The mediating role of cortical thickness and gray matter volume on sleep slow-wave activity during adolescence
During the course of adolescence, reductions occur in cortical thickness and gray matter (GM) volume, along with a 65% reduction in slow-wave (delta) activity during sleep (SWA) but empirical data linking these structural brain and functional sleep differences, is lacking. Here, we investigated spec...
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| Veröffentlicht in: | Brain Structure and Function 2018-03, Vol.223 (2), p.669-685 |
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| creator | Goldstone, Aimée Willoughby, Adrian R. de Zambotti, Massimiliano Franzen, Peter L. Kwon, Dongjin Pohl, Kilian M. Pfefferbaum, Adolf Sullivan, Edith V. Müller-Oehring, Eva M. Prouty, Devin E. Hasler, Brant P. Clark, Duncan B. Colrain, Ian M. Baker, Fiona C. |
| description | During the course of adolescence, reductions occur in cortical thickness and gray matter (GM) volume, along with a 65% reduction in slow-wave (delta) activity during sleep (SWA) but empirical data linking these structural brain and functional sleep differences, is lacking. Here, we investigated specifically whether age-related differences in cortical thickness and GM volume and cortical thickness accounted for the typical age-related difference in slow-wave (delta) activity (SWA) during sleep. 132 healthy participants (age 12–21 years) from the National Consortium on Alcohol and NeuroDevelopment in Adolescence study were included in this cross-sectional analysis of baseline polysomnographic, electroencephalographic, and magnetic resonance imaging data. By applying mediation models, we identified a large, direct effect of age on SWA in adolescents, which explained 45% of the variance in ultra-SWA (0.3–1 Hz) and 52% of the variance in delta-SWA (1 to |
| doi_str_mv | 10.1007/s00429-017-1509-9 |
| format | Article |
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Here, we investigated specifically whether age-related differences in cortical thickness and GM volume and cortical thickness accounted for the typical age-related difference in slow-wave (delta) activity (SWA) during sleep. 132 healthy participants (age 12–21 years) from the National Consortium on Alcohol and NeuroDevelopment in Adolescence study were included in this cross-sectional analysis of baseline polysomnographic, electroencephalographic, and magnetic resonance imaging data. By applying mediation models, we identified a large, direct effect of age on SWA in adolescents, which explained 45% of the variance in ultra-SWA (0.3–1 Hz) and 52% of the variance in delta-SWA (1 to <4 Hz), where SWA was lower in older adolescents, as has been reported previously. In addition, we provide evidence that the structure of several, predominantly frontal, and parietal brain regions, partially mediated this direct age effect, models including measures of brain structure explained an additional 3–9% of the variance in ultra-SWA and 4–5% of the variance in delta-SWA, with no differences between sexes. Replacing age with pubertal status in models produced similar results. As reductions in GM volume and cortical thickness likely indicate synaptic pruning and myelination, these results suggest that diminished SWA in older, more mature adolescents may largely be driven by such processes within a number of frontal and parietal brain regions.</description><identifier>ISSN: 1863-2653</identifier><identifier>EISSN: 1863-2661</identifier><identifier>EISSN: 0340-2061</identifier><identifier>DOI: 10.1007/s00429-017-1509-9</identifier><identifier>PMID: 28913599</identifier><language>eng</language><publisher>Berlin/Heidelberg: Springer Berlin Heidelberg</publisher><subject>Adolescence ; Adolescent ; Adolescents ; Age ; Age Factors ; Biomedical and Life Sciences ; Biomedicine ; Brain ; Brain Mapping ; Cell Biology ; Cerebral Cortex - diagnostic imaging ; Cerebral Cortex - physiology ; Child ; Child development ; Cortex ; EEG ; Female ; Functional Laterality ; Gray Matter - diagnostic imaging ; Gray Matter - physiology ; Humans ; Image Processing, Computer-Assisted ; Magnetic Resonance Imaging ; Male ; Myelination ; Neuroimaging ; Neurology ; Neurosciences ; Original Article ; Sleep ; Sleep, Slow-Wave - physiology ; Structure-function relationships ; Substantia grisea ; Teenagers ; Young Adult</subject><ispartof>Brain Structure and Function, 2018-03, Vol.223 (2), p.669-685</ispartof><rights>Springer-Verlag GmbH Germany 2017</rights><rights>Brain Structure and Function is a copyright of Springer, (2017). All Rights Reserved.