Plasticity and Susceptibility of Brain Morphometry Alterations to Insufficient Sleep

Background: Insufficient sleep is common in daily life and can lead to cognitive impairment. Sleep disturbance also exists in neuropsychiatric diseases. However, whether and how acute and chronic sleep loss affect brain morphology remain largely unknown.Methods: We used voxel-based morphology method...

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Main Authors: Xi-Jian Dai, Jian Jiang, Zhiqiang Zhang, Xiao Nie, Bi-Xia Liu, Li Pei, Honghan Gong, Jianping Hu, Guangming Lu, Yang Zhan
Format: Article
Language:English
Published: Frontiers Media S.A. 2018-06-01
Series:Frontiers in Psychiatry
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fpsyt.2018.00266/full
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author Xi-Jian Dai
Xi-Jian Dai
Jian Jiang
Zhiqiang Zhang
Xiao Nie
Xiao Nie
Bi-Xia Liu
Li Pei
Honghan Gong
Jianping Hu
Guangming Lu
Yang Zhan
spellingShingle Xi-Jian Dai
Xi-Jian Dai
Jian Jiang
Zhiqiang Zhang
Xiao Nie
Xiao Nie
Bi-Xia Liu
Li Pei
Honghan Gong
Jianping Hu
Guangming Lu
Yang Zhan
Plasticity and Susceptibility of Brain Morphometry Alterations to Insufficient Sleep
Frontiers in Psychiatry
insomnia
sleep deprivation
voxel-based morphometry
gray matter
attention network test
spatial working memory
author_facet Xi-Jian Dai
Xi-Jian Dai
Jian Jiang
Zhiqiang Zhang
Xiao Nie
Xiao Nie
Bi-Xia Liu
Li Pei
Honghan Gong
Jianping Hu
Guangming Lu
Yang Zhan
author_sort Xi-Jian Dai
title Plasticity and Susceptibility of Brain Morphometry Alterations to Insufficient Sleep
title_short Plasticity and Susceptibility of Brain Morphometry Alterations to Insufficient Sleep
title_full Plasticity and Susceptibility of Brain Morphometry Alterations to Insufficient Sleep
title_fullStr Plasticity and Susceptibility of Brain Morphometry Alterations to Insufficient Sleep
title_full_unstemmed Plasticity and Susceptibility of Brain Morphometry Alterations to Insufficient Sleep
title_sort plasticity and susceptibility of brain morphometry alterations to insufficient sleep
publisher Frontiers Media S.A.
series Frontiers in Psychiatry
issn 1664-0640
publishDate 2018-06-01
description Background: Insufficient sleep is common in daily life and can lead to cognitive impairment. Sleep disturbance also exists in neuropsychiatric diseases. However, whether and how acute and chronic sleep loss affect brain morphology remain largely unknown.Methods: We used voxel-based morphology method to study the brain structural changes during sleep deprivation (SD) at six time points of rested wakefulness, 20, 24, 32, 36 h SD, and after one night sleep in 22 healthy subjects, and in 39 patients with chronic primary insomnia relative to 39 status-matched good sleepers. Attention network and spatial memory tests were performed at each SD time point in the SD Procedure. The longitudinal data were analyzed using one-way repeated measures ANOVA, and post-hoc analysis was used to determine the between-group differences.Results: Acute SD is associated with widespread gray matter volume (GMV) changes in the thalamus, cerebellum, insula and parietal cortex. Insomnia is associated with increased GMV in temporal cortex, insula and cerebellum. Acute SD is associated with brain atrophy and as SD hours prolong more areas show reduced GMV, and after one night sleep the brain atrophy is restored and replaced by increased GMV in brain areas. SD has accumulative negative effects on attention and working memory.Conclusions: Acute SD and insomnia exhibit distinct morphological changes of GMV. SD has accumulative negative effects on brain morphology and advanced cognitive function. The altered GMV may provide neurobiological basis for attention and memory impairments following sleep loss.Statement of significanceSleep is less frequently studied using imaging techniques than neurological and psychiatric disorders. Whether and how acute and chronic sleep loss affect brain morphology remain largely unknown. We used voxel-based morphology method to study brain structural changes in healthy subjects over multiple time points during sleep deprivation (SD) status and in patients with chronic insomnia. We found that prolonged acute SD together with one night sleep recovery exhibits accumulative atrophic effect and recovering plasticity on brain morphology, in line with behavioral changes on attentional tasks. Furthermore, acute SD and chronic insomnia exhibit distinct morphological changes of gray matter volume (GMV) but they also share overlapping GMV changes. The altered GMV may provide structural basis for attention and memory impairments following sleep loss.
