Neural mechanisms that promote food consumption following sleep loss and social stress: an fMRI study in adolescent girls with overweight/obesity
Abstract Study Objectives Insufficient sleep and social stress are associated with weight gain and obesity development in adolescent girls. Functional magnetic resonance imaging (fMRI) research suggests that altered engagement of emotion-related neural networks may explain overeating when under stre...
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Veröffentlicht in: | Sleep (New York, N.Y.) N.Y.), 2022-03, Vol.45 (3), p.1 |
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creator | Jensen, Chad D Zaugg, Kelsey K Muncy, Nathan M Allen, Whitney D Blackburn, Robyn Duraccio, Kara M Barnett, Kimberly A Brock Kirwan, C Jarcho, Johanna M |
description | Abstract
Study Objectives
Insufficient sleep and social stress are associated with weight gain and obesity development in adolescent girls. Functional magnetic resonance imaging (fMRI) research suggests that altered engagement of emotion-related neural networks may explain overeating when under stress. The purpose of this study is to explore the effects of acute sleep restriction on female adolescents’ neural responding during social evaluative stress and their subsequent eating behavior.
Methods
Forty-two adolescent females (ages 15−18 years) with overweight or obesity completed a social stress induction task in which they were told they would be rated by peers based on their photograph and profile. Participants were randomly assigned to one night of sleep deprivation or 9 h of sleep the night before undergoing fMRI while receiving positive and negative evaluations from their peers. After which, subjects participated in an ad libitum buffet.
Results
Sleep deprived, relative to nondeprived girls had distinct patterns of neural engagement to positive and negative evaluation in anterior, mid, and posterior aspects of midline brain structures. Moreover, a sleep deprivation-by-evaluation valence-by-caloric intake interaction emerged in bilateral dorsal anterior cingulate. Among sleep deprived girls, greater engagement during negative, but not positive, feedback was associated with lower caloric intake. This was not observed for nonsleep deprived girls.
Conclusions
Results suggest an interaction between acute sleep loss and social evaluation that predicts emotion-related neural activation and caloric intake in adolescents. This research helps to elucidate the relationship between sleep loss, social stress, and weight status using a novel health neuroscience model. |
doi_str_mv | 10.1093/sleep/zsab263 |
format | Article |
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Study Objectives
Insufficient sleep and social stress are associated with weight gain and obesity development in adolescent girls. Functional magnetic resonance imaging (fMRI) research suggests that altered engagement of emotion-related neural networks may explain overeating when under stress. The purpose of this study is to explore the effects of acute sleep restriction on female adolescents’ neural responding during social evaluative stress and their subsequent eating behavior.
Methods
Forty-two adolescent females (ages 15−18 years) with overweight or obesity completed a social stress induction task in which they were told they would be rated by peers based on their photograph and profile. Participants were randomly assigned to one night of sleep deprivation or 9 h of sleep the night before undergoing fMRI while receiving positive and negative evaluations from their peers. After which, subjects participated in an ad libitum buffet.
Results
Sleep deprived, relative to nondeprived girls had distinct patterns of neural engagement to positive and negative evaluation in anterior, mid, and posterior aspects of midline brain structures. Moreover, a sleep deprivation-by-evaluation valence-by-caloric intake interaction emerged in bilateral dorsal anterior cingulate. Among sleep deprived girls, greater engagement during negative, but not positive, feedback was associated with lower caloric intake. This was not observed for nonsleep deprived girls.