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c470t-f38744f37d23403aac995e210404ee347902b7a3cc775abcc348237491bcc5ca3</citedby><cites>FETCH-LOGICAL-c470t-f38744f37d23403aac995e210404ee347902b7a3cc775abcc348237491bcc5ca3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://link.springer.com/content/pdf/10.1007/s00429-017-1509-9$$EPDF$$P50$$Gspringer$$H</linktopdf><linktohtml>$$Uhttps://link.springer.com/10.1007/s00429-017-1509-9$$EHTML$$P50$$Gspringer$$H</linktohtml><link.rule.ids>230,314,776,780,881,27901,27902,41464,42533,51294</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/28913599$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Goldstone, Aimée</creatorcontrib><creatorcontrib>Willoughby, Adrian R.</creatorcontrib><creatorcontrib>de Zambotti, Massimiliano</creatorcontrib><creatorcontrib>Franzen, Peter L.</creatorcontrib><creatorcontrib>Kwon, Dongjin</creatorcontrib><creatorcontrib>Pohl, Kilian M.</creatorcontrib><creatorcontrib>Pfefferbaum, Adolf</creatorcontrib><creatorcontrib>Sullivan, Edith V.</creatorcontrib><creatorcontrib>Müller-Oehring, Eva M.</creatorcontrib><creatorcontrib>Prouty, Devin E.</creatorcontrib><creatorcontrib>Hasler, Brant P.</creatorcontrib><creatorcontrib>Clark, Duncan B.</creatorcontrib><creatorcontrib>Colrain, Ian M.</creatorcontrib><creatorcontrib>Baker, Fiona C.</creatorcontrib><title>The mediating role of cortical thickness and gray matter volume on sleep slow-wave activity during adolescence</title><title>Brain Structure and Function</title><addtitle>Brain Struct Funct</addtitle><addtitle>Brain Struct Funct</addtitle><description>During the course of adolescence, reductions occur in cortical thickness and gray matter (GM) volume, along with a 65% reduction in slow-wave (delta) activity during sleep (SWA) but empirical data linking these structural brain and functional sleep differences, is lacking. Here, we investigated specifically whether age-related differences in cortical thickness and GM volume and cortical thickness accounted for the typical age-related difference in slow-wave (delta) activity (SWA) during sleep. 132 healthy participants (age 12–21 years) from the National Consortium on Alcohol and NeuroDevelopment in Adolescence study were included in this cross-sectional analysis of baseline polysomnographic, electroencephalographic, and magnetic resonance imaging data. By applying mediation models, we identified a large, direct effect of age on SWA in adolescents, which explained 45% of the variance in ultra-SWA (0.3–1 Hz) and 52% of the variance in delta-SWA (1 to <4 Hz), where SWA was lower in older adolescents, as has been reported previously. In addition, we provide evidence that the structure of several, predominantly frontal, and parietal brain regions, partially mediated this direct age effect, models including measures of brain structure explained an additional 3–9% of the variance in ultra-SWA and 4–5% of the variance in delta-SWA, with no differences between sexes. Replacing age with pubertal status in models produced similar results. As reductions in GM volume and cortical thickness likely indicate synaptic pruning and myelination, these results suggest that diminished SWA in older, more mature adolescents may largely be driven by such processes within a number of frontal and parietal brain regions.</description><subject>Adolescence</subject><subject>Adolescent</subject><subject>Adolescents</subject><subject>Age</subject><subject>Age Factors</subject><subject>Biomedical and Life Sciences</subject><subject>Biomedicine</subject><subject>Brain</subject><subject>Brain Mapping</subject><subject>Cell Biology</subject><subject>Cerebral Cortex - diagnostic imaging</subject><subject>Cerebral Cortex - physiology</subject><subject>Child</subject><subject>Child development</subject><subject>Cortex</subject><subject>EEG</subject><subject>Female</subject><subject>Functional Laterality</subject><subject>Gray Matter - diagnostic imaging</subject><subject>Gray Matter - physiology</subject><subject>Humans</subject><subject>Image Processing, Computer-Assisted</subject><subject>Magnetic Resonance Imaging</subject><subject>Male</subject><subject>Myelination</subject><subject>Neuroimaging</subject><subject>Neurology</subject><subject>Neurosciences</subject><subject>Original Article</subject><subject>Sleep</subject><subject>Sleep, Slow-Wave - physiology</subject><subject>Structure-function relationships</subject><subject>Substantia grisea</subject><subject>Teenagers</subject><subject>Young