Interhemispheric Structural Connectivity Underlies Motor Recovery after Stroke

Author:

Paul Theresa12ORCID,Wiemer Valerie M.12ORCID,Hensel Lukas1ORCID,Cieslak Matthew3ORCID,Tscherpel Caroline1ORCID,Grefkes Christian4ORCID,Grafton Scott T.5ORCID,Fink Gereon R.12ORCID,Volz Lukas J.1ORCID

Affiliation:

1. Medical Faculty, University of Cologne, and Department of Neurology University Hospital Cologne Cologne Germany

2. Institute of Neuroscience and Medicine, Cognitive Neuroscience (INM‐3) Research Centre Juelich Juelich Germany

3. Department of Psychiatry, Perelman School of Medicine University of Pennsylvania Philadelphia PA

4. Department of Neurology University Hospital Frankfurt, Goethe University Frankfurt Frankfurt am Main Germany

5. Department of Psychological & Brain Sciences University of California Santa Barbara CA

Abstract

ObjectiveAlthough ample evidence highlights that the ipsilesional corticospinal tract (CST) plays a crucial role in motor recovery after stroke, studies on cortico‐cortical motor connections remain scarce and provide inconclusive results. Given their unique potential to serve as structural reserve enabling motor network reorganization, the question arises whether cortico‐cortical connections may facilitate motor control depending on CST damage.MethodsDiffusion spectrum imaging (DSI) and a novel compartment‐wise analysis approach were used to quantify structural connectivity between bilateral cortical core motor regions in chronic stroke patients. Basal and complex motor control were differentially assessed.ResultsBoth basal and complex motor performance were correlated with structural connectivity between bilateral premotor areas and ipsilesional primary motor cortex (M1) as well as interhemispheric M1 to M1 connectivity. Whereas complex motor skills depended on CST integrity, a strong association between M1 to M1 connectivity and basal motor control was observed independent of CST integrity especially in patients who underwent substantial motor recovery. Harnessing the informational wealth of cortico‐cortical connectivity facilitated the explanation of both basal and complex motor control.InterpretationWe demonstrate for the first time that distinct aspects of cortical structural reserve enable basal and complex motor control after stroke. In particular, recovery of basal motor control may be supported via an alternative route through contralesional M1 and non‐crossing fibers of the contralesional CST. Our findings help to explain previous conflicting interpretations regarding the functional role of the contralesional M1 and highlight the potential of cortico‐cortical structural connectivity as a future biomarker for motor recovery post‐stroke. ANN NEUROL 2023;94:785–797

Funder

Army Research Office

Deutsche Forschungsgemeinschaft

Publisher

Wiley

Subject

Neurology (clinical),Neurology

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