Article (Scientific journals)
Sleep-dependent structural neuroplasticity after a spatial navigation task: A diffusion imaging study.
Villemonteix, Thomas; Guerreri, Michele; Deantoni, Michele et al.
2023In Journal of Neuroscience Research, 101 (7), p. 1031 - 1043
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Keywords :
NODDI; diffusion imaging; sleep; spatial navigation; structural; Young Adult; Humans; Diffusion Tensor Imaging/methods; Neurites; Diffusion Magnetic Resonance Imaging/methods; Hippocampus/diagnostic imaging; Brain; Spatial Navigation; White Matter; Diffusion Magnetic Resonance Imaging; Diffusion Tensor Imaging; Hippocampus; Cellular and Molecular Neuroscience
Abstract :
[en] 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.
Disciplines :
Neurosciences & behavior
Author, co-author :
Villemonteix, Thomas ;  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 ; Laboratoire Psychopathologie et Processus de Changement, EA2027, Paris 8 University, Saint-Denis, France
Guerreri, Michele;  Department of Computer Science & Centre for Medical Image Computing, University College London, London, UK
Deantoni, Michele ;  Université de Liège - ULiège > Département de Psychologie > Neuropsychologie de l'adulte ; 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
Balteau, Evelyne ;  Université de Liège - ULiège > Département des sciences de la vie > Virologie - Immunologie
Schmidt, Christina  ;  Université de Liège - ULiège > Département de Psychologie > Neuropsychologie de l'adulte
Stee, Whitney;  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 ; Sleep & Chronobiology Group, GIGA-CRC-In Vivo Imaging Research Unit, University of Liège, Liège, Belgium
Zhang, Hui;  Department of Computer Science & Centre for Medical Image Computing, University College London, London, UK
Peigneux, Philippe ;  Université de Liège - ULiège > Département des sciences cliniques > Neuroimagerie des troubles de la mémoire et revalidation cognitive ; 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
Language :
English
Title :
Sleep-dependent structural neuroplasticity after a spatial navigation task: A diffusion imaging study.
Publication date :
July 2023
Journal title :
Journal of Neuroscience Research
ISSN :
0360-4012
eISSN :
1097-4547
Publisher :
John Wiley and Sons Inc, United States
Volume :
101
Issue :
7
Pages :
1031 - 1043
Peer reviewed :
Peer Reviewed verified by ORBi
Funders :
FRIA - Fonds pour la Formation à la Recherche dans l'Industrie et dans l'Agriculture
F.R.S.-FNRS - Fonds de la Recherche Scientifique
Funding text :
This study was supported by the Fonds de la Recherche Scientifique (F.R.S.‐F.N.R.S.) and the Fonds Wetenschappelijk Onderzoek – Vlaanderen (F.W.O.) under the Excellence of Science (EOS) Project (MEMODYN, No. 30446199) coordinated by P.P. W.S. is supported by an F.N.R.S. Aspirant Research Fellowship. M.G. received postdoctoral salary support from the EOS MEMODYN project. At the time of the study, T.V. was funded by an Université Libre de Bruxelles (ULB) Individual Fellowship. M.D. is supported by the Fonds pour la Recherche dans l'Industrie et l'Agriculture (FRIA) Fellowship. C.S. is FNRS Research Associate. The authors have no conflict of interest to declare.
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