The impacts of sex and the 5xFAD model of Alzheimer’s disease on the sleep and spatial learning responses to feeding time
IntroductionThe relationships between the feeding rhythm, sleep and cognition in Alzheimer’s disease (AD) are incompletely understood, but meal time could provide an easy-to-implement method of curtailing disease-associated disruptions in sleep and cognition. Furthermore, known sex differences in AD...
| المؤلفون الرئيسيون: | , , , , , , , , |
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| التنسيق: | مقال |
| اللغة: | English |
| منشور في: |
Frontiers Media S.A.
2024-07-01
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| سلاسل: | Frontiers in Neurology |
| الموضوعات: | |
| الوصول للمادة أونلاين: | https://www.frontiersin.org/articles/10.3389/fneur.2024.1430989/full |
| _version_ | 1827173667781476352 |
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| author | Katrina J. Campbell Katrina J. Campbell Peng Jiang Peng Jiang Christopher Olker Christopher Olker Xuanyi Lin Xuanyi Lin Sarah Y. Kim Sarah Y. Kim Christopher J. Lee Christopher J. Lee Eun Joo Song Eun Joo Song Fred W. Turek Fred W. Turek Martha Hotz Vitaterna Martha Hotz Vitaterna |
| author_facet | Katrina J. Campbell Katrina J. Campbell Peng Jiang Peng Jiang Christopher Olker Christopher Olker Xuanyi Lin Xuanyi Lin Sarah Y. Kim Sarah Y. Kim Christopher J. Lee Christopher J. Lee Eun Joo Song Eun Joo Song Fred W. Turek Fred W. Turek Martha Hotz Vitaterna Martha Hotz Vitaterna |
| author_sort | Katrina J. Campbell |
| collection | DOAJ |
| description | IntroductionThe relationships between the feeding rhythm, sleep and cognition in Alzheimer’s disease (AD) are incompletely understood, but meal time could provide an easy-to-implement method of curtailing disease-associated disruptions in sleep and cognition. Furthermore, known sex differences in AD incidence could relate to sex differences in circadian rhythm/sleep/cognition interactions.MethodsThe 5xFAD transgenic mouse model of AD and non-transgenic wild-type controls were studied. Both female and male mice were used. Food access was restricted each day to either the 12-h light phase (light-fed groups) or the 12-h dark phase (dark-fed groups). Sleep (electroencephalographic/electromyographic) recording and cognitive behavior measures were collected.ResultsThe 5xFAD genotype reduces NREM and REM as well as the number of sleep spindles. In wild-type mice, light-fed groups had disrupted vigilance state amounts, characteristics, and rhythms relative to dark-fed groups. These feeding time differences were reduced in 5xFAD mice. Sex modulates these effects. 5xFAD mice display poorer spatial memory that, in female mice, is curtailed by dark phase feeding. Similarly, female 5xFAD mice have decreased anxiety-associated behavior. These emotional and cognitive measures are correlated with REM amount.DiscussionOur study demonstrates that the timing of feeding can alter many aspects of wake, NREM and REM. Unexpectedly, 5xFAD mice are less sensitive to these feeding time effects. 5xFAD mice demonstrate deficits in cognition which are correlated with REM, suggesting that this circadian-timed aspect of sleep may link feeding time and cognition. Sex plays an important role in regulating the impact of feeding time on sleep and cognition in both wild-type and 5xFAD mice, with females showing a greater cognitive response to feeding time than males. |
| first_indexed | 2025-03-21T03:43:18Z |
| format | Article |
| id | doaj.art-e5cb1546c84d4a3ba7605a01468e254d |
| institution | Directory Open Access Journal |
| issn | 1664-2295 |
| language | English |
| last_indexed | 2025-03-21T03:43:18Z |
| publishDate | 2024-07-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Neurology |
| spelling | doaj.art-e5cb1546c84d4a3ba7605a01468e254d2024-07-31T05:02:43ZengFrontiers Media S.A.Frontiers in Neurology1664-22952024-07-011510.3389/fneur.2024.14309891430989The impacts of sex and the 5xFAD model of Alzheimer’s disease on the sleep and spatial learning responses to feeding timeKatrina J. Campbell0Katrina J. Campbell1Peng Jiang2Peng Jiang3Christopher Olker4Christopher Olker5Xuanyi Lin6Xuanyi Lin7Sarah Y. Kim8Sarah Y. Kim9Christopher J. Lee10Christopher J. Lee11Eun Joo Song12Eun Joo Song13Fred W. Turek14Fred W. Turek15Martha Hotz Vitaterna16Martha Hotz Vitaterna17Center for Sleep and Circadian Biology, Northwestern University, Evanston, IL, United StatesDepartment of Neurobiology, Weinberg College of Arts and Sciences, Northwestern University, Evanston, IL, United StatesCenter for Sleep and Circadian Biology, Northwestern University, Evanston, IL, United StatesDepartment of Neurobiology, Weinberg College of Arts and Sciences, Northwestern University, Evanston, IL, United StatesCenter for Sleep and Circadian Biology, Northwestern University, Evanston, IL, United StatesDepartment of Neurobiology, Weinberg College of Arts and Sciences, Northwestern