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

Evidence 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. This study evidenced a coherent set of cortical microstructural changes associated with spatial learning and relearning, accounted for by decreases in free water fraction in the revised biophysical neurite orientation/dispersion and density imaging model. Post‐learning sleep‐related changes were found in subcortical regions after exposing participants to a sleep deprivation protocol.