Adult</subject><issn>1863-2653</issn><issn>1863-2661</issn><issn>0340-2061</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2018</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>BENPR</sourceid><recordid>eNp1kU1v1DAQhi0EoqXwA7ggS1y4BPyVdXxBQlWhlSpxKWdr1pnsuiT2Yjtb7b_H0ZblQ-Jij-Rn3vE7LyGvOXvPGdMfMmNKmIZx3fCWmcY8Iee8W8lGrFb86alu5Rl5kfM9Y63puHlOzkRnuGyNOSfhbot0wt5D8WFDUxyRxoG6mIp3MNKy9e57wJwphJ5uEhzoBKVgovs4zlOFA80j4q6e8aF5gD1ScMXvfTnQfk6LKPRVNTsMDl-SZwOMGV893hfk2-eru8vr5vbrl5vLT7eNU5qVZpCdVmqQuhdSMQngjGlRcKaYQpRKGybWGqRzWrewdk6qTkitDK9160BekI9H3d28ru7q7JJgtLvkJ0gHG8Hbv1-C39pN3Nu2q7sRrAq8exRI8ceMudjJVwvjCAHjnC03qq6zU5xX9O0_6H2cU6j2rKgpaaOZWCh-pFyKOSccTp_hzC5p2mOatqZplzStqT1v_nRx6vgVXwXEEci7ZdOYfo_-v-pPmjysJw</recordid><startdate>20180301</startdate><enddate>20180301</enddate><creator>Goldstone, Aimée</creator><creator>Willoughby, Adrian R.</creator><creator>de Zambotti, Massimiliano</creator><creator>Franzen, Peter L.</creator><creator>Kwon, Dongjin</creator><creator>Pohl, Kilian M.</creator><creator>Pfefferbaum, Adolf</creator><creator>Sullivan, Edith V.</creator><creator>Müller-Oehring, Eva M.</creator><creator>Prouty, Devin E.</creator><creator>Hasler, Brant P.</creator><creator>Clark, Duncan B.</creator><creator>Colrain, Ian M.</creator><creator>Baker, Fiona C.</creator><general>Springer Berlin Heidelberg</general><general>Springer Nature B.V</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>3V.</scope><scope>7RV</scope><scope>7TK</scope><scope>7X7</scope><scope>7XB</scope><scope>88A</scope><scope>88E</scope><scope>88G</scope><scope>8AO</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>KB0</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M2M</scope><scope>M7P</scope><scope>NAPCQ</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>PSYQQ</scope><scope>Q9U</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>20180301</creationdate><title>The mediating role of cortical thickness and gray matter volume on sleep slow-wave activity during adolescence</title><author>Goldstone, Aimée ; Willoughby, Adrian R. ; de Zambotti, Massimiliano ; Franzen, Peter L. ; Kwon, Dongjin ; Pohl, Kilian M. ; Pfefferbaum, Adolf ; Sullivan, Edith V. ; Müller-Oehring, Eva M. ; Prouty, Devin E. ; Hasler, Brant P. ; Clark, Duncan B. ; Colrain, Ian M. ; Baker, Fiona C.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c470t-f38744f37d23403aac995e210404ee347902b7a3cc775abcc348237491bcc5ca3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2018</creationdate><topic>Adolescence</topic><topic>Adolescent</topic><topic>Adolescents</topic><topic>Age</topic><topic>Age Factors</topic><topic>Biomedical and Life Sciences</topic><topic>Biomedicine</topic><topic>Brain</topic><topic>Brain Mapping</topic><topic>Cell Biology</topic><topic>Cerebral Cortex - diagnostic imaging</topic><topic>Cerebral Cortex - physiology</topic><topic>Child</topic><topic>Child development</topic><topic>Cortex</topic><topic>EEG</topic><topic>Female</topic><topic>Functional Laterality</topic><topic>Gray Matter - diagnostic imaging</topic><topic>Gray Matter - physiology</topic><topic>Humans</topic><topic>Image Processing, Computer-Assisted</topic><topic>Magnetic Resonance Imaging</topic><topic>Male</topic><topic>Myelination</topic><topic>Neuroimaging</topic><topic>Neurology</topic><topic>Neurosciences</topic><topic>Original Article</topic><topic>Sleep</topic><topic>Sleep, Slow-Wave - physiology</topic><topic>Structure-function relationships</topic><topic>Substantia grisea</topic><topic>Teenagers</topic><topic>Young Adult</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Goldstone, Aimée</creatorcontrib><creatorcontrib>Willoughby, Adrian R.</creatorcontrib><creatorcontrib>de Zambotti, Massimiliano</creatorcontrib><creatorcontrib>Franzen, Peter L.</creatorcontrib><creatorcontrib>Kwon, Dongjin</creatorcontrib><creatorcontrib>Pohl, Kilian M.</creatorcontrib><creatorcontrib>Pfefferbaum, Adolf</creatorcontrib><creatorcontrib>Sullivan, Edith V.</creatorcontrib><creatorcontrib>Müller-Oehring, Eva M.</creatorcontrib><creatorcontrib>Prouty, Devin E.</creatorcontrib><creatorcontrib>Hasler, Brant P.</creatorcontrib><creatorcontrib>Clark, Duncan B.</creatorcontrib><creatorcontrib>Colrain, Ian M.</creatorcontrib><creatorcontrib>Baker, Fiona C.