Fish oil supplementation alleviates metabolic and anxiodepressive effects of diet-induced obesity and associated changes in brain lipid composition in mice
Objective Obesity significantly elevates the odds of developing mood disorders. Chronic consumption of a saturated high-fat diet (HFD) elicits anxiodepressive behavior in a manner linked to metabolic dysfunction and neuroinflammation in mice. Dietary omega-3 polyunsaturated fatty acids (n-3 PUFA) ca...
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| Veröffentlicht in: | International Journal of Obesity 2020-09, Vol.44 (9), p.1936-1945 |
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| creator | Demers, Geneviève Roy, Jerome Machuca-Parra, Arturo Israel Dashtehei pour, Zahra Bairamian, Diane Daneault, Caroline Rosiers, Christine Des Ferreira, Guillaume Alquier, Thierry Fulton, Stephanie |
| description | Objective
Obesity significantly elevates the odds of developing mood disorders. Chronic consumption of a saturated high-fat diet (HFD) elicits anxiodepressive behavior in a manner linked to metabolic dysfunction and neuroinflammation in mice. Dietary omega-3 polyunsaturated fatty acids (n-3 PUFA) can improve both metabolic and mood impairments by relieving inflammation. Despite these findings, the effects of n-3 PUFA supplementation on energy homeostasis, anxiodepressive behavior, brain lipid composition, and gliosis in the diet-induced obese state are unclear.
Methods
Male C57Bl/6J mice were fed a saturated high-fat diet (HFD) or chow for 20 weeks. During the last 5 weeks mice received daily gavage (“supplementation”) of fish oil (FO) enriched with equal amounts of docosahexaenoic (DHA) and eicosapentaenoic acid (EPA) or control corn oil. Food intake and body weight were measured throughout while additional metabolic parameters and anxiety- and despair-like behavior (elevated-plus maze, light–dark box, and forced swim tasks) were evaluated during the final week of supplementation. Forebrain lipid composition and markers of microglia activation and astrogliosis were assessed by gas chromatography–mass spectrometry and real-time PCR, respectively.
Results
Five weeks of FO supplementation corrected glucose intolerance and attenuated hyperphagia in HFD-induced obese mice without affecting adipose mass. FO supplementation also defended against the anxiogenic and depressive-like effects of HFD. Brain lipids, particularly anti-inflammatory PUFA, were diminished by HFD, whereas FO restored levels beyond control values. Gene expression markers of brain reactive gliosis were supressed by FO.
Conclusions
Supplementing a saturated HFD with FO rich in EPA and DHA corrects glucose intolerance, inhibits food intake, suppresses anxiodepressive behaviors, enhances anti-inflammatory brain lipids, and dampens indices of brain gliosis in obese mice. Together, these findings support increasing dietary n-3 PUFA for the treatment of metabolic and mood disturbances associated with excess fat intake and obesity. |
| doi_str_mv | 10.1038/s41366-020-0623-6 |
| format | Article |
