Habitual sleep durations and subjective sleep quality predict white matter differences in the human brain

Sakh Khalsa , Joanne R. Hale , Aimee Goldstone , Rebecca S. Wilson , Stephen D. Mayhew , Manny Bagary , Andrew P. Bagshaw
{"title":"Habitual sleep durations and subjective sleep quality predict white matter differences in the human brain","authors":"Sakh Khalsa ,&nbsp;Joanne R. Hale ,&nbsp;Aimee Goldstone ,&nbsp;Rebecca S. Wilson ,&nbsp;Stephen D. Mayhew ,&nbsp;Manny Bagary ,&nbsp;Andrew P. Bagshaw","doi":"10.1016/j.nbscr.2017.03.001","DOIUrl":null,"url":null,"abstract":"<div><p>Self-imposed short sleep durations are increasingly commonplace in society, and have considerable health and performance implications for individuals. Reduced sleep duration over multiple nights has similar behavioural effects to those observed following acute total sleep deprivation, suggesting that lack of sleep affects brain function cumulatively. A link between habitual sleep patterns and functional connectivity has previously been observed, and the effect of sleep duration on the brain's intrinsic functional architecture may provide a link between sleep status and cognition. However, it is currently not known whether differences in habitual sleep patterns across individuals are related to changes in the brain's white matter, which underlies structural connectivity. In the present study we use diffusion–weighted imaging and a group comparison application of tract based spatial statistics (TBSS) to investigate changes to fractional anisotropy (FA) and mean diffusivity (MD) in relation to sleep duration and quality, hypothesising that white matter metrics would be positively associated with sleep duration and quality. Diffusion weighted imaging data was acquired from a final cohort of 33 (23–29 years, 10 female, mean 25.4 years) participants. Sleep patterns were assessed for a 14<!--> <!-->day period using wrist actigraphs and sleep diaries, and subjective sleep quality with the Pittsburgh Sleep Quality Index (PSQI). Median splits based on total sleep time and PSQI were used to create groups of shorter/longer and poorer/better sleepers, whose imaging data was compared using TBSS followed by post-hoc correlation analysis in regions identified as significantly different between the groups<strong>.</strong> There were significant positive correlations between sleep duration and FA in the left orbito-frontal region and the right superior corona radiata, and significant negative correlations between sleep duration and MD in right orbito-frontal white matter and the right inferior longitudinal fasciculus. Improved sleep quality was positively correlated with FA in left caudate nucleus, white matter tracts to the left orbito-frontal region, the left anterior cingulum bundle and the white matter tracts associated with the right operculum and insula, and negatively correlated with MD in left orbito-frontal white matter and the left anterior cingulum bundle. Our findings suggest that reduced cumulative total sleep time (cTST) and poorer subjective sleep quality are associated with subtle white matter micro-architectural changes. The regions we identified as being related to habitual sleep patterns were restricted to the frontal and temporal lobes, and the functions they support are consistent with those which have previously been demonstrated as being affected by short sleep durations (e.g., attention, cognitive control, memory). Examining how inter-individual differences in brain structure are related to habitual sleep patterns could help to shed light on the mechanisms by which sleep habits are associated with brain function, behaviour and cognition, as well as potentially the networks and systems responsible for variations in sleep patterns themselves.</p></div>","PeriodicalId":37827,"journal":{"name":"Neurobiology of Sleep and Circadian Rhythms","volume":null,"pages":null},"PeriodicalIF":0.0000,"publicationDate":"2017-06-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://sci-hub-pdf.com/10.1016/j.nbscr.2017.03.001","citationCount":"40","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Neurobiology of Sleep and Circadian Rhythms","FirstCategoryId":"1085","ListUrlMain":"https://www.sciencedirect.com/science/article/pii/S2451994416300256","RegionNum":0,"RegionCategory":null,"ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q2","JCRName":"Medicine","Score":null,"Total":0}
引用次数: 40

Abstract

Self-imposed short sleep durations are increasingly commonplace in society, and have considerable health and performance implications for individuals. Reduced sleep duration over multiple nights has similar behavioural effects to those observed following acute total sleep deprivation, suggesting that lack of sleep affects brain function cumulatively. A link between habitual sleep patterns and functional connectivity has previously been observed, and the effect of sleep duration on the brain's intrinsic functional architecture may provide a link between sleep status and cognition. However, it is currently not known whether differences in habitual sleep patterns across individuals are related to changes in the brain's white matter, which underlies structural connectivity. In the present study we use diffusion–weighted imaging and a group comparison application of tract based spatial statistics (TBSS) to investigate changes to fractional anisotropy (FA) and mean diffusivity (MD) in relation to sleep duration and quality, hypothesising that white matter metrics would be positively associated with sleep duration and quality. Diffusion weighted imaging data was acquired from a final cohort of 33 (23–29 years, 10 female, mean 25.4 years) participants. Sleep patterns were assessed for a 14 day period using wrist actigraphs and sleep diaries, and subjective sleep quality with the Pittsburgh Sleep Quality Index (PSQI). Median splits based on total sleep time and PSQI were used to create groups of shorter/longer and poorer/better sleepers, whose imaging data was compared using TBSS followed by post-hoc correlation analysis in regions identified as significantly different between the groups. There were significant positive correlations between sleep duration and FA in the left orbito-frontal region and the right superior corona radiata, and significant negative correlations between sleep duration and MD in right orbito-frontal white matter and the right inferior longitudinal fasciculus. Improved sleep quality was positively correlated with FA in left caudate nucleus, white matter tracts to the left orbito-frontal region, the left anterior cingulum bundle and the white matter tracts associated with the right operculum and insula, and negatively correlated with MD in left orbito-frontal white matter and the left anterior cingulum bundle. Our findings suggest that reduced cumulative total sleep time (cTST) and poorer subjective sleep quality are associated with subtle white matter micro-architectural changes. The regions we identified as being related to habitual sleep patterns were restricted to the frontal and temporal lobes, and the functions they support are consistent with those which have previously been demonstrated as being affected by short sleep durations (e.g., attention, cognitive control, memory). Examining how inter-individual differences in brain structure are related to habitual sleep patterns could help to shed light on the mechanisms by which sleep habits are associated with brain function, behaviour and cognition, as well as potentially the networks and systems responsible for variations in sleep patterns themselves.

