Cargando…

Protective effects of sleep duration and physical activity on cognitive performance are influenced by β-amyloid and brain volume but not tau burden among cognitively unimpaired older adults

BACKGROUND AND OBJECTIVES: Sleep and physical activity have gained traction as modifiable risk factors for Alzheimer’s disease. Sleep duration is linked to amyloid-β clearance while physical activity is associated with brain volume maintenance. We investigate how sleep duration and physical activity...

Descripción completa

Detalles Bibliográficos
Autores principales: Aslanyan, Vahan, Ortega, Nancy, Fenton, Laura, Harrison, Theresa M., Raman, Rema, Mack, Wendy J., Pa, Judy
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Elsevier 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10316126/
https://www.ncbi.nlm.nih.gov/pubmed/37379733
http://dx.doi.org/10.1016/j.nicl.2023.103460
_version_ 1785067648272302080
author Aslanyan, Vahan
Ortega, Nancy
Fenton, Laura
Harrison, Theresa M.
Raman, Rema
Mack, Wendy J.
Pa, Judy
author_facet Aslanyan, Vahan
Ortega, Nancy
Fenton, Laura
Harrison, Theresa M.