| fullrecord | <record><control><sourceid>gale_hal_p</sourceid><recordid>TN_cdi_hal_primary_oai_HAL_hal_02902619v1</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><galeid>A633468339</galeid><sourcerecordid>A633468339</sourcerecordid><originalsourceid>FETCH-LOGICAL-c641t-2d6d0091d8b380f6fd0a83954da1daab639cea4dd4c59ddad34758a10390b8033</originalsourceid><addsrcrecordid>eNp9ktGK1TAQhoso7nH1AbyRgiB60XXSpGlzeVhcVzjgjV6HNJlus6RNbdKD-yy-rCldd11RKWlg8v0zzMyfZS8JnBGgzfvACOW8gBIK4CUt-KNsR1jNi4qJ-nG2Awp1ARWvTrJnIVwDQFVB-TQ7oWXFeFNVu-zHhQ197q3LwzJNDgcco4rWj7lyDo9WRQz5gFG13lmdq9Gk8916g9OMIdgj5th1qGPIfZcbi7Gwo1k0mty3GGy82TQheL0mM7nu1XiVktoxb2eV_s5ONoX9MPnEr6VTcLAan2dPOuUCvri9T7OvFx--nF8Wh88fP53vD4XmjMSiNNwACGKaljbQ8c6AaqiomFHEKNVyKjQqZgzTlTBGGcrqqlFpggLaBig9zd5teXvl5DTbQc030isrL_cHucagFFByIo4ksW83dpr9twVDlIMNGp1TI_olyJIRxgghpUjo6z_Qa7_MY-okUTWvqRCs-T-VtiuaGsp76ko5lHbsfJyVXkvLPac0LZPSteLZX6j0GUzz9CN2NsUfCN78JuhRudgH75Z1C-EhSDZQzz6EGbu7ORGQqxfl5sU0KpCrFyVPmle3nS3tgOZO8ct8CSg3IKSn5In5vvV_Z_0Jdp3oTg</addsrcrecordid><sourcetype>Open Access Repository</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>2436698702</pqid></control><display><type>article</type><title>Fish oil supplementation alleviates metabolic and anxiodepressive effects of diet-induced obesity and associated changes in brain lipid composition in mice</title><source>Nature Journals Online</source><source>SpringerLink Journals - AutoHoldings</source><creator>Demers, Geneviève ; Roy, Jerome ; Machuca-Parra, Arturo Israel ; Dashtehei pour, Zahra ; Bairamian, Diane ; Daneault, Caroline ; Rosiers, Christine Des ; Ferreira, Guillaume ; Alquier, Thierry ; Fulton, Stephanie</creator><creatorcontrib>Demers, Geneviève ; Roy, Jerome ; Machuca-Parra, Arturo Israel ; Dashtehei pour, Zahra ; Bairamian, Diane ; Daneault, Caroline ; Rosiers, Christine Des ; Ferreira, Guillaume ; Alquier, Thierry ; Fulton, Stephanie ; Representative of consortium</creatorcontrib><description>Objective
Obesity significantly elevates the odds of developing mood disorders. Chronic consumption of a saturated high-fat diet (HFD) elicits anxiodepressive behavior in a manner linked to metabolic dysfunction and neuroinflammation in mice. Dietary omega-3 polyunsaturated fatty acids (n-3 PUFA) can improve both metabolic and mood impairments by relieving inflammation. Despite these findings, the effects of n-3 PUFA supplementation on energy homeostasis, anxiodepressive behavior, brain lipid composition, and gliosis in the diet-induced obese state are unclear.
Methods
Male C57Bl/6J mice were fed a saturated high-fat diet (HFD) or chow for 20 weeks. During the last 5 weeks mice received daily gavage (“supplementation”) of fish oil (FO) enriched with equal amounts of docosahexaenoic (DHA) and eicosapentaenoic acid (EPA) or control corn oil. Food intake and body weight were measured throughout while additional metabolic parameters and anxiety- and despair-like behavior (elevated-plus maze, light–dark box, and forced swim tasks) were evaluated during the final week of supplementation. Forebrain lipid composition and markers of microglia activation and astrogliosis were assessed by gas chromatography–mass spectrometry and real-time PCR, respectively.
Results
Five weeks of FO supplementation corrected glucose intolerance and attenuated hyperphagia in HFD-induced obese mice without affecting adipose mass. FO supplementation also defended against the anxiogenic and depressive-like effects of HFD. Brain lipids, particularly anti-inflammatory PUFA, were diminished by HFD, whereas FO restored levels beyond control values. Gene expression markers of brain reactive gliosis were supressed by FO.