</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Nursing & Allied Health Database</collection><collection>Neurosciences Abstracts</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Biology Database (Alumni Edition)</collection><collection>Medical Database (Alumni Edition)</collection><collection>Psychology Database (Alumni)</collection><collection>ProQuest Pharma Collection</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest Central UK/Ireland</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Natural Science Collection</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Nursing & Allied Health Database (Alumni Edition)</collection><collection>ProQuest Biological Science Collection</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>ProQuest Psychology</collection><collection>Biological Science Database</collection><collection>Nursing & Allied Health Premium</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>ProQuest One Psychology</collection><collection>ProQuest Central Basic</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Brain Structure and Function</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Goldstone, Aimée</au><au>Willoughby, Adrian R.</au><au>de Zambotti, Massimiliano</au><au>Franzen, Peter L.</au><au>Kwon, Dongjin</au><au>Pohl, Kilian M.</au><au>Pfefferbaum, Adolf</au><au>Sullivan, Edith V.</au><au>Müller-Oehring, Eva M.</au><au>Prouty, Devin E.</au><au>Hasler, Brant P.</au><au>Clark, Duncan B.</au><au>Colrain, Ian M.</au><au>Baker, Fiona C.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>The mediating role of cortical thickness and gray matter volume on sleep slow-wave activity during adolescence</atitle><jtitle>Brain Structure and Function</jtitle><stitle>Brain Struct Funct</stitle><addtitle>Brain Struct Funct</addtitle><date>2018-03-01</date><risdate>2018</risdate><volume>223</volume><issue>2</issue><spage>669</spage><epage>685</epage><pages>669-685</pages><issn>1863-2653</issn><eissn>1863-2661</eissn><eissn>0340-2061</eissn><abstract>During the course of adolescence, reductions occur in cortical thickness and gray matter (GM) volume, along with a 65% reduction in slow-wave (delta) activity during sleep (SWA) but empirical data linking these structural brain and functional sleep differences, is lacking. Here, we investigated specifically whether age-related differences in cortical thickness and GM volume and cortical thickness accounted for the typical age-related difference in slow-wave (delta) activity (SWA) during sleep. 132 healthy participants (age 12–21 years) from the National Consortium on Alcohol and NeuroDevelopment in Adolescence study were included in this cross-sectional analysis of baseline polysomnographic, electroencephalographic, and magnetic resonance imaging data. By applying mediation models, we identified a large, direct effect of age on SWA in adolescents, which explained 45% of the variance in ultra-SWA (0.3–1 Hz) and 52% of the variance in delta-SWA (1 to <4 Hz), where SWA was lower in older adolescents, as has been reported previously. In addition, we provide evidence that the structure of several, predominantly frontal, and parietal brain regions, partially mediated this direct age effect, models including measures of brain structure explained an additional 3–9% of the variance in ultra-SWA and 4–5% of the variance in delta-SWA, with no differences between sexes. Replacing age with pubertal status in models produced similar results. As reductions in GM volume and cortical thickness likely indicate synaptic pruning and myelination, these results suggest that diminished SWA in older, more mature adolescents may largely be driven by such processes within a number of frontal and parietal brain regions.</abstract><cop>Berlin/Heidelberg</cop><pub>Springer Berlin Heidelberg</pub><pmid>28913599</pmid><doi>10.1007/s00429-017-1509-9</doi><tpages>17</tpages><oa>free_for_read</oa></addata></record> |
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| ispartof | Brain Structure and Function, 2018-03, Vol.223 (2), p.669-685 |
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| subjects | Adolescence Adolescent Adolescents Age Age Factors Biomedical and Life Sciences Biomedicine Brain Brain Mapping Cell Biology Cerebral Cortex - diagnostic imaging Cerebral Cortex - physiology Child Child development Cortex EEG Female Functional Laterality Gray Matter - diagnostic imaging Gray Matter - physiology Humans Image Processing, Computer-Assisted Magnetic Resonance Imaging Male Myelination Neuroimaging Neurology Neurosciences Original Article Sleep Sleep, Slow-Wave - physiology Structure-function relationships Substantia grisea Teenagers Young Adult |
| title | The mediating role of cortical thickness and gray matter volume on sleep slow-wave activity during adolescence |
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