Conclusions
Results suggest an interaction between acute sleep loss and social evaluation that predicts emotion-related neural activation and caloric intake in adolescents. This research helps to elucidate the relationship between sleep loss, social stress, and weight status using a novel health neuroscience model.</description><identifier>ISSN: 0161-8105</identifier><identifier>EISSN: 1550-9109</identifier><identifier>DOI: 10.1093/sleep/zsab263</identifier><identifier>PMID: 34727185</identifier><language>eng</language><publisher>US: Oxford University Press</publisher><subject>Adolescent ; Child development ; Clinical Neurology ; Female ; Food consumption ; Food habits ; Girls ; Humans ; Life Sciences & Biomedicine ; Magnetic Resonance Imaging ; Neural networks ; Neurosciences ; Neurosciences & Neurology ; Obesity ; Obesity - complications ; Obesity - diagnostic imaging ; Obesity in adolescence ; Overweight ; Science & Technology ; Sleep ; Sleep deprivation ; Sleep Deprivation - complications ; Sleep Deprivation - diagnostic imaging ; Stress in children ; Teenage girls ; Teenagers</subject><ispartof>Sleep (New York, N.Y.), 2022-03, Vol.45 (3), p.1</ispartof><rights>The Author(s) 2021. Published by Oxford University Press on behalf of Sleep Research Society. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com 2021</rights><rights>Sleep Research Society 2021. Published by Oxford University Press on behalf of the Sleep Research Society. All rights reserved. For permissions, please email: journals.permissions@oup.com.</rights><rights>COPYRIGHT 2022 Oxford University Press</rights><rights>The Author(s) 2021. Published by Oxford University Press on behalf of Sleep Research Society. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>true</woscitedreferencessubscribed><woscitedreferencescount>4</woscitedreferencescount><woscitedreferencesoriginalsourcerecordid>wos000763951800001</woscitedreferencesoriginalsourcerecordid><citedby>FETCH-LOGICAL-c460t-7d0497b83a98c5aa5eabf5c1d16ef8227686058c302252cac39a9c493c5686bf3</citedby><cites>FETCH-LOGICAL-c460t-7d0497b83a98c5aa5eabf5c1d16ef8227686058c302252cac39a9c493c5686bf3</cites><orcidid>0000-0003-1070-2834 ; 0000-0002-1390-4338 ; 0000-0003-0768-1446 ; 0000-0001-5671-0317 ; 0000-0002-4721-5020</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>315,781,785,1585,27928,27929</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/34727185$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Jensen, Chad D</creatorcontrib><creatorcontrib>Zaugg, Kelsey K</creatorcontrib><creatorcontrib>Muncy, Nathan M</creatorcontrib><creatorcontrib>Allen, Whitney D</creatorcontrib><creatorcontrib>Blackburn, Robyn</creatorcontrib><creatorcontrib>Duraccio, Kara M</creatorcontrib><creatorcontrib>Barnett, Kimberly A</creatorcontrib><creatorcontrib>Brock Kirwan, C</creatorcontrib><creatorcontrib>Jarcho, Johanna M</creatorcontrib><title>Neural mechanisms that promote food consumption following sleep loss and social stress: an fMRI study in adolescent girls with overweight/obesity</title><title>Sleep (New York, N.Y.)</title><addtitle>SLEEP</addtitle><addtitle>Sleep</addtitle><description>Abstract
Study Objectives
Insufficient sleep and social stress are associated with weight gain and obesity development in adolescent girls. Functional magnetic resonance imaging (fMRI) research suggests that altered engagement of emotion-related neural networks may explain overeating when under stress. The purpose of this study is to explore the effects of acute sleep restriction on female adolescents’ neural responding during social evaluative stress and their subsequent eating behavior.
Methods
Forty-two adolescent females (ages 15−18 years) with overweight or obesity completed a social stress induction task in which they were told they would be rated by peers based on their photograph and profile. Participants were randomly assigned to one night of sleep deprivation or 9 h of sleep the night before undergoing fMRI while receiving positive and negative evaluations from their peers. After which, subjects participated in an ad libitum buffet.
Results
Sleep deprived, relative to nondeprived girls had distinct patterns of neural engagement to positive and negative evaluation in anterior, mid, and posterior aspects of midline brain structures. Moreover, a sleep deprivation-by-evaluation valence-by-caloric intake interaction emerged in bilateral dorsal anterior cingulate. Among sleep deprived girls, greater engagement during negative, but not positive, feedback was associated with lower caloric intake. This was not observed for nonsleep deprived girls.