Conclusions
Supplementing a saturated HFD with FO rich in EPA and DHA corrects glucose intolerance, inhibits food intake, suppresses anxiodepressive behaviors, enhances anti-inflammatory brain lipids, and dampens indices of brain gliosis in obese mice. Together, these findings support increasing dietary n-3 PUFA for the treatment of metabolic and mood disturbances associated with excess fat intake and obesity.</description><identifier>ISSN: 0307-0565</identifier><identifier>EISSN: 1476-5497</identifier><identifier>EISSN: 0307-0565</identifier><identifier>DOI: 10.1038/s41366-020-0623-6</identifier><identifier>PMID: 32546855</identifier><language>eng</language><publisher>London: Nature Publishing Group UK</publisher><subject>38/90 ; 45/77 ; 631/378/1488/393 ; 631/443/319/1488/393 ; 631/443/319/1557 ; 631/443/319/1642/137 ; 631/443/319/1642/393 ; 64 ; 64/60 ; 82 ; 82/58 ; 82/80 ; Analysis ; Body weight ; Brain ; Composition ; Corn oil ; Diet ; Dietary supplements ; Eicosapentaenoic acid ; Energy balance ; Epidemiology ; Fatty acids ; Fish oils ; Food intake ; Food intolerance ; Forebrain ; Gas chromatography ; Gene expression ; Gliosis ; Glucose ; Glucose tolerance ; Health Promotion and Disease Prevention ; High fat diet ; Homeostasis ; Hyperphagia ; Inflammation ; Internal Medicine ; Life Sciences ; Lipid composition ; Lipids ; Markers ; Mass spectrometry ; Mass spectroscopy ; Medicine ; Medicine & Public Health ; Metabolic Diseases ; Metabolism ; Microglia ; Mood ; Obesity ; Omega-3 fatty acids ; Polyunsaturated fatty acids ; Public Health ; Unsaturated fatty acids</subject><ispartof>International Journal of Obesity, 2020-09, Vol.44 (9), p.1936-1945</ispartof><rights>The Author(s), under exclusive licence to Springer Nature Limited 2020</rights><rights>COPYRIGHT 2020 Nature Publishing Group</rights><rights>The Author(s), under exclusive licence to Springer Nature Limited 2020.</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c641t-2d6d0091d8b380f6fd0a83954da1daab639cea4dd4c59ddad34758a10390b8033</citedby><cites>FETCH-LOGICAL-c641t-2d6d0091d8b380f6fd0a83954da1daab639cea4dd4c59ddad34758a10390b8033</cites><orcidid>0000-0002-8673-1052 ; 0000-0001-8171-802X ; 0000-0001-5984-8143 ; 0000-0002-3007-1585</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://link.springer.com/content/pdf/10.1038/s41366-020-0623-6$$EPDF$$P50$$Gspringer$$H</linktopdf><linktohtml>$$Uhttps://link.springer.com/10.1038/s41366-020-0623-6$$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/32546855$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.inrae.fr/hal-02902619$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Demers, Geneviève</creatorcontrib><creatorcontrib>Roy, Jerome</creatorcontrib><creatorcontrib>Machuca-Parra, Arturo Israel</creatorcontrib><creatorcontrib>Dashtehei pour, Zahra</creatorcontrib><creatorcontrib>Bairamian, Diane</creatorcontrib><creatorcontrib>Daneault, Caroline</creatorcontrib><creatorcontrib>Rosiers, Christine Des</creatorcontrib><creatorcontrib>Ferreira, Guillaume</creatorcontrib><creatorcontrib>Alquier, Thierry</creatorcontrib><creatorcontrib>Fulton, Stephanie</creatorcontrib><creatorcontrib>Representative of consortium</creatorcontrib><title>Fish oil supplementation alleviates metabolic and anxiodepressive effects of diet-induced obesity and associated changes in brain lipid composition in mice</title><title>International Journal of Obesity</title><addtitle>Int J Obes</addtitle><addtitle>Int J Obes (Lond)</addtitle><description>Objective
Obesity significantly elevates the odds of developing mood disorders. Chronic consumption of a saturated high-fat diet (HFD) elicits anxiodepressive behavior in a manner linked to metabolic dysfunction and neuroinflammation in mice. Dietary omega-3 polyunsaturated fatty acids (n-3 PUFA) can improve both metabolic and mood impairments by relieving inflammation. Despite these findings, the effects of n-3 PUFA supplementation on energy homeostasis, anxiodepressive behavior, brain lipid composition, and gliosis in the diet-induced obese state are unclear.