Abstract Image

Abstract Image

Abstract Image

查看原文
分享 分享
微信好友 朋友圈 QQ好友 复制链接
本刊更多论文
习惯性睡眠时间和主观睡眠质量可以预测人类大脑中白质的差异
自我强加的短睡眠时间在社会上越来越普遍,对个人的健康和表现有相当大的影响。连续多个夜晚睡眠时间减少对行为的影响与急性完全睡眠剥夺后观察到的相似,这表明睡眠不足会逐渐影响大脑功能。习惯睡眠模式和功能连接之间的联系此前已经被观察到,睡眠持续时间对大脑内在功能结构的影响可能提供了睡眠状态和认知之间的联系。然而,目前尚不清楚个体之间习惯性睡眠模式的差异是否与大脑白质的变化有关,而大脑白质是结构连接的基础。在本研究中,我们使用弥散加权成像和基于通道空间统计(TBSS)的组比较应用来研究分数各向异性(FA)和平均弥散性(MD)与睡眠持续时间和质量的关系,并假设白质指标与睡眠持续时间和质量呈正相关。弥散加权成像数据来自最终队列的33名参与者(23-29岁,10名女性,平均25.4岁)。研究人员使用腕部活动记录仪和睡眠日记评估了14天的睡眠模式,并使用匹兹堡睡眠质量指数(PSQI)评估了主观睡眠质量。基于总睡眠时间和PSQI的中位数分割被用于创建短/长和差/好睡眠的组,其成像数据使用TBSS进行比较,然后在确定组间显著差异的区域进行事后相关分析。睡眠时间与左眶额区和右上辐射冠区FA呈显著正相关,与右眶额白质和右下纵束MD呈显著负相关。改善睡眠质量与左尾状核FA、左侧眶额区白质束、左侧前扣带束以及与右脑盖和脑岛相关的白质束呈正相关,与左侧眶额白质和左侧前扣带束MD呈负相关。我们的研究结果表明,累积总睡眠时间(cTST)的减少和主观睡眠质量的下降与细微的白质微结构变化有关。我们确定的与习惯性睡眠模式相关的区域仅限于额叶和颞叶,它们支持的功能与之前被证明受到短睡眠时间影响的功能(例如,注意力、认知控制、记忆)一致。研究大脑结构的个体间差异与习惯性睡眠模式之间的关系,有助于揭示睡眠习惯与大脑功能、行为和认知之间的关系机制,以及潜在的导致睡眠模式变化的网络和系统。
本文章由计算机程序翻译,如有差异,请以英文原文为准。
求助全文
约1分钟内获得全文 去求助
来源期刊
Neurobiology of Sleep and Circadian Rhythms
Neurobiology of Sleep and Circadian Rhythms Neuroscience-Behavioral Neuroscience
CiteScore
4.50
自引率
0.00%
发文量
9
审稿时长
69 days
期刊介绍: Neurobiology of Sleep and Circadian Rhythms is a multidisciplinary journal for the publication of original research and review articles on basic and translational research into sleep and circadian rhythms. The journal focuses on topics covering the mechanisms of sleep/wake and circadian regulation from molecular to systems level, and on the functional consequences of sleep and circadian disruption. A key aim of the journal is the translation of basic research findings to understand and treat sleep and circadian disorders. Topics include, but are not limited to: Basic and translational research, Molecular mechanisms, Genetics and epigenetics, Inflammation and immunology, Memory and learning, Neurological and neurodegenerative diseases, Neuropsychopharmacology and neuroendocrinology, Behavioral sleep and circadian disorders, Shiftwork, Social jetlag.
期刊最新文献
Synergy between time-restricted feeding and time-restricted running is necessary to shift the muscle clock in male wistar rats Gender differences in sleep quality among Iranian traditional and industrial drug users Development of Sleep and Circadian Rhythms: Function and Dysfunction. Effects of age and sex on photoperiod modulation of nucleus accumbens monoamine content and release in adolescence and adulthood The impact of long haul travel on the sleep of elite athletes
×
引用
GB/T 7714-2015
复制
MLA
复制
APA
复制
导出至
BibTeX EndNote RefMan NoteFirst NoteExpress
×
×
提示
您的信息不完整,为了账户安全,请先补充。
现在去补充
×
提示
您因"违规操作"
具体请查看互助需知
我知道了
×
提示
现在去查看 取消
×
提示
确定
0
微信
客服QQ
Book学术公众号 扫码关注我们
反馈
×
意见反馈
请填写您的意见或建议
请填写您的手机或邮箱
已复制链接
已复制链接
快去分享给好友吧!
我知道了
×
扫码分享
扫码分享
Book学术官方微信
Book学术文献互助
Book学术文献互助群
群 号:481959085
Book学术
文献互助 智能选刊 最新文献 互助须知 联系我们:info@booksci.cn
Book学术提供免费学术资源搜索服务,方便国内外学者检索中英文文献。致力于提供最便捷和优质的服务体验。
Copyright © 2023 Book学术 All rights reserved.
ghs 京公网安备 11010802042870号 京ICP备2023020795号-1