Differential Impact of Brain Network Efficiency on Poststroke Motor and Attentional Deficits

Author:

Evangelista Giorgia G.12ORCID,Egger Philip12ORCID,Brügger Julia12ORCID,Beanato Elena12ORCID,Koch Philipp J.34,Ceroni Martino12ORCID,Fleury Lisa12ORCID,Cadic-Melchior Andéol12ORCID,Meyer Nathalie H.5ORCID,Rodríguez Diego de León1256ORCID,Girard Gabriel789ORCID,Léger Bertrand10ORCID,Turlan Jean-Luc10ORCID,Mühl Andreas10,Vuadens Philippe10,Adolphsen Jan11,Jagella Caroline E.12,Constantin Christophe6ORCID,Alvarez Vincent6,San Millán Diego6ORCID,Bonvin Christophe6ORCID,Morishita Takuya12ORCID,Wessel Maximilian J.1213,Van De Ville Dimitri1415ORCID,Hummel Friedhelm C.1216ORCID

Affiliation:

1. Defitech Chair of Clinical Neuroengineering, Neuro-X Institute (INX), École polytechnique fédérale de Lausanne (EPFL), Geneva, Switzerland (G.G.E., P.E., J.B., E.B., M.C., L.F., A.C.-M., D.d.L.R., T.M., M.J.W., F.C.H.).

2. Defitech Chair of Clinical Neuroengineering, INX, EPFL Valais, Clinique Romande de Réadaptation, Switzerland (G.G.E., P.E., J.B., E.B., M.C., L.F., A.C.-M., T.M., D.d.L.R., M.J.W., F.C.H.).

3. Department of Neurology, University of Lübeck, Germany (P.J.K.).

4. Center of Brain, Behavior and Metabolism, University of Lübeck, Germany (P.J.K.).

5. Laboratory of Cognitive Neuroscience, CNP and BMI, EPFL, Switzerland (N.H.M., D.d.L.R.).

6. Department of Neurology, Hôpital du Valais, Switzerland (C.C., V.A., D.d.L.R., D.S.M., C.B.).

7. Signal Processing Laboratory (LTS5), School of Engineering, EPFL, Switzerland (G.G.).

8. Center for Biomedical Imaging (CIBM), Switzerland (G.G.).

9. Department of Radiology, CHUV, Switzerland (G.G.).

10. Clinique Romande de Réadaptation, Switzerland (B.L., A.M., P.V., J.-L.T.).

11. Mediclin Reha-Zentrum, Germany (J.A.).

12. Migräne- und Kopfschmerzklinik Königstein, Germany (C.E.J.).

13. Department of Neurology, University Hospital Würzburg, Germany (M.J.W.).

14. Medical Image Processing Laboratory, Institute of Bioengineering, EPFL, Switzerland (D.V.D.V.).

15. Department of Radiology and Medical Informatics, University of Geneva (UNIGE), Switzerland (D.V.D.V.).

16. Clinical Neuroscience, Geneva University Hospital (HUG), Switzerland (F.C.H.).

Abstract

Background: Most studies on stroke have been designed to examine one deficit in isolation; yet, survivors often have multiple deficits in different domains. While the mechanisms underlying multiple-domain deficits remain poorly understood, network-theoretical methods may open new avenues of understanding. Methods: Fifty subacute stroke patients (7±3days poststroke) underwent diffusion-weighted magnetic resonance imaging and a battery of clinical tests of motor and cognitive functions. We defined indices of impairment in strength, dexterity, and attention. We also computed imaging-based probabilistic tractography and whole-brain connectomes. To efficiently integrate inputs from different sources, brain networks rely on a rich-club of a few hub nodes. Lesions harm efficiency, particularly when they target the rich-club. Overlaying individual lesion masks onto the tractograms enabled us to split the connectomes into their affected and unaffected parts and associate them to impairment. Results: We computed efficiency of the unaffected connectome and found it was more strongly correlated to impairment in strength, dexterity, and attention than efficiency of the total connectome. The magnitude of the correlation between efficiency and impairment followed the order attention>dexterity ≈ strength (strength: | r |=.03, P =0.02, dexterity: | r |=.30, P =0.05, attention: | r |=.55, P <0.001). Network weights associated with the rich-club were more strongly correlated to efficiency than non-rich-club weights. Conclusions: Attentional impairment is more sensitive to disruption of coordinated networks between brain regions than motor impairment, which is sensitive to disruption of localized networks. Providing more accurate reflections of actually functioning parts of the network enables the incorporation of information about the impact of brain lesions on connectomics contributing to a better understanding of underlying stroke mechanisms.

Publisher

Ovid Technologies (Wolters Kluwer Health)

Subject

Advanced and Specialized Nursing,Cardiology and Cardiovascular Medicine,Neurology (clinical)

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