Altered isotropic volume fraction in gray matter after sleep deprivation and its association with visuospatial memory: A neurite orientation dispersion and density imaging study

Background and aimsDiffusion magnetic resonance imaging (dMRI) studies have revealed microstructural abnormalities in white matter resulting from sleep deprivation (SD). This study aimed to adopt neurite orientation dispersion and density imaging (NODDI) to investigate the effect of SD on gray matte...

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Main Authors: Jia-Hui Lin, Xu-Hui Chen, Ye Wu, Yun-Bin Cao, Hua-Jun Chen, Nao-Xin Huang
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-03-01
Series:Frontiers in Neuroscience
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fnins.2023.1144802/full
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author Jia-Hui Lin
Xu-Hui Chen
Ye Wu
Yun-Bin Cao
Hua-Jun Chen
Nao-Xin Huang
author_facet Jia-Hui Lin
Xu-Hui Chen
Ye Wu
Yun-Bin Cao
Hua-Jun Chen
Nao-Xin Huang
author_sort Jia-Hui Lin
collection DOAJ
description Background and aimsDiffusion magnetic resonance imaging (dMRI) studies have revealed microstructural abnormalities in white matter resulting from sleep deprivation (SD). This study aimed to adopt neurite orientation dispersion and density imaging (NODDI) to investigate the effect of SD on gray matter (GM) microstructural properties and its association to visuospatial memory (VSM).MethodsTwenty-four healthy women underwent two sessions of dMRI scanning and visuospatial ability assessment by Complex Figure Test (CFT), once during rested wakefulness (RW) and once after 24 h of SD. We calculated NODDI metrics, including intracellular volume fraction (ICVF), orientation dispersion index (ODI), and isotropic volume fraction (ISO). Differences in NODDI-related metrics between RW and SD were determined using a voxel-wise paired t-test. We identified an association between NODDI metrics and CFT results using Spearman’s correlation coefficient.ResultsSleep deprivation worsened subjects’ performance in the delayed-CFT trial. We observed no significant difference in ICVF and ODI between RW and SD. After SD, subjects showed decreases in ISO, primarily in the prefrontal cortex and temporal lobe, while exhibiting ISO increases in the anterior and posterior cerebellar lobe and cerebellar vermis. Furthermore, ISO change in the left superior, middle and inferior frontal gyrus was significantly correlated with completion time change in delayed-CFT trial performance.ConclusionOur results suggested that SD hardly affected the density and spatial organization of neurites in GM, but the extra-neurite water molecule diffusion process was affected (perhaps resulting from neuroinflammation), which contributed to VSM dysfunction.
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spelling doaj.art-8014d0006deb45fa9bab2530786f77482023-04-19T14:20:03ZengFrontiers Media S.A.Frontiers in Neuroscience1662-453X2023-03-011710.3389/fnins.2023.11448021144802Altered isotropic volume fraction in gray matter after sleep deprivation and its association with visuospatial memory: A neurite orientation dispersion and density imaging studyJia-Hui Lin0Xu-Hui Chen1Ye Wu2Yun-Bin Cao3Hua-Jun Chen4Nao-Xin Huang5Department of Radiology, Fujian Medical University Union Hospital, Fuzhou, ChinaDepartment of Radiology, Fujian Medical University Union Hospital, Fuzhou, ChinaSchool of Computer Science and Engineering, Nanjing University of Science and Technology, Nanjing, ChinaDepartment of Radiology, Fujian Medical University Union Hospital, Fuzhou, ChinaDepartment of Radiology, Fujian Medical University Union Hospital, Fuzhou, ChinaDepartment of Radiology, Fujian Medical University Union Hospital, Fuzhou, ChinaBackground and aimsDiffusion magnetic resonance imaging (dMRI) studies have revealed microstructural abnormalities in white matter resulting from sleep deprivation (SD). This study aimed to adopt neurite orientation dispersion and density imaging (NODDI) to investigate the effect of SD on gray matter (GM) microstructural properties and its association to visuospatial memory (VSM).MethodsTwenty-four healthy women underwent two sessions of dMRI scanning and visuospatial ability assessment by Complex Figure Test (CFT), once during rested wakefulness (RW) and once after 24 h of SD. We calculated NODDI metrics, including intracellular volume fraction (ICVF), orientation dispersion index (ODI), and isotropic volume fraction (ISO). Differences in NODDI-related metrics between RW and SD were determined using a voxel-wise paired t-test. We identified an association between NODDI metrics and CFT results using Spearman’s correlation coefficient.ResultsSleep deprivation worsened subjects’ performance in the delayed-CFT trial. We observed no significant difference in ICVF and ODI between RW and SD. After SD, subjects showed decreases in ISO, primarily in the prefrontal cortex and temporal lobe, while exhibiting ISO increases in the anterior and posterior cerebellar lobe and cerebellar vermis. Furthermore, ISO change in the left superior, middle and inferior frontal gyrus was significantly correlated with completion time change in delayed-CFT trial performance.ConclusionOur results suggested that SD hardly affected the density and spatial organization of neurites in GM, but the extra-neurite water molecule diffusion process was affected (perhaps resulting from neuroinflammation), which contributed to VSM dysfunction.https://www.frontiersin.org/articles/10.3389/fnins.2023.1144802/fullsleep deprivationneurite orientation dispersion and density imaginggray matterisotropic volume fractionvisuospatial memory
spellingShingle Jia-Hui Lin
Xu-Hui Chen
Ye Wu
Yun-Bin Cao
Hua-Jun Chen
Nao-Xin Huang
Altered isotropic volume fraction in gray matter after sleep deprivation and its association with visuospatial memory: A neurite orientation dispersion and density imaging study
Frontiers in Neuroscience
sleep deprivation
neurite orientation dispersion and density imaging
gray matter
isotropic volume fraction
visuospatial memory
title Altered isotropic volume fraction in gray matter after sleep deprivation and its association with visuospatial memory: A neurite orientation dispersion and density imaging study
title_full Altered isotropic volume fraction in gray matter after sleep deprivation and its association with visuospatial memory: A neurite orientation dispersion and density imaging study
title_fullStr Altered isotropic volume fraction in gray matter after sleep deprivation and its association with visuospatial memory: A neurite orientation dispersion and density imaging study
title_full_unstemmed Altered isotropic volume fraction in gray matter after sleep deprivation and its association with visuospatial memory: A neurite orientation dispersion and density imaging study
title_short Altered isotropic volume fraction in gray matter after sleep deprivation and its association with visuospatial memory: A neurite orientation dispersion and density imaging study
title_sort altered isotropic volume fraction in gray matter after sleep deprivation and its association with visuospatial memory a neurite orientation dispersion and density imaging study
topic sleep deprivation
neurite orientation dispersion and density imaging
gray matter
isotropic volume fraction
visuospatial memory
url https://www.frontiersin.org/articles/10.3389/fnins.2023.1144802/full
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