University, Evanston, IL, United StatesCenter for Sleep and Circadian Biology, Northwestern University, Evanston, IL, United StatesDepartment of Neurobiology, Weinberg College of Arts and Sciences, Northwestern University, Evanston, IL, United StatesCenter for Sleep and Circadian Biology, Northwestern University, Evanston, IL, United StatesDepartment of Neurobiology, Weinberg College of Arts and Sciences, Northwestern University, Evanston, IL, United StatesCenter for Sleep and Circadian Biology, Northwestern University, Evanston, IL, United StatesDepartment of Neurobiology, Weinberg College of Arts and Sciences, Northwestern University, Evanston, IL, United StatesCenter for Sleep and Circadian Biology, Northwestern University, Evanston, IL, United StatesDepartment of Neurobiology, Weinberg College of Arts and Sciences, Northwestern University, Evanston, IL, United StatesCenter for Sleep and Circadian Biology, Northwestern University, Evanston, IL, United StatesDepartment of Neurobiology, Weinberg College of Arts and Sciences, Northwestern University, Evanston, IL, United StatesCenter for Sleep and Circadian Biology, Northwestern University, Evanston, IL, United StatesDepartment of Neurobiology, Weinberg College of Arts and Sciences, Northwestern University, Evanston, IL, United StatesIntroductionThe relationships between the feeding rhythm, sleep and cognition in Alzheimer’s disease (AD) are incompletely understood, but meal time could provide an easy-to-implement method of curtailing disease-associated disruptions in sleep and cognition. Furthermore, known sex differences in AD incidence could relate to sex differences in circadian rhythm/sleep/cognition interactions.MethodsThe 5xFAD transgenic mouse model of AD and non-transgenic wild-type controls were studied. Both female and male mice were used. Food access was restricted each day to either the 12-h light phase (light-fed groups) or the 12-h dark phase (dark-fed groups). Sleep (electroencephalographic/electromyographic) recording and cognitive behavior measures were collected.ResultsThe 5xFAD genotype reduces NREM and REM as well as the number of sleep spindles. In wild-type mice, light-fed groups had disrupted vigilance state amounts, characteristics, and rhythms relative to dark-fed groups. These feeding time differences were reduced in 5xFAD mice. Sex modulates these effects. 5xFAD mice display poorer spatial memory that, in female mice, is curtailed by dark phase feeding. Similarly, female 5xFAD mice have decreased anxiety-associated behavior. These emotional and cognitive measures are correlated with REM amount.DiscussionOur study demonstrates that the timing of feeding can alter many aspects of wake, NREM and REM. Unexpectedly, 5xFAD mice are less sensitive to these feeding time effects. 5xFAD mice demonstrate deficits in cognition which are correlated with REM, suggesting that this circadian-timed aspect of sleep may link feeding time and cognition. Sex plays an important role in regulating the impact of feeding time on sleep and cognition in both wild-type and 5xFAD mice, with females showing a greater cognitive response to feeding time than males.https://www.frontiersin.org/articles/10.3389/fneur.2024.1430989/fullAlzheimer’s diseasetime-restricted feedingphase-restricted feedingsleepcognition5xFAD |
| spellingShingle | Katrina J. Campbell Katrina J. Campbell Peng Jiang Peng Jiang Christopher Olker Christopher Olker Xuanyi Lin Xuanyi Lin Sarah Y. Kim Sarah Y. Kim Christopher J. Lee Christopher J. Lee Eun Joo Song Eun Joo Song Fred W. Turek Fred W. Turek Martha Hotz Vitaterna Martha Hotz Vitaterna The impacts of sex and the 5xFAD model of Alzheimer’s disease on the sleep and spatial learning responses to feeding time Frontiers in Neurology Alzheimer’s disease time-restricted feeding phase-restricted feeding sleep cognition 5xFAD |
| title | The impacts of sex and the 5xFAD model of Alzheimer’s disease on the sleep and spatial learning responses to feeding time |
| title_full | The impacts of sex and the 5xFAD model of Alzheimer’s disease on the sleep and spatial learning responses to feeding time |
| title_fullStr | The impacts of sex and the 5xFAD model of Alzheimer’s disease on the sleep and spatial learning responses to feeding time |
| title_full_unstemmed | The impacts of sex and the 5xFAD model of Alzheimer’s disease on the sleep and spatial learning responses to feeding time |
| title_short | The impacts of sex and the 5xFAD model of Alzheimer’s disease on the sleep and spatial learning responses to feeding time |
| title_sort | impacts of sex and the 5xfad model of alzheimer s disease on the sleep and spatial learning responses to feeding time |
| topic | Alzheimer’s disease time-restricted feeding phase-restricted feeding sleep cognition 5xFAD |
| url | https://www.frontiersin.org/articles/10.3389/fneur.2024.1430989/full |
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