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NREM sleep as a novel protective cognitive reserve factor in the face of Alzheimer's disease pathology

BACKGROUND: Alzheimer’s disease (AD) pathology impairs cognitive function. Yet some individuals with high amounts of AD pathology suffer marked memory impairment, while others with the same degree of pathology burden show little impairment. Why is this? One proposed explanation is cognitive reserve...

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Autores principales: Zavecz, Zsófia, Shah, Vyoma D., Murillo, Olivia G., Vallat, Raphael, Mander, Bryce A., Winer, Joseph R., Jagust, William J., Walker, Matthew P.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10155344/
https://www.ncbi.nlm.nih.gov/pubmed/37138290
http://dx.doi.org/10.1186/s12916-023-02811-z
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author Zavecz, Zsófia
Shah, Vyoma D.
Murillo, Olivia G.
Vallat, Raphael
Mander, Bryce A.
Winer, Joseph R.
Jagust, William J.
Walker, Matthew P.
author_facet Zavecz, Zsófia
Shah, Vyoma D.
Murillo, Olivia G.
Vallat, Raphael
Mander, Bryce A.
Winer, Joseph R.
Jagust, William J.
Walker, Matthew P.
author_sort Zavecz, Zsófia
collection PubMed
description BACKGROUND: Alzheimer’s disease (AD) pathology impairs cognitive function. Yet some individuals with high amounts of AD pathology suffer marked memory impairment, while others with the same degree of pathology burden show little impairment. Why is this? One proposed explanation is cognitive reserve i.e., factors that confer resilience against, or compensation for the effects of AD pathology. Deep NREM slow wave sleep (SWS) is recognized to enhance functions of learning and memory in healthy older adults. However, that the quality of NREM SWS (NREM slow wave activity, SWA) represents a novel cognitive reserve factor in older adults with AD pathology, thereby providing compensation against memory dysfunction otherwise caused by high AD pathology burden, remains unknown. METHODS: Here, we tested this hypothesis in cognitively normal older adults (N = 62) by combining (11)C-PiB (Pittsburgh compound B) positron emission tomography (PET) scanning for the quantification of β-amyloid (Aβ) with sleep electroencephalography (EEG) recordings to quantify NREM SWA and a hippocampal-dependent face-name learning task. RESULTS: We demonstrated that NREM SWA significantly moderates the effect of Aβ status on memory function. Specifically, NREM SWA selectively supported superior memory function in individuals suffering high Aβ burden, i.e., those most in need of cognitive reserve (B = 2.694, p = 0.019). In contrast, those without significant Aβ pathological burden, and thus without the same  need for cognitive reserve, did not similarly benefit from the presence of NREM SWA (B = -0.115, p = 0.876). This interaction between NREM SWA and Aβ status predicting memory function was significant after correcting for age, sex, Body Mass Index, gray matter atrophy, and previously identified cognitive reserve factors, such as education and physical activity (p = 0.042). CONCLUSIONS: These findings indicate that NREM SWA is a novel cognitive reserve factor providing resilience against the memory impairment otherwise caused by high AD pathology burden. Furthermore, this cognitive reserve function of NREM SWA remained significant when accounting both for covariates, and factors previously linked to resilience, suggesting that sleep might be an independent cognitive reserve resource. Beyond such mechanistic insights are potential therapeutic implications. Unlike many other cognitive reserve factors (e.g., years of education, prior job complexity), sleep is a modifiable factor. As such, it represents an intervention possibility that may aid the preservation of cognitive function in the face of AD pathology, both present moment and longitudinally. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12916-023-02811-z.
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spelling pubmed-101553442023-05-04 NREM sleep as a novel protective cognitive reserve factor in the face of Alzheimer's disease pathology Zavecz, Zsófia Shah, Vyoma D. Murillo, Olivia G. Vallat, Raphael Mander, Bryce A. Winer, Joseph R. Jagust, William J. Walker, Matthew P. BMC Med Research Article BACKGROUND: Alzheimer’s disease (AD) pathology impairs cognitive function. Yet some individuals with high amounts of AD pathology suffer marked memory impairment, while others with the same degree of pathology burden show little impairment. Why is this? One proposed explanation is cognitive reserve i.e., factors that confer resilience against, or compensation for the effects of AD pathology. Deep NREM slow wave sleep (SWS) is recognized to enhance functions of learning and memory in healthy older adults. However, that the quality of NREM SWS (NREM slow wave activity, SWA) represents a novel cognitive reserve factor in older adults with AD pathology, thereby providing compensation against memory dysfunction otherwise caused by high AD pathology burden, remains unknown. METHODS: Here, we tested this hypothesis in cognitively normal older adults (N = 62) by combining (11)C-PiB (Pittsburgh compound B) positron emission tomography (PET) scanning for the quantification of β-amyloid (Aβ) with sleep electroencephalography (EEG) recordings to quantify NREM SWA and a hippocampal-dependent face-name learning task. RESULTS: We demonstrated that NREM SWA significantly moderates the effect of Aβ status on memory function. Specifically, NREM SWA selectively supported superior memory function in individuals suffering high Aβ burden, i.e., those most in need of cognitive reserve (B = 2.694, p = 0.019). In contrast, those without significant Aβ pathological burden, and thus without the same  need for cognitive reserve, did not similarly benefit from the presence of NREM SWA (B = -0.115, p = 0.876). This interaction between NREM SWA and Aβ status predicting memory function was significant after correcting for age, sex, Body Mass Index, gray matter atrophy, and previously identified cognitive reserve factors, such as education and physical activity (p = 0.042). CONCLUSIONS: These findings indicate that NREM SWA is a novel cognitive reserve factor providing resilience against the memory impairment otherwise caused by high AD pathology burden. Furthermore, this cognitive reserve function of NREM SWA remained significant when accounting both for covariates, and factors previously linked to resilience, suggesting that sleep might be an independent cognitive reserve resource. Beyond such mechanistic insights are potential therapeutic implications. Unlike many other cognitive reserve factors (e.g., years of education, prior job complexity), sleep is a modifiable factor. As such, it represents an intervention possibility that may aid the preservation of cognitive function in the face of AD pathology, both present moment and longitudinally. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12916-023-02811-z. BioMed Central 2023-05-03 /pmc/articles/PMC10155344/ /pubmed/37138290 http://dx.doi.org/10.1186/s12916-023-02811-z Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research Article
Zavecz, Zsófia
Shah, Vyoma D.
Murillo, Olivia G.
Vallat, Raphael
Mander, Bryce A.
Winer, Joseph R.
Jagust, William J.
Walker, Matthew P.
NREM sleep as a novel protective cognitive reserve factor in the face of Alzheimer's disease pathology
title NREM sleep as a novel protective cognitive reserve factor in the face of Alzheimer's disease pathology
title_full NREM sleep as a novel protective cognitive reserve factor in the face of Alzheimer's disease pathology
title_fullStr NREM sleep as a novel protective cognitive reserve factor in the face of Alzheimer's disease pathology
title_full_unstemmed NREM sleep as a novel protective cognitive reserve factor in the face of Alzheimer's disease pathology
title_short NREM sleep as a novel protective cognitive reserve factor in the face of Alzheimer's disease pathology
title_sort nrem sleep as a novel protective cognitive reserve factor in the face of alzheimer's disease pathology
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10155344/
https://www.ncbi.nlm.nih.gov/pubmed/37138290
http://dx.doi.org/10.1186/s12916-023-02811-z
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