Methods
Male C57Bl/6J mice were fed a saturated high-fat diet (HFD) or chow for 20 weeks. During the last 5 weeks mice received daily gavage (“supplementation”) of fish oil (FO) enriched with equal amounts of docosahexaenoic (DHA) and eicosapentaenoic acid (EPA) or control corn oil. Food intake and body weight were measured throughout while additional metabolic parameters and anxiety- and despair-like behavior (elevated-plus maze, light–dark box, and forced swim tasks) were evaluated during the final week of supplementation. Forebrain lipid composition and markers of microglia activation and astrogliosis were assessed by gas chromatography–mass spectrometry and real-time PCR, respectively.
Results
Five weeks of FO supplementation corrected glucose intolerance and attenuated hyperphagia in HFD-induced obese mice without affecting adipose mass. FO supplementation also defended against the anxiogenic and depressive-like effects of HFD. Brain lipids, particularly anti-inflammatory PUFA, were diminished by HFD, whereas FO restored levels beyond control values. Gene expression markers of brain reactive gliosis were supressed by FO.
Conclusions
Supplementing a saturated HFD with FO rich in EPA and DHA corrects glucose intolerance, inhibits food intake, suppresses anxiodepressive behaviors, enhances anti-inflammatory brain lipids, and dampens indices of brain gliosis in obese mice. Together, these findings support increasing dietary n-3 PUFA for the treatment of metabolic and mood disturbances associated with excess fat intake and obesity.</description><subject>38/90</subject><subject>45/77</subject><subject>631/378/1488/393</subject><subject>631/443/319/1488/393</subject><subject>631/443/319/1557</subject><subject>631/443/319/1642/137</subject><subject>631/443/319/1642/393</subject><subject>64</subject><subject>64/60</subject><subject>82</subject><subject>82/58</subject><subject>82/80</subject><subject>Analysis</subject><subject>Body weight</subject><subject>Brain</subject><subject>Composition</subject><subject>Corn oil</subject><subject>Diet</subject><subject>Dietary supplements</subject><subject>Eicosapentaenoic acid</subject><subject>Energy balance</subject><subject>Epidemiology</subject><subject>Fatty acids</subject><subject>Fish oils</subject><subject>Food intake</subject><subject>Food intolerance</subject><subject>Forebrain</subject><subject>Gas chromatography</subject><subject>Gene expression</subject><subject>Gliosis</subject><subject>Glucose</subject><subject>Glucose tolerance</subject><subject>Health Promotion and Disease Prevention</subject><subject>High fat diet</subject><subject>Homeostasis</subject><subject>Hyperphagia</subject><subject>Inflammation</subject><subject>Internal Medicine</subject><subject>Life Sciences</subject><subject>Lipid composition</subject><subject>Lipids</subject><subject>Markers</subject><subject>Mass spectrometry</subject><subject>Mass spectroscopy</subject><subject>Medicine</subject><subject>Medicine & Public Health</subject><subject>Metabolic Diseases</subject><subject>Metabolism</subject><subject>Microglia</subject><subject>Mood</subject><subject>Obesity</subject><subject>Omega-3 fatty acids</subject><subject>Polyunsaturated fatty acids</subject><subject>Public Health</subject><subject>Unsaturated fatty 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oil supplementation alleviates metabolic and anxiodepressive effects of diet-induced obesity and associated changes in brain lipid composition in mice</title><author>Demers, Geneviève ; Roy, Jerome ; Machuca-Parra, Arturo Israel ; Dashtehei pour, Zahra ; Bairamian, Diane ; Daneault, Caroline ; Rosiers, Christine Des ; Ferreira, Guillaume ; Alquier, Thierry ; Fulton, Stephanie</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c641t-2d6d0091d8b380f6fd0a83954da1daab639cea4dd4c59ddad34758a10390b8033</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>38/90</topic><topic>45/77</topic><topic>631/378/1488/393</topic><topic>631/443/319/1488/393</topic><topic>631/443/319/1557</topic><topic>631/443/319/1642/137</topic><topic>631/443/319/1642/393</topic><topic>64</topic><topic>64/60</topic><topic>82</topic><topic>82/58</topic><topic>82/80</topic><topic>Analysis</topic><topic>Body weight</topic><topic>Brain</topic><topic>Composition</topic><topic>Corn oil</topic><topic>Diet</topic><topic>Dietary supplements</topic><topic>Eicosapentaenoic acid</topic><topic>Energy balance</topic><topic>Epidemiology</topic><topic>Fatty acids</topic><topic>Fish oils</topic><topic>Food intake</topic><topic>Food intolerance</topic><topic>Forebrain</topic><topic>Gas chromatography</topic><topic>Gene expression</topic><topic>Gliosis</topic><topic>Glucose</topic><topic>Glucose tolerance</topic><topic>Health Promotion and Disease Prevention</topic><topic>High fat diet</topic><topic>Homeostasis</topic><topic>Hyperphagia</topic><topic>Inflammation</topic><topic>Internal Medicine</topic><topic>Life Sciences</topic><topic>Lipid composition</topic><topic>Lipids</topic><topic>Markers</topic><topic>Mass spectrometry</topic><topic>Mass spectroscopy</topic><topic>Medicine</topic><topic>Medicine & Public Health</topic><topic>Metabolic Diseases</topic><topic>Metabolism</topic><topic>Microglia</topic><topic>Mood</topic><topic>Obesity</topic><topic>Omega-3 fatty acids</topic><topic>Polyunsaturated fatty acids</topic><topic>Public Health</topic><topic>Unsaturated fatty acids</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Demers, Geneviève</creatorcontrib><creatorcontrib>Roy, Jerome</creatorcontrib><creatorcontrib>Machuca-Parra, Arturo Israel</creatorcontrib><creatorcontrib>Dashtehei pour, Zahra</creatorcontrib><creatorcontrib>Bairamian, Diane</creatorcontrib><creatorcontrib>Daneault, Caroline</creatorcontrib><creatorcontrib>Rosiers, Christine Des</creatorcontrib><creatorcontrib>Ferreira, Guillaume</creatorcontrib><creatorcontrib>Alquier, Thierry</creatorcontrib><creatorcontrib>Fulton, Stephanie</creatorcontrib><creatorcontrib>Representative of consortium</creatorcontrib><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central 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Des</au><au>Ferreira, Guillaume</au><au>Alquier, Thierry</au><au>Fulton, Stephanie</au><aucorp>Representative of consortium</aucorp><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Fish oil supplementation alleviates metabolic and anxiodepressive effects of diet-induced obesity and associated changes in brain lipid composition in mice</atitle><jtitle>International Journal of Obesity</jtitle><stitle>Int J Obes</stitle><addtitle>Int J Obes (Lond)</addtitle><date>2020-09-01</date><risdate>2020</risdate><volume>44</volume><issue>9</issue><spage>1936</spage><epage>1945</epage><pages>1936-1945</pages><issn>0307-0565</issn><eissn>1476-5497</eissn><eissn>0307-0565</eissn><abstract>Objective
Obesity significantly elevates the odds of developing mood disorders. Chronic consumption of a saturated high-fat diet (HFD) elicits anxiodepressive behavior in a manner linked to metabolic dysfunction and neuroinflammation in mice. Dietary omega-3 polyunsaturated fatty acids (n-3 PUFA) can improve both metabolic and mood impairments by relieving inflammation. Despite these findings, the effects of n-3 PUFA supplementation on energy homeostasis, anxiodepressive behavior, brain lipid composition, and gliosis in the diet-induced obese state are unclear.
