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REM sleep is associated with white matter integrity in cognitively healthy, older adults
There is increasing awareness that self-reported sleep abnormalities are negatively associated with brain structure and function in older adults. Less is known, however, about how objectively measured sleep associates with brain structure. We objectively measured at-home sleep to investigate how sle...
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Published in: | PloS one 2020-07, Vol.15 (7), p.e0235395-e0235395 |
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creator | Altendahl, Marie Cotter, Devyn L Staffaroni, Adam M Wolf, Amy Mumford, Paige Cobigo, Yann Casaletto, Kaitlin Elahi, Fanny Ruoff, Leslie Javed, Samirah Bettcher, Brianne M Fox, Emily You, Michelle Saloner, Rowan Neylan, Thomas C Kramer, Joel H Walsh, Christine M |
description | There is increasing awareness that self-reported sleep abnormalities are negatively associated with brain structure and function in older adults. Less is known, however, about how objectively measured sleep associates with brain structure. We objectively measured at-home sleep to investigate how sleep architecture and sleep quality related to white matter microstructure in older adults. 43 cognitively normal, older adults underwent diffusion tensor imaging (DTI) and a sleep assessment within a six-month period. Participants completed the PSQI, a subjective measure of sleep quality, and used an at-home sleep recorder (Zeo, Inc.) to measure total sleep time (TST), sleep efficiency (SE), and percent time in light sleep (LS), deep sleep (DS), and REM sleep (RS). Multiple regressions predicted fractional anisotropy (FA) and mean diffusivity (MD) of the corpus callosum as a function of total PSQI score, TST, SE, and percent of time spent in each sleep stage, controlling for age and sex. Greater percent time spent in RS was significantly associated with higher FA (β = 0.41, p = 0.007) and lower MD (β = -0.30, p = 0.03). Total PSQI score, TST, SE, and time spent in LS or DS were not significantly associated with FA or MD (p>0.13). Percent time spent in REM sleep, but not quantity of light and deep sleep or subjective/objective measures of sleep quality, positively predicted white matter microstructure integrity. Our results highlight an important link between REM sleep and brain health that has the potential to improve sleep interventions in the elderly. |
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Less is known, however, about how objectively measured sleep associates with brain structure. We objectively measured at-home sleep to investigate how sleep architecture and sleep quality related to white matter microstructure in older adults. 43 cognitively normal, older adults underwent diffusion tensor imaging (DTI) and a sleep assessment within a six-month period. Participants completed the PSQI, a subjective measure of sleep quality, and used an at-home sleep recorder (Zeo, Inc.) to measure total sleep time (TST), sleep efficiency (SE), and percent time in light sleep (LS), deep sleep (DS), and REM sleep (RS). Multiple regressions predicted fractional anisotropy (FA) and mean diffusivity (MD) of the corpus callosum as a function of total PSQI score, TST, SE, and percent of time spent in each sleep stage, controlling for age and sex. Greater percent time spent in RS was significantly associated with higher FA (β = 0.41, p = 0.007) and lower MD (β = -0.30, p = 0.03). Total PSQI score, TST, SE, and time spent in LS or DS were not significantly associated with FA or MD (p>0.13). Percent time spent in REM sleep, but not quantity of light and deep sleep or subjective/objective measures of sleep quality, positively predicted white matter microstructure integrity. Our results highlight an important link between REM sleep and brain health that has the potential to improve sleep interventions in the elderly.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0235395</identifier><identifier>PMID: 32645032</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Abnormalities ; Adults ; Age ; Aged ; Aged, 80 and over ; Aging ; Anisotropy ; Biology and Life Sciences ; Brain ; Brain research ; Cerebral white matter ; Cognition - physiology ; Cognitive ability ; Corpus callosum ; Dementia ; Diffusion ; Diffusion Magnetic Resonance Imaging ; Efficiency ; Elderly ; Eye movements ; Female ; Functional anatomy ; Health aspects ; Humans ; Integrity ; Male ; Medical research ; Medicine and Health Sciences ; Memory ; Mental health ; Microstructure ; Neuroimaging ; Neurology ; Neurosciences ; Older people ; People