Conclusions
Results suggest an interaction between acute sleep loss and social evaluation that predicts emotion-related neural activation and caloric intake in adolescents. This research helps to elucidate the relationship between sleep loss, social stress, and weight status using a novel health neuroscience model.</description><subject>Adolescent</subject><subject>Child development</subject><subject>Clinical Neurology</subject><subject>Female</subject><subject>Food consumption</subject><subject>Food habits</subject><subject>Girls</subject><subject>Humans</subject><subject>Life Sciences & Biomedicine</subject><subject>Magnetic Resonance Imaging</subject><subject>Neural networks</subject><subject>Neurosciences</subject><subject>Neurosciences & Neurology</subject><subject>Obesity</subject><subject>Obesity - complications</subject><subject>Obesity - diagnostic imaging</subject><subject>Obesity in adolescence</subject><subject>Overweight</subject><subject>Science & Technology</subject><subject>Sleep</subject><subject>Sleep deprivation</subject><subject>Sleep Deprivation - complications</subject><subject>Sleep Deprivation - diagnostic imaging</subject><subject>Stress in children</subject><subject>Teenage girls</subject><subject>Teenagers</subject><issn>0161-8105</issn><issn>1550-9109</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2022</creationdate><recordtype>article</recordtype><sourceid>HGBXW</sourceid><sourceid>EIF</sourceid><sourceid>8G5</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><sourceid>GUQSH</sourceid><sourceid>M2O</sourceid><recordid>eNqNkt2L1DAQwIMo3rr66KsEfBGkt0nTtIlvx-LHwakg-lzSdLqbI01qkrqs_4X_sdnb9Q5FUEJIZvKbyXwh9JSSc0okW0ULMK2-R9WVNbuHFpRzUsj8dB8tCK1pISjhZ-hRjNcky5VkD9EZq5qyoYIv0I8PMAdl8Qh6q5yJY8RpqxKegh99Ajx432PtXZzHKRnvssJavzNug29-xtbHiJXrcfTaZEcxBYjxVVbh4f2nyyzP_R4bh1XvLUQNLuGNCTbinUlb7L9B2IHZbNPKdxBN2j9GDwZlIzw5nUv05c3rz-t3xdXHt5fri6tCVzVJRdOTSjadYEoKzZXioLqBa9rTGgZRlk0tasKFZqQseamVZlJJndPXPL90A1uiF0e_OdWvM8TUjiaHZ61y4OfYllwyUrHDXqLnf6DXfg4uR9fmoktJJS3FHbVRFlrjBp-C0gen7UVDK1ILRkmmzv9C5dXDaHKhYTBZ_5tBcTTQIZc6wNBOwYwq7FtK2sMItDeNaE8jkPlnp2DnboT-lv7V8wyII7CDzg9RG3AabjFCSJNz4lTkG6Frk9Sh72s_u5RNX_6_6V2F_Tz9I-ifWCzeBQ</recordid><startdate>20220301</startdate><enddate>20220301</enddate><creator>Jensen, Chad D</creator><creator>Zaugg, Kelsey K</creator><creator>Muncy, Nathan M</creator><creator>Allen, Whitney D</creator><creator>Blackburn, Robyn</creator><creator>Duraccio, Kara M</creator><creator>Barnett, Kimberly A</creator><creator>Brock Kirwan, C</creator><creator>Jarcho, Johanna M</creator><general>Oxford University Press</general><general>Oxford Univ Press</general><scope>BLEPL</scope><scope>DTL</scope><scope>HGBXW</scope><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>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>88G</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>8G5</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BENPR</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>GUQSH</scope><scope>K9.</scope><scope>M0S</scope><scope>M1P</scope><scope>M2M</scope><scope>M2O</scope><scope>MBDVC</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>PSYQQ</scope><scope>Q9U</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0003-1070-2834</orcidid><orcidid>https://orcid.org/0000-0002-1390-4338</orcidid><orcidid>https://orcid.org/0000-0003-0768-1446</orcidid><orcidid>https://orcid.org/0000-0001-5671-0317</orcidid><orcidid>https://orcid.org/0000-0002-4721-5020</orcidid></search><sort><creationdate>20220301</creationdate><title>Neural mechanisms that promote food consumption following sleep loss and social stress: an fMRI study in adolescent girls with overweight/obesity</title><author>Jensen, Chad D ; Zaugg, Kelsey K ; Muncy, Nathan M ; Allen, Whitney D ; Blackburn, Robyn ; Duraccio, Kara M ; Barnett, Kimberly A ; Brock Kirwan, C ; Jarcho, Johanna M</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c460t-7d0497b83a98c5aa5eabf5c1d16ef8227686058c302252cac39a9c493c5686bf3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2022</creationdate><topic>Adolescent</topic><topic>Child development</topic><topic>Clinical Neurology</topic><topic>Female</topic><topic>Food consumption</topic><topic>Food habits</topic><topic>Girls</topic><topic>Humans</topic><topic>Life Sciences & Biomedicine</topic><topic>Magnetic Resonance Imaging</topic><topic>Neural networks</topic><topic>Neurosciences</topic><topic>Neurosciences & Neurology</topic><topic>Obesity</topic><topic>Obesity - complications</topic><topic>Obesity - diagnostic imaging</topic><topic>Obesity in adolescence</topic><topic>Overweight</topic><topic>Science & Technology</topic><topic>Sleep</topic><topic>Sleep deprivation</topic><topic>Sleep Deprivation - complications</topic><topic>Sleep Deprivation - diagnostic imaging</topic><topic>Stress in children</topic><topic>Teenage girls</topic><topic>Teenagers</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Jensen, Chad