Methods
Male C57Bl/6J mice were fed a saturated high-fat diet (HFD) or chow for 20 weeks. During the last 5 weeks mice received daily gavage (“supplementation”) of fish oil (FO) enriched with equal amounts of docosahexaenoic (DHA) and eicosapentaenoic acid (EPA) or control corn oil. Food intake and body weight were measured throughout while additional metabolic parameters and anxiety- and despair-like behavior (elevated-plus maze, light–dark box, and forced swim tasks) were evaluated during the final week of supplementation. Forebrain lipid composition and markers of microglia activation and astrogliosis were assessed by gas chromatography–mass spectrometry and real-time PCR, respectively.
Results
Five weeks of FO supplementation corrected glucose intolerance and attenuated hyperphagia in HFD-induced obese mice without affecting adipose mass. FO supplementation also defended against the anxiogenic and depressive-like effects of HFD. Brain lipids, particularly anti-inflammatory PUFA, were diminished by HFD, whereas FO restored levels beyond control values. Gene expression markers of brain reactive gliosis were supressed by FO.
Conclusions
Supplementing a saturated HFD with FO rich in EPA and DHA corrects glucose intolerance, inhibits food intake, suppresses anxiodepressive behaviors, enhances anti-inflammatory brain lipids, and dampens indices of brain gliosis in obese mice. Together, these findings support increasing dietary n-3 PUFA for the treatment of metabolic and mood disturbances associated with excess fat intake and obesity.</abstract><cop>London</cop><pub>Nature Publishing Group UK</pub><pmid>32546855</pmid><doi>10.1038/s41366-020-0623-6</doi><tpages>10</tpages><orcidid>https://orcid.org/0000-0002-8673-1052</orcidid><orcidid>https://orcid.org/0000-0001-8171-802X</orcidid><orcidid>https://orcid.org/0000-0001-5984-8143</orcidid><orcidid>https://orcid.org/0000-0002-3007-1585</orcidid><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 0307-0565 |
| ispartof | International Journal of Obesity, 2020-09, Vol.44 (9), p.1936-1945 |
| issn | 0307-0565 1476-5497 0307-0565 |
| language | eng |
| recordid | cdi_hal_primary_oai_HAL_hal_02902619v1 |
| source | Nature Journals Online; SpringerLink Journals - AutoHoldings |
| subjects | 38/90 45/77 631/378/1488/393 631/443/319/1488/393 631/443/319/1557 631/443/319/1642/137 631/443/319/1642/393 64 64/60 82 82/58 82/80 Analysis Body weight Brain Composition Corn oil Diet Dietary supplements Eicosapentaenoic acid Energy balance Epidemiology Fatty acids Fish oils Food intake Food intolerance Forebrain Gas chromatography Gene expression Gliosis Glucose Glucose tolerance Health Promotion and Disease Prevention High fat diet Homeostasis Hyperphagia Inflammation Internal Medicine Life Sciences Lipid composition Lipids Markers Mass spectrometry Mass spectroscopy Medicine Medicine & Public Health Metabolic Diseases Metabolism Microglia Mood Obesity Omega-3 fatty acids Polyunsaturated fatty acids Public Health Unsaturated fatty acids |
| title | Fish oil supplementation alleviates metabolic and anxiodepressive effects of diet-induced obesity and associated changes in brain lipid composition in mice |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-02-09T07%3A44%3A27IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_hal_p&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Fish%20oil%20supplementation%20alleviates%20metabolic%20and%20anxiodepressive%20effects%20of%20diet-induced%20obesity%20and%20associated%20changes%20in%20brain%20lipid%20composition%20in%20mice&rft.jtitle=International%20Journal%20of%20Obesity&rft.au=Demers,%20Genevi%C3%A8ve&rft.aucorp=Representative%20of%20consortium&rft.date=2020-09-01&rft.volume=44&rft.issue=9&rft.spage=1936&rft.epage=1945&rft.pages=1936-1945&rft.issn=0307-0565&rft.eissn=1476-5497&rft_id=info:doi/10.1038/s41366-020-0623-6&rft_dat=%3Cgale_hal_p%3EA633468339%3C/gale_hal_p%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=2436698702&rft_id=info:pmid/32546855&rft_galeid=A633468339&rfr_iscdi=true |