Compensatory increase in ipsilesional supplementary motor area and premotor connectivity is associated with greater gait impairments: a personalized fMRI analysis in chronic stroke

Xiaolong Peng; Shraddha Srivastava; Falon Sutton; Yongkuan Zhang; Bashar W Badran; Steven A Kautz

doi:10.3389/fnhum.2024.1340374

Compensatory increase in ipsilesional supplementary motor area and premotor connectivity is associated with greater gait impairments: a personalized fMRI analysis in chronic stroke

Front Hum Neurosci. 2024 Feb 29:18:1340374. doi: 10.3389/fnhum.2024.1340374. eCollection 2024.

Authors

Xiaolong Peng^#¹, Shraddha Srivastava^#^{2

3}, Falon Sutton¹, Yongkuan Zhang¹, Bashar W Badran¹, Steven A Kautz^{2

3

4}

Affiliations

¹ Department of Psychiatry and Behavioral Sciences, Neuro-X Lab, Medical University of South Carolina, Charleston, SC, United States.
² Ralph H. Johnson VA Medical Center, Charleston, SC, United States.
³ Department of Health Sciences and Research, College of Health Professions, Medical University of South Carolina, Charleston, SC, United States.
⁴ Division of Physical Therapy, Department of Rehabilitation Sciences, College of Health Professions, Medical University of South Carolina, Charleston, SC, United States.

^# Contributed equally.

Abstract

Background: Balance and mobility impairments are prevalent post-stroke and a large number of survivors require walking assistance at 6 months post-stroke which diminishes their overall quality of life. Personalized interventions for gait and balance rehabilitation are crucial. Recent evidence indicates that stroke lesions in primary motor pathways, such as corticoreticular pathways (CRP) and corticospinal tract (CST), may lead to reliance on alternate motor pathways as compensation, but the current evidence lacks comprehensive knowledge about the underlying neural mechanisms.

Methods: In this study, we investigate the functional connectivity (FC) changes within the motor network derived from an individualized cortical parcellation approach in 33 participants with chronic stroke compared to 17 healthy controls. The correlations between altered motor FC and gait deficits (i.e., walking speed and walking balance) were then estimated in the stroke population to understand the compensation mechanism of the motor network in motor function rehabilitation post-stroke.

Results: Our results demonstrated significant FC increases between ipsilesional medial supplementary motor area (SMA) and premotor in stroke compared to healthy controls. Furthermore, we also revealed a negative correlation between ipsilesional SMA-premotor FC and self-selected walking speed, as well as the Functional Gait Assessment (FGA) scores.

Conclusion: The increased FC between the ipsilesional SMA and premotor regions could be a compensatory mechanism within the motor network following a stroke when the individual can presumably no longer rely on the more precise CST modulation of movements to produce a healthy walking pattern. These findings enhance our understanding of individualized motor network FC changes and their connection to gait and walking balance impairments post-stroke, improving stroke rehabilitation interventions.

Keywords: fMRI; functional connectivity; gait; motor rehabilitation; stroke.

Grants and funding

The author(s) declare financial support was received for the research, authorship, and/or publication of this article. Research reported in this publication was supported by the Rehabilitation Research and Development Service of the Department of Veterans Affairs grant 1I01RX001935, the Senior Research Career Scientist award grant 1IK6RX003075, the National Institutes of Health grant P20-GM109040, and the National Institute on Drug Abuse of the National Institutes of Health grant 5P50DA046373.