D</creatorcontrib><creatorcontrib>Zaugg, Kelsey K</creatorcontrib><creatorcontrib>Muncy, Nathan M</creatorcontrib><creatorcontrib>Allen, Whitney D</creatorcontrib><creatorcontrib>Blackburn, Robyn</creatorcontrib><creatorcontrib>Duraccio, Kara M</creatorcontrib><creatorcontrib>Barnett, Kimberly A</creatorcontrib><creatorcontrib>Brock Kirwan, C</creatorcontrib><creatorcontrib>Jarcho, Johanna M</creatorcontrib><collection>Web of Science Core Collection</collection><collection>Science Citation Index Expanded</collection><collection>Web of Science - Science Citation Index Expanded - 2021</collection><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>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>Psychology Database (Alumni)</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>Research Library (Alumni Edition)</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest Central UK/Ireland</collection><collection>ProQuest Central Essentials</collection><collection>ProQuest Central</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>Research Library Prep</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Psychology Database</collection><collection>Research Library</collection><collection>Research Library (Corporate)</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><jtitle>Sleep (New York, N.Y.)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Jensen, Chad D</au><au>Zaugg, Kelsey K</au><au>Muncy, Nathan M</au><au>Allen, Whitney D</au><au>Blackburn, Robyn</au><au>Duraccio, Kara M</au><au>Barnett, Kimberly A</au><au>Brock Kirwan, C</au><au>Jarcho, Johanna M</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Neural mechanisms that promote food consumption following sleep loss and social stress: an fMRI study in adolescent girls with overweight/obesity</atitle><jtitle>Sleep (New York, N.Y.)</jtitle><stitle>SLEEP</stitle><addtitle>Sleep</addtitle><date>2022-03-01</date><risdate>2022</risdate><volume>45</volume><issue>3</issue><spage>1</spage><pages>1-</pages><issn>0161-8105</issn><eissn>1550-9109</eissn><abstract>Abstract
Study Objectives
Insufficient sleep and social stress are associated with weight gain and obesity development in adolescent girls. Functional magnetic resonance imaging (fMRI) research suggests that altered engagement of emotion-related neural networks may explain overeating when under stress. The purpose of this study is to explore the effects of acute sleep restriction on female adolescents’ neural responding during social evaluative stress and their subsequent eating behavior.
Methods
Forty-two adolescent females (ages 15−18 years) with overweight or obesity completed a social stress induction task in which they were told they would be rated by peers based on their photograph and profile. Participants were randomly assigned to one night of sleep deprivation or 9 h of sleep the night before undergoing fMRI while receiving positive and negative evaluations from their peers. After which, subjects participated in an ad libitum buffet.
Results
Sleep deprived, relative to nondeprived girls had distinct patterns of neural engagement to positive and negative evaluation in anterior, mid, and posterior aspects of midline brain structures. Moreover, a sleep deprivation-by-evaluation valence-by-caloric intake interaction emerged in bilateral dorsal anterior cingulate. Among sleep deprived girls, greater engagement during negative, but not positive, feedback was associated with lower caloric intake. This was not observed for nonsleep deprived girls.
Conclusions
Results suggest an interaction between acute sleep loss and social evaluation that predicts emotion-related neural activation and caloric intake in adolescents. This research helps to elucidate the relationship between sleep loss, social stress, and weight status using a novel health neuroscience model.</abstract><cop>US</cop><pub>Oxford University Press</pub><pmid>34727185</pmid><doi>10.1093/sleep/zsab263</doi><tpages>11</tpages><orcidid>https://orcid.org/0000-0003-1070-2834</orcidid><orcidid>https://orcid.org/0000-0002-1390-4338</orcidid><orcidid>https://orcid.org/0000-0003-0768-1446</orcidid><orcidid>https://orcid.org/0000-0001-5671-0317</orcidid><orcidid>https://orcid.org/0000-0002-4721-5020</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Adolescent Child development Clinical Neurology Female Food consumption Food habits Girls Humans Life Sciences & Biomedicine Magnetic Resonance Imaging Neural networks Neurosciences Neurosciences & Neurology Obesity Obesity - complications Obesity - diagnostic imaging Obesity in adolescence Overweight Science & Technology Sleep Sleep deprivation Sleep Deprivation - complications Sleep Deprivation - diagnostic imaging Stress in children Teenage girls Teenagers |
title | Neural mechanisms that promote food consumption following sleep loss and social stress: an fMRI study in adolescent girls with overweight/obesity |
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