topic insomnia
sleep deprivation
voxel-based morphometry
gray matter
attention network test
spatial working memory
url https://www.frontiersin.org/article/10.3389/fpsyt.2018.00266/full
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spelling doaj-eaafce570f874836a2e951b6e0c19d882020-11-24T23:10:44ZengFrontiers Media S.A.Frontiers in Psychiatry1664-06402018-06-01910.3389/fpsyt.2018.00266381031Plasticity and Susceptibility of Brain Morphometry Alterations to Insufficient SleepXi-Jian Dai0Xi-Jian Dai1Jian Jiang2Zhiqiang Zhang3Xiao Nie4Xiao Nie5Bi-Xia Liu6Li Pei7Honghan Gong8Jianping Hu9Guangming Lu10Yang Zhan11Department of Medical Imaging, Medical School of Nanjing University, Jinling Hospital, Nanjing, ChinaDepartment of Radiology, The First Affiliated Hospital of Nanchang University, Nangchang, ChinaDepartment of Radiology, The First Affiliated Hospital of Nanchang University, Nangchang, ChinaDepartment of Medical Imaging, Medical School of Nanjing University, Jinling Hospital, Nanjing, ChinaDepartment of Radiology, The First Affiliated Hospital of Nanchang University, Nangchang, ChinaDepartment of Radiology, Yiyang Central Hospital, Yiyang, ChinaDepartment of ICU, Jiangxi Cancer Hospital, Nanchang, ChinaDepartment of Radiology, The First Affiliated Hospital of Nanchang University, Nangchang, ChinaDepartment of Radiology, The First Affiliated Hospital of Nanchang University, Nangchang, ChinaDepartment of Medical Imaging, Medical School of Nanjing University, Jinling Hospital, Nanjing, ChinaDepartment of Medical Imaging, Medical School of Nanjing University, Jinling Hospital, Nanjing, ChinaBrain Cognition and Brain Disease Institute, Shenzhen Institutes of Advanced Technology, Chinese Academy of Sciences, Shenzhen, ChinaBackground: Insufficient sleep is common in daily life and can lead to cognitive impairment. Sleep disturbance also exists in neuropsychiatric diseases. However, whether and how acute and chronic sleep loss affect brain morphology remain largely unknown.Methods: We used voxel-based morphology method to study the brain structural changes during sleep deprivation (SD) at six time points of rested wakefulness, 20, 24, 32, 36 h SD, and after one night sleep in 22 healthy subjects, and in 39 patients with chronic primary insomnia relative to 39 status-matched good sleepers. Attention network and spatial memory tests were performed at each SD time point in the SD Procedure. The longitudinal data were analyzed using one-way repeated measures ANOVA, and post-hoc analysis was used to determine the between-group differences.Results: Acute SD is associated with widespread gray matter volume (GMV) changes in the thalamus, cerebellum, insula and parietal cortex. Insomnia is associated with increased GMV in temporal cortex, insula and cerebellum. Acute SD is associated with brain atrophy and as SD hours prolong more areas show reduced GMV, and after one night sleep the brain atrophy is restored and replaced by increased GMV in brain areas. SD has accumulative negative effects on attention and working memory.Conclusions: Acute SD and insomnia exhibit distinct morphological changes of GMV. SD has accumulative negative effects on brain morphology and advanced cognitive function. The altered GMV may provide neurobiological basis for attention and memory impairments following sleep loss.Statement of significanceSleep is less frequently studied using imaging techniques than neurological and psychiatric disorders. Whether and how acute and chronic sleep loss affect brain morphology remain largely unknown. We used voxel-based morphology method to study brain structural changes in healthy subjects over multiple time points during sleep deprivation (SD) status and in patients with chronic insomnia. We found that prolonged acute SD together with one night sleep recovery exhibits accumulative atrophic effect and recovering plasticity on brain morphology, in line with behavioral changes on attentional tasks. Furthermore, acute SD and chronic insomnia exhibit distinct morphological changes of gray matter volume (GMV) but they also share overlapping GMV changes. The altered GMV may provide structural basis for attention and memory impairments following sleep loss.https://www.frontiersin.org/article/10.3389/fpsyt.2018.00266/fullinsomniasleep deprivationvoxel-based morphometrygray matterattention network testspatial working memory