and Places ; Physical Sciences ; Physiological aspects ; Psychiatry ; Rapid eye movement ; Regression Analysis ; REM sleep ; Research and Analysis Methods ; Sleep ; Sleep (REM) ; Sleep apnea ; Sleep, REM - physiology ; Structure-function relationships ; Substantia alba ; Tensors ; White Matter - anatomy & histology ; White Matter - physiology</subject><ispartof>PloS one, 2020-07, Vol.15 (7), p.e0235395-e0235395</ispartof><rights>COPYRIGHT 2020 Public Library of Science</rights><rights>2020 Altendahl et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2020 Altendahl et al 2020 Altendahl et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c692t-4fa1542b70b7b5f317071eaddf3cb316e9ee35f2c36991d2030b79c5b7f173753</citedby><cites>FETCH-LOGICAL-c692t-4fa1542b70b7b5f317071eaddf3cb316e9ee35f2c36991d2030b79c5b7f173753</cites><orcidid>0000-0003-2282-1531</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.proquest.com/docview/2422010741/fulltextPDF?pq-origsite=primo$$EPDF$$P50$$Gproquest$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.proquest.com/docview/2422010741?pq-origsite=primo$$EHTML$$P50$$Gproquest$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,885,25753,27924,27925,37012,37013,44590,53791,53793,75126</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/32645032$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Najbauer, Joseph</contributor><creatorcontrib>Altendahl, Marie</creatorcontrib><creatorcontrib>Cotter, Devyn L</creatorcontrib><creatorcontrib>Staffaroni, Adam M</creatorcontrib><creatorcontrib>Wolf, Amy</creatorcontrib><creatorcontrib>Mumford, Paige</creatorcontrib><creatorcontrib>Cobigo, Yann</creatorcontrib><creatorcontrib>Casaletto, Kaitlin</creatorcontrib><creatorcontrib>Elahi, Fanny</creatorcontrib><creatorcontrib>Ruoff, Leslie</creatorcontrib><creatorcontrib>Javed, Samirah</creatorcontrib><creatorcontrib>Bettcher, Brianne M</creatorcontrib><creatorcontrib>Fox, Emily</creatorcontrib><creatorcontrib>You, Michelle</creatorcontrib><creatorcontrib>Saloner, Rowan</creatorcontrib><creatorcontrib>Neylan, Thomas C</creatorcontrib><creatorcontrib>Kramer, Joel H</creatorcontrib><creatorcontrib>Walsh, Christine M</creatorcontrib><title>REM sleep is associated with white matter integrity in cognitively healthy, older adults</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>There is increasing awareness that self-reported sleep abnormalities are negatively associated with brain structure and function in older adults. Less is known, however, about how objectively measured sleep associates with brain structure. We objectively measured at-home sleep to investigate how sleep architecture and sleep quality related to white matter microstructure in older adults. 43 cognitively normal, older adults underwent diffusion tensor imaging (DTI) and a sleep assessment within a six-month period. Participants completed the PSQI, a subjective measure of sleep quality, and used an at-home sleep recorder (Zeo, Inc.) to measure total sleep time (TST), sleep efficiency (SE), and percent time in light sleep (LS), deep sleep (DS), and REM sleep (RS). Multiple regressions predicted fractional anisotropy (FA) and mean diffusivity (MD) of the corpus callosum as a function of total PSQI score, TST, SE, and percent of time spent in each sleep stage, controlling for age and sex. Greater percent time spent in RS was significantly associated with higher FA (β = 0.41, p = 0.007) and lower MD (β = -0.30, p = 0.03). Total PSQI score, TST, SE, and time spent in LS or DS were not significantly associated with FA or MD (p>0.13). Percent time spent in REM sleep, but not quantity of light and deep sleep or subjective/objective measures of sleep quality, positively predicted white matter microstructure integrity. Our results highlight an important link between REM sleep and brain health that has the potential to improve sleep interventions in the elderly.</description><subject>Abnormalities</subject><subject>Adults</subject><subject>Age</subject><subject>Aged</subject><subject>Aged, 80 and over</subject><subject>Aging</subject><subject>Anisotropy</subject><subject>Biology and Life Sciences</subject><subject>Brain</subject><subject>Brain research</subject><subject>Cerebral white matter</subject><subject>Cognition - physiology</subject><subject>Cognitive ability</subject><subject>Corpus callosum</subject><subject>Dementia</subject><subject>Diffusion</subject><subject>Diffusion Magnetic Resonance Imaging</subject><subject>Efficiency</subject><subject>Elderly</subject><subject>Eye movements</subject><subject>Female</subject><subject>Functional anatomy</subject><subject>Health aspects</subject><subject>Humans</subject><subject>Integrity</subject><subject>Male</subject><subject>Medical research</subject><subject>Medicine and Health Sciences</subject><subject>Memory</subject><subject>Mental health</subject><subject>Microstructure</subject><subject>Neuroimaging</subject><subject>Neurology</subject><subject>Neurosciences</subject><subject>Older people</subject><subject>People and Places</subject><subject>Physical Sciences</subject><subject>Physiological aspects</subject><subject>Psychiatry</subject><subject>Rapid eye movement</subject><subject>Regression Analysis</subject><subject>REM sleep</subject><subject>Research and Analysis Methods</subject><subject>Sleep</subject><subject>Sleep (REM)</subject><subject>Sleep apnea</subject><subject>Sleep, REM - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Altendahl, Marie</au><au>Cotter, Devyn L</au><au>Staffaroni, Adam M</au><au>Wolf, Amy</au><au>Mumford, Paige</au><au>Cobigo, Yann</au><au>Casaletto, Kaitlin</au><au>Elahi, Fanny</au><au>Ruoff, Leslie</au><au>Javed, Samirah</au><au>Bettcher, Brianne M</au><au>Fox, Emily</au><au>You, Michelle</au><au>Saloner, Rowan</au><au>Neylan, Thomas C</au><au>Kramer, Joel H</au><au>Walsh, Christine M</au><au>Najbauer, Joseph</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>REM sleep is associated with white matter integrity in cognitively healthy, older adults</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2020-07-09</date><risdate>2020</risdate><volume>15</volume><issue>7</issue><spage>e0235395</spage><epage>e0235395</epage><pages>e0235395-e0235395</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>There is increasing awareness that self-reported sleep abnormalities are negatively associated with brain structure and function in older adults. Less is known, however, about how objectively measured sleep associates with brain structure. We objectively measured at-home sleep to investigate how sleep architecture and sleep quality related to white matter microstructure in older adults. 43 cognitively normal, older adults underwent diffusion tensor imaging (DTI) and a sleep assessment within a six-month period. Participants completed the PSQI, a subjective measure of sleep quality, and used an at-home sleep recorder (Zeo, Inc.) to measure total sleep time (TST), sleep efficiency (SE), and percent time in light sleep (LS), deep sleep (DS), and REM sleep (RS). Multiple regressions predicted fractional anisotropy (FA) and mean diffusivity (MD) of the corpus callosum as a function of total PSQI score, TST, SE, and percent of time spent in each sleep stage, controlling for age and sex. Greater percent time spent in RS was significantly associated with higher FA (β = 0.41, p = 0.007) and lower MD (β = -0.30, p = 0.03). Total PSQI score, TST, SE, and time spent in LS or DS were not significantly associated with FA or MD (p>0.13). Percent time spent in REM sleep, but not quantity of light and deep sleep or subjective/objective measures of sleep quality, positively predicted white matter microstructure integrity. Our results highlight an important link between REM sleep and brain health that has the potential to improve sleep interventions in the elderly.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>32645032</pmid><doi>10.1371/journal.pone.0235395</doi><tpages>e0235395</tpages><orcidid>https://orcid.org/0000-0003-2282-1531</orcidid><oa>free_for_read</oa></addata></record> |
fulltext | fulltext |
identifier | ISSN: 1932-6203 |
ispartof | PloS one, 2020-07, Vol.15 (7), p.e0235395-e0235395 |
issn | 1932-6203 1932-6203 |
language | eng |
recordid | cdi_plos_journals_2422010741 |
source | PubMed Central Free; Publicly Available Content Database |
subjects | Abnormalities Adults Age Aged Aged, 80 and over Aging Anisotropy Biology and Life Sciences Brain Brain research Cerebral white matter Cognition - physiology Cognitive ability Corpus callosum Dementia Diffusion Diffusion Magnetic Resonance Imaging Efficiency Elderly Eye movements Female Functional anatomy Health aspects Humans Integrity Male Medical research Medicine and Health Sciences Memory Mental health Microstructure Neuroimaging Neurology Neurosciences Older people People and Places Physical Sciences Physiological aspects Psychiatry Rapid eye movement Regression Analysis REM sleep Research and Analysis Methods Sleep Sleep (REM) Sleep apnea Sleep, REM - physiology Structure-function relationships Substantia alba Tensors White Matter - anatomy & histology White Matter - physiology |
title | REM sleep is associated with white matter integrity in cognitively healthy, older adults |
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