harvard Medical School; Department of Occupational Therapy (H.J., K.S.E.), MGH Institute of Health Professions, Boston, MA; Department of Rehabilitation (P.B.), Exercise and Nutrition Sciences, University of Cincinnati College of Allied Health Sciences, OH; Department of Biostatistics (J.G.), Columbia University Mailman School of Public Health, New York, NY; Department of Occupational Therapy (J.R.), Massachusetts General Hospital, Boston; School of Engineering (L.R.H.), Brown University, Providence, RI; and Department of Neurology (S.C.C.), University of California, Los Angeles, California Rehabilitation Hospital.

Kimberly S Erler (KS)

From the Center for Neurotechnology and Neurorecovery (D.J.L., R.H., J.A.D., S.M., H.J., K.S.E., K.R., L.R.H.), Department of Neurology, Massachusetts General Hospital, Harvard Medical School; Division of Neurocritical Care (D.J.L., L.R.H.), Department of Neurology; Stroke Service (D.J.L., S.P.F., L.H.S., L.R.H.), Department of Neurology, Massachusetts General Hospital, Boston; VA RR&D Center for Neurorestoration and Neurotechnology (D.J.L., L.R.H.), Rehabilitation R&D Service, Department of VA Medical Center, Providence, RI; Division of Neurocritical Care (S.B.S.), Department of Neurology, Brigham and Women's Hospital, Harvard Medical School; Department of Occupational Therapy (H.J., K.S.E.), MGH Institute of Health Professions, Boston, MA; Department of Rehabilitation (P.B.), Exercise and Nutrition Sciences, University of Cincinnati College of Allied Health Sciences, OH; Department of Biostatistics (J.G.), Columbia University Mailman School of Public Health, New York, NY; Department of Occupational Therapy (J.R.), Massachusetts General Hospital, Boston; School of Engineering (L.R.H.), Brown University, Providence, RI; and Department of Neurology (S.C.C.), University of California, Los Angeles, California Rehabilitation Hospital.

Kelly Rishe (K)

From the Center for Neurotechnology and Neurorecovery (D.J.L., R.H., J.A.D., S.M., H.J., K.S.E., K.R., L.R.H.), Department of Neurology, Massachusetts General Hospital, Harvard Medical School; Division of Neurocritical Care (D.J.L., L.R.H.), Department of Neurology; Stroke Service (D.J.L., S.P.F., L.H.S., L.R.H.), Department of Neurology, Massachusetts General Hospital, Boston; VA RR&D Center for Neurorestoration and Neurotechnology (D.J.L., L.R.H.), Rehabilitation R&D Service, Department of VA Medical Center, Providence, RI; Division of Neurocritical Care (S.B.S.), Department of Neurology, Brigham and Women's Hospital, Harvard Medical School; Department of Occupational Therapy (H.J., K.S.E.), MGH Institute of Health Professions, Boston, MA; Department of Rehabilitation (P.B.), Exercise and Nutrition Sciences, University of Cincinnati College of Allied Health Sciences, OH; Department of Biostatistics (J.G.), Columbia University Mailman School of Public Health, New York, NY; Department of Occupational Therapy (J.R.), Massachusetts General Hospital, Boston; School of Engineering (L.R.H.), Brown University, Providence, RI; and Department of Neurology (S.C.C.), University of California, Los Angeles, California Rehabilitation Hospital.

Pierce Boyne (P)

From the Center for Neurotechnology and Neurorecovery (D.J.L., R.H., J.A.D., S.M., H.J., K.S.E., K.R., L.R.H.), Department of Neurology, Massachusetts General Hospital, Harvard Medical School; Division of Neurocritical Care (D.J.L., L.R.H.), Department of Neurology; Stroke Service (D.J.L., S.P.F., L.H.S., L.R.H.), Department of Neurology, Massachusetts General Hospital, Boston; VA RR&D Center for Neurorestoration and Neurotechnology (D.J.L., L.R.H.), Rehabilitation R&D Service, Department of VA Medical Center, Providence, RI; Division of Neurocritical Care (S.B.S.), Department of Neurology, Brigham and Women's Hospital, Harvard Medical School; Department of Occupational Therapy (H.J., K.S.E.), MGH Institute of Health Professions, Boston, MA; Department of Rehabilitation (P.B.), Exercise and Nutrition Sciences, University of Cincinnati College of Allied Health Sciences, OH; Department of Biostatistics (J.G.), Columbia University Mailman School of Public Health, New York, NY; Department of Occupational Therapy (J.R.), Massachusetts General Hospital, Boston; School of Engineering (L.R.H.), Brown University, Providence, RI; and Department of Neurology (S.C.C.), University of California, Los Angeles, California Rehabilitation Hospital.

Jeff Goldsmith (J)

From the Center for Neurotechnology and Neurorecovery (D.J.L., R.H., J.A.D., S.M., H.J., K.S.E., K.R., L.R.H.), Department of Neurology, Massachusetts General Hospital, Harvard Medical School; Division of Neurocritical Care (D.J.L., L.R.H.), Department of Neurology; Stroke Service (D.J.L., S.P.F., L.H.S., L.R.H.), Department of Neurology, Massachusetts General Hospital, Boston; VA RR&D Center for Neurorestoration and Neurotechnology (D.J.L., L.R.H.), Rehabilitation R&D Service, Department of VA Medical Center, Providence, RI; Division of Neurocritical Care (S.B.S.), Department of Neurology, Brigham and Women's Hospital, Harvard Medical School; Department of Occupational Therapy (H.J., K.S.E.), MGH Institute of Health Professions, Boston, MA; Department of Rehabilitation (P.B.), Exercise and Nutrition Sciences, University of Cincinnati College of Allied Health Sciences, OH; Department of Biostatistics (J.G.), Columbia University Mailman School of Public Health, New York, NY; Department of Occupational Therapy (J.R.), Massachusetts General Hospital, Boston; School of Engineering (L.R.H.), Brown University, Providence, RI; and Department of Neurology (S.C.C.), University of California, Los Angeles, California Rehabilitation Hospital.

Jessica Ranford (J)

From the Center for Neurotechnology and Neurorecovery (D.J.L., R.H., J.A.D., S.M., H.J., K.S.E., K.R., L.R.H.), Department of Neurology, Massachusetts General Hospital, Harvard Medical School; Division of Neurocritical Care (D.J.L., L.R.H.), Department of Neurology; Stroke Service (D.J.L., S.P.F., L.H.S., L.R.H.), Department of Neurology, Massachusetts General Hospital, Boston; VA RR&D Center for Neurorestoration and Neurotechnology (D.J.L., L.R.H.), Rehabilitation R&D Service, Department of VA Medical Center, Providence, RI; Division of Neurocritical Care (S.B.S.), Department of Neurology, Brigham and Women's Hospital, Harvard Medical School; Department of Occupational Therapy (H.J., K.S.E.), MGH Institute of Health Professions, Boston, MA; Department of Rehabilitation (P.B.), Exercise and Nutrition Sciences, University of Cincinnati College of Allied Health Sciences, OH; Department of Biostatistics (J.G.), Columbia University Mailman School of Public Health, New York, NY; Department of Occupational Therapy (J.R.), Massachusetts General Hospital, Boston; School of Engineering (L.R.H.), Brown University, Providence, RI; and Department of Neurology (S.C.C.), University of California, Los Angeles, California Rehabilitation Hospital.

Seth P Finklestein (SP)

From the Center for Neurotechnology and Neurorecovery (D.J.L., R.H., J.A.D., S.M., H.J., K.S.E., K.R., L.R.H.), Department of Neurology, Massachusetts General Hospital, Harvard Medical School; Division of Neurocritical Care (D.J.L., L.R.H.), Department of Neurology; Stroke Service (D.J.L., S.P.F., L.H.S., L.R.H.), Department of Neurology, Massachusetts General Hospital, Boston; VA RR&D Center for Neurorestoration and Neurotechnology (D.J.L., L.R.H.), Rehabilitation R&D Service, Department of VA Medical Center, Providence, RI; Division of Neurocritical Care (S.B.S.), Department of Neurology, Brigham and Women's Hospital, Harvard Medical School; Department of Occupational Therapy (H.J., K.S.E.), MGH Institute of Health Professions, Boston, MA; Department of Rehabilitation (P.B.), Exercise and Nutrition Sciences, University of Cincinnati College of Allied Health Sciences, OH; Department of Biostatistics (J.G.), Columbia University Mailman School of Public Health, New York, NY; Department of Occupational Therapy (J.R.), Massachusetts General Hospital, Boston; School of Engineering (L.R.H.), Brown University, Providence, RI; and Department of Neurology (S.C.C.), University of California, Los Angeles, California Rehabilitation Hospital.

Lee H Schwamm (LH)

From the Center for Neurotechnology and Neurorecovery (D.J.L., R.H., J.A.D., S.M., H.J., K.S.E., K.R., L.R.H.), Department of Neurology, Massachusetts General Hospital, Harvard Medical School; Division of Neurocritical Care (D.J.L., L.R.H.), Department of Neurology; Stroke Service (D.J.L., S.P.F., L.H.S., L.R.H.), Department of Neurology, Massachusetts General Hospital, Boston; VA RR&D Center for Neurorestoration and Neurotechnology (D.J.L., L.R.H.), Rehabilitation R&D Service, Department of VA Medical Center, Providence, RI; Division of Neurocritical Care (S.B.S.), Department of Neurology, Brigham and Women's Hospital, Harvard Medical School; Department of Occupational Therapy (H.J., K.S.E.), MGH Institute of Health Professions, Boston, MA; Department of Rehabilitation (P.B.), Exercise and Nutrition Sciences, University of Cincinnati College of Allied Health Sciences, OH; Department of Biostatistics (J.G.), Columbia University Mailman School of Public Health, New York, NY; Department of Occupational Therapy (J.R.), Massachusetts General Hospital, Boston; School of Engineering (L.R.H.), Brown University, Providence, RI; and Department of Neurology (S.C.C.), University of California, Los Angeles, California Rehabilitation Hospital.

Leigh R Hochberg (LR)

From the Center for Neurotechnology and Neurorecovery (D.J.L., R.H., J.A.D., S.M., H.J., K.S.E., K.R., L.R.H.), Department of Neurology, Massachusetts General Hospital, Harvard Medical School; Division of Neurocritical Care (D.J.L., L.R.H.), Department of Neurology; Stroke Service (D.J.L., S.P.F., L.H.S., L.R.H.), Department of Neurology, Massachusetts General Hospital, Boston; VA RR&D Center for Neurorestoration and Neurotechnology (D.J.L., L.R.H.), Rehabilitation R&D Service, Department of VA Medical Center, Providence, RI; Division of Neurocritical Care (S.B.S.), Department of Neurology, Brigham and Women's Hospital, Harvard Medical School; Department of Occupational Therapy (H.J., K.S.E.), MGH Institute of Health Professions, Boston, MA; Department of Rehabilitation (P.B.), Exercise and Nutrition Sciences, University of Cincinnati College of Allied Health Sciences, OH; Department of Biostatistics (J.G.), Columbia University Mailman School of Public Health, New York, NY; Department of Occupational Therapy (J.R.), Massachusetts General Hospital, Boston; School of Engineering (L.R.H.), Brown University, Providence, RI; and Department of Neurology (S.C.C.), University of California, Los Angeles, California Rehabilitation Hospital.

Steven C Cramer (SC)

From the Center for Neurotechnology and Neurorecovery (D.J.L., R.H., J.A.D., S.M., H.J., K.S.E., K.R., L.R.H.), Department of Neurology, Massachusetts General Hospital, Harvard Medical School; Division of Neurocritical Care (D.J.L., L.R.H.), Department of Neurology; Stroke Service (D.J.L., S.P.F., L.H.S., L.R.H.), Department of Neurology, Massachusetts General Hospital, Boston; VA RR&D Center for Neurorestoration and Neurotechnology (D.J.L., L.R.H.), Rehabilitation R&D Service, Department of VA Medical Center, Providence, RI; Division of Neurocritical Care (S.B.S.), Department of Neurology, Brigham and Women's Hospital, Harvard Medical School; Department of Occupational Therapy (H.J., K.S.E.), MGH Institute of Health Professions, Boston, MA; Department of Rehabilitation (P.B.), Exercise and Nutrition Sciences, University of Cincinnati College of Allied Health Sciences, OH; Department of Biostatistics (J.G.), Columbia University Mailman School of Public Health, New York, NY; Department of Occupational Therapy (J.R.), Massachusetts General Hospital, Boston; School of Engineering (L.R.H.), Brown University, Providence, RI; and Department of Neurology (S.C.C.), University of California, Los Angeles, California Rehabilitation Hospital.

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