Post-stroke reorganization of transient brain activity characterizes deficits and recovery of cognitive functions

Elvira Pirondini; Nawal Kinany; Cécile Le Sueur; Joseph C Griffis; Gordon L Shulman; Maurizio Corbetta; Dimitri Van De Ville

doi:10.1016/j.neuroimage.2022.119201

Post-stroke reorganization of transient brain activity characterizes deficits and recovery of cognitive functions

Neuroimage. 2022 Jul 15:255:119201. doi: 10.1016/j.neuroimage.2022.119201. Epub 2022 Apr 9.

Authors

Elvira Pirondini¹, Nawal Kinany², Cécile Le Sueur³, Joseph C Griffis⁴, Gordon L Shulman⁴, Maurizio Corbetta⁵, Dimitri Van De Ville⁶

Affiliations

¹ Department of Radiology and Medical Informatics, University of Geneva; 1211 Geneva, Switzerland; Medical Image Processing Laboratory, Center for Neuroprosthetics, Institute of Bioengineering, Ecole Polytechnique Fédérale de Lausanne (EPFL); 1202 Geneva, Switzerland; Department of Physical Medicine and Rehabilitation, University of Pittsburgh; Pittsburgh, PA, USA; Rehabilitation Neural Engineering Laboratories, University of Pittsburgh; Pittsburgh, PA, USA; Department of BioEngineering, University of Pittsburgh; Pittsburgh, PA, USA. Electronic address: elvirap@pitt.edu.
² Department of Radiology and Medical Informatics, University of Geneva; 1211 Geneva, Switzerland; Medical Image Processing Laboratory, Center for Neuroprosthetics, Institute of Bioengineering, Ecole Polytechnique Fédérale de Lausanne (EPFL); 1202 Geneva, Switzerland; Bertarelli Foundation Chair in Translational Neuroengineering, Center for Neuroprosthetics, Institute of Bioengineerin, Ecole Polytechnique Fédérale de Lausanne (EPFL); 1202 Geneva, Switzerland.
³ Medical Image Processing Laboratory, Center for Neuroprosthetics, Institute of Bioengineering, Ecole Polytechnique Fédérale de Lausanne (EPFL); 1202 Geneva, Switzerland.
⁴ Department of Neurology, Washington University School of Medicine, St. Louis; MO, 63110, USA.
⁵ Department of Neurology, Washington University School of Medicine, St. Louis; MO, 63110, USA; Department of Radiology, Washington University School of Medicine, St. Louis; MO, 63110, USA; Department of Anatomy and Neurobiology, Washington University School of Medicine, St. Louis; MO, 63110, USA; Department of Bioengineering, Washington University School of Medicine, St. Louis; MO, 63110, USA; Department of Neuroscience and Padua Neuroscience Center, University of Padua; Padua, Italy; Venetian Institute of Molecular Medicine (VIMM); Padua, Italy.
⁶ Department of Radiology and Medical Informatics, University of Geneva; 1211 Geneva, Switzerland; Medical Image Processing Laboratory, Center for Neuroprosthetics, Institute of Bioengineering, Ecole Polytechnique Fédérale de Lausanne (EPFL); 1202 Geneva, Switzerland. Electronic address: dimitri.vandeville@epfl.ch.

PMID: 35405342
DOI: 10.1016/j.neuroimage.2022.119201

Abstract

Functional magnetic resonance imaging (fMRI) has been widely employed to study stroke pathophysiology. In particular, analyses of fMRI signals at rest were directed at quantifying the impact of stroke on spatial features of brain networks. However, brain networks have intrinsic time features that were, so far, disregarded in these analyses. In consequence, standard fMRI analysis failed to capture temporal imbalance resulting from stroke lesions, hence restricting their ability to reveal the interdependent pathological changes in structural and temporal network features following stroke. Here, we longitudinally analyzed hemodynamic-informed transient activity in a large cohort of stroke patients (n = 103) to assess spatial and temporal changes of brain networks after stroke. Metrics extracted from the hemodynamic-informed transient activity were replicable within- and between-individuals in healthy participants, hence supporting their robustness and their clinical applicability. While large-scale spatial patterns of brain networks were preserved after stroke, their durations were altered, with stroke subjects exhibiting a varied pattern of longer and shorter network activations compared to healthy individuals. Specifically, patients showed a longer duration in the lateral precentral gyrus and anterior cingulum, and a shorter duration in the occipital lobe and in the cerebellum. These temporal alterations were associated with white matter damage in projection and association pathways. Furthermore, they were tied to deficits in specific behavioral domains as restoration of healthy brain dynamics paralleled recovery of cognitive functions (attention, language and spatial memory), but was not significantly correlated to motor recovery. These findings underscore the critical importance of network temporal properties in dissecting the pathophysiology of brain changes after stroke, thus shedding new light on the clinical potential of time-resolved methods for fMRI analysis.

Keywords: Dynamic functional connectivity; Stroke; Test-retest reliability; fMRI.

MeSH terms

Brain / diagnostic imaging
Brain Mapping
Cognition
Humans
Magnetic Resonance Imaging
Nerve Net
Stroke* / complications
Stroke* / diagnostic imaging