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June 02, 2023Research Article

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

View ORCID ProfileDavid J Lin, View ORCID ProfileRichard Hardstone, Julie A DiCarlo, Sydney Mckiernan, Samuel B Snider, Hannah Jacobs, View ORCID ProfileKimberly S Erler, Kelly Rishe, Pierce Boyne, Jeff Goldsmith, Jessica Ranford, Seth P. Finklestein, View ORCID ProfileLee H. Schwamm, View ORCID ProfileLeigh R Hochberg, Steven C. Cramer
First published June 2, 2023, DOI: https://doi.org/10.1212/WNL.0000000000207417
David J Lin
1Center for Neurotechnology and Neurorecovery, Department of Neurology, Massachusetts General Hospital, Harvard Medical School, Boston, MA, 02114, USA
2Division of Neurocritical Care, Department of Neurology, Massachusetts General Hospital, Boston, MA, 02114, USA
3Stroke Service, Department of Neurology, Massachusetts General Hospital, Boston, MA, 02114, USA
4VA RR&D Center for Neurorestoration and Neurotechnology, Rehabilitation R&D Service, Department of VA Medical Center, Providence, RI, 02908, USA
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  • ORCID record for David J Lin
  • For correspondence: dlin7@mgh.harvard.edu
Richard Hardstone
1Center for Neurotechnology and Neurorecovery, Department of Neurology, Massachusetts General Hospital, Harvard Medical School, Boston, MA, 02114, USA
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  • ORCID record for Richard Hardstone
Julie A DiCarlo
1Center for Neurotechnology and Neurorecovery, Department of Neurology, Massachusetts General Hospital, Harvard Medical School, Boston, MA, 02114, USA
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Sydney Mckiernan
1Center for Neurotechnology and Neurorecovery, Department of Neurology, Massachusetts General Hospital, Harvard Medical School, Boston, MA, 02114, USA
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Samuel B Snider
5Division of Neurocritical Care, Department of Neurology, Brigham and Women’s Hospital, Harvard Medical School, Boston, MA, 02115, USA
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Hannah Jacobs
1Center for Neurotechnology and Neurorecovery, Department of Neurology, Massachusetts General Hospital, Harvard Medical School, Boston, MA, 02114, USA
6Department of Occupational Therapy, MGH Institute of Health Professions, Boston, MA, 02129, USA
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Kimberly S Erler
1Center for Neurotechnology and Neurorecovery, Department of Neurology, Massachusetts General Hospital, Harvard Medical School, Boston, MA, 02114, USA
6Department of Occupational Therapy, MGH Institute of Health Professions, Boston, MA, 02129, USA
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  • ORCID record for Kimberly S Erler
Kelly Rishe
1Center for Neurotechnology and Neurorecovery, Department of Neurology, Massachusetts General Hospital, Harvard Medical School, Boston, MA, 02114, USA
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Pierce Boyne
7Department of Rehabilitation, Exercise and Nutrition Sciences, University of Cincinnati College of Allied Health Sciences, Cincinnati, OH, 45221, USA
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Jeff Goldsmith
8Department of Biostatistics, Columbia University Mailman School of Public Health, New York, NY, 10032, USA
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Jessica Ranford
9Department of Occupational Therapy, Massachusetts General Hospital, Boston, MA, 02114, USA
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Seth P. Finklestein
3Stroke Service, Department of Neurology, Massachusetts General Hospital, Boston, MA, 02114, USA
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Lee H. Schwamm
3Stroke Service, Department of Neurology, Massachusetts General Hospital, Boston, MA, 02114, USA
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  • ORCID record for Lee H. Schwamm
Leigh R Hochberg
1Center for Neurotechnology and Neurorecovery, Department of Neurology, Massachusetts General Hospital, Harvard Medical School, Boston, MA, 02114, USA
2Division of Neurocritical Care, Department of Neurology, Massachusetts General Hospital, Boston, MA, 02114, USA
3Stroke Service, Department of Neurology, Massachusetts General Hospital, Boston, MA, 02114, USA
4VA RR&D Center for Neurorestoration and Neurotechnology, Rehabilitation R&D Service, Department of VA Medical Center, Providence, RI, 02908, USA
10School of Engineering, Brown University, Providence RI, 02912, USA
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  • ORCID record for Leigh R Hochberg
Steven C. Cramer
11Department of Neurology, University of California, Los Angeles; California Rehabilitation Hospital; Los Angeles, CA, 90095 USA
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Citation
Distinguishing Distinct Neural Systems for Proximal vs Distal Upper Extremity Motor Control After Acute Stroke
David J Lin, Richard Hardstone, Julie A DiCarlo, Sydney Mckiernan, Samuel B Snider, Hannah Jacobs, Kimberly S Erler, Kelly Rishe, Pierce Boyne, Jeff Goldsmith, Jessica Ranford, Seth P. Finklestein, Lee H. Schwamm, Leigh R Hochberg, Steven C. Cramer
Neurology Jun 2023, 10.1212/WNL.0000000000207417; DOI: 10.1212/WNL.0000000000207417

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Abstract

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 two 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 seven days of acute stroke. Partial correlation analysis was used to assess the relationship between proximal and distal motor scores. Functional outcomes including the Box & Blocks Test, Barthel Index, and modified Rankin Scale were examined in relation to proximal versus distal motor patterns of deficit. Voxel-based lesion-symptom mapping was used to identify regions of injury associated with proximal versus 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 (p = 0.002). A pattern of proximal more than distal injury (i.e., relatively preserved distal motor control) was not rare, observed in 23% of acute stroke subjects. Patients with relatively preserved distal motor control, even after controlling for total extent of deficit, had better outcomes in the first week and at 90-days post-stroke (Box and Block Test, ρ = 0.51, p < 0.001; Barthel Index, ρ = 0.41, p < 0.001; modified Rankin Scale, ρ = 0.38, p < 0.001). Deficits in proximal motor control were associated with widespread injury to subcortical white and gray matter, while deficits in distal motor control were associated with injury restricted to the posterior aspect of the precentral gyrus, consistent with the organization of proximal versus distal neural circuits in the healthy CNS.

Conclusions: 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 post-stroke upper extremity hemiparesis.

  • Received November 27, 2022.
  • Accepted in final form March 31, 2023.
  • 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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