Sleep‐dependent structural neuroplasticity after a spatial navigation task: A diffusion imaging study

Author:

Villemonteix Thomas12ORCID,Guerreri Michele3,Deantoni Michele14,Balteau Evelyne4,Schmidt Christina4,Stee Whitney14,Zhang Hui3,Peigneux Philippe14

Affiliation:

1. UR2NF‐Neuropsychology and Functional Neuroimaging Research Unit affiliated at CRCN – Centre for Research in Cognition and Neurosciences and UNI – ULB Neuroscience Institute Université Libre de Bruxelles (ULB) Brussels Belgium

2. Laboratoire Psychopathologie et Processus de Changement, EA2027 Paris 8 University Saint‐Denis France

3. Department of Computer Science & Centre for Medical Image Computing University College London London UK

4. Sleep & Chronobiology Group, GIGA‐CRC‐In Vivo Imaging Research Unit University of Liège Liège Belgium

Abstract

AbstractEvidence for sleep‐dependent changes in microstructural neuroplasticity remains scarce, despite the fact that it is a mandatory correlate of the reorganization of learning‐related functional networks. We investigated the effects of post‐training sleep on structural neuroplasticity markers measuring standard diffusion tensor imaging (DTI), mean diffusivity (MD), and the revised biophysical neurite orientation dispersion and density imaging (NODDI), free water fraction (FWF), and neurite density (NDI) parameters that enable disentangling whether MD changes result from modifications in neurites or in other cellular components (e.g., glial cells). Thirty‐four healthy young adults were scanned using diffusion‐weighted imaging (DWI) on Day1 before and after 40‐min route learning (navigation) in a virtual environment, then were sleep deprived (SD) or slept normally (RS) for the night. After recovery sleep for 2 nights, they were scanned again (Day4) before and after 40‐min route learning (navigation) in an extended environment. Sleep‐related microstructural changes were computed on DTI (MD) and NODDI (NDI and FWF) parameters in the cortical ribbon and subcortical hippocampal and striatal regions of interest (ROIs). Results disclosed navigation learning‐related decreased DWI parameters in the cortical ribbon (MD, FWF) and subcortical (MD, FWF, NDI) areas. Post‐learning sleep‐related changes were found at Day4 in the extended learning session (pre‐ to post‐relearning percentage changes), suggesting a rapid sleep‐related remodeling of neurites and glial cells subtending learning and memory processes in basal ganglia and hippocampal structures.

Funder

Fonds pour la Formation à la Recherche dans l’Industrie et dans l’Agriculture

Publisher

Wiley

Subject

Cellular and Molecular Neuroscience

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