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

Abstract

Evidence for sleep-dependent changes in micro-structural 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-minutes 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-minutes 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 remodelling of neurites and glial cells subtending learning and memory processes in basal ganglia and hippocampal structures..

Microstructural dynamics of motor learning and sleep-dependent consolidation: A diffusion imaging study

“…Finally, ODI changes in a few clusters, again in analogous regions, also suggest tissue reorganization in the brain tissue microstructure, even if at a smaller scale. Interestingly, although MD decreases have been repeatedly reported in the neocortex following learning, 28 , 30 , 56 a previous study using NODDI to investigate spatial learning-related structural plasticity observed FWF decreases but no NDI increase contrary to our results. 56 Besides task differences, this might be due to the fact that we used the revised version 57 , 58 instead of the original NODDI model 32 used in this preceding experiment, probably giving us the opportunity to gain in preciseness when it comes to disentangling the different components influencing MD alterations.…”

Microstructural dynamics of motor learning and sleep-dependent consolidation: a diffusion imaging study

“…Finally, ODI changes in a few clusters, again in analogous regions, also suggest tissue reorganization in the brain tissue microstructure, even if at a smaller scale. Interestingly, although MD decreases have been repeatedly reported in the neocortex following learning, 28,30,56 a previous study using NODDI to investigate spatial learningrelated structural plasticity observed FWF decreases but no NDI increase contrary to our results. 56 Besides task differences, this might be due to the fact that we used the revised version 57,58 instead of the original NODDI model 32 used in this preceding experiment, probably giving us the opportunity to gain in preciseness when it comes to disentangling the different components influencing MD alterations.…”

“…Interestingly, although MD decreases have been repeatedly reported in the neocortex following learning, 28,30,56 a previous study using NODDI to investigate spatial learningrelated structural plasticity observed FWF decreases but no NDI increase contrary to our results. 56 Besides task differences, this might be due to the fact that we used the revised version 57,58 instead of the original NODDI model 32 used in this preceding experiment, probably giving us the opportunity to gain in preciseness when it comes to disentangling the different components influencing MD alterations. Then, in subcortical regions of interest, decreased MD was found in the left putamen, right thalamus and caudate, bilateral hippocampus, and cerebellar cortex, together with increased FA in the right caudate and cerebellar cortex.…”

“…64,65 Lastly, we hypothesized that microstructural parameters would change again when re-exposed to the initial motor task and that these changes could be modulated by the sleep opportunity on the post-learning night, as shown in a prior study investigating topographical learning. 56 In the cortical ribbon, the pattern was similar to the one observed during the first learning episode but less extended, and this was not affected by the sleep manipulation. At the functional level, cortical involvement was shown to increase with sequential proficiency, whereas hippocampus and dorsomedial striatum progressively disengage.…”

Continuous structural neuroplasticity during motor learning - a diffusion MRI study

“…Numerous studies have explored the structural and functional alterations that accompany learning using structural and functional magnetic resonance imaging (MRI), respectively. Over the last decade, diffusion-weighted MRI (dMRI) has also been employed to study short-term microstructural neuroplasticity (Brodt et al, 2018; Hofstetter et al, 2017; Jacobacci et al, 2020; Keller and Just, 2016; Sagi et al, 2012; Tavor et al, 2020, 2013; Villemonteix et al, 2023). dMRI measures the translational displacement of water molecules (Bihan and Warach, 1995) and is mainly used for white matter assessment and reconstruction (Catani et al, 2002; Moseley et al, 1990; Warach et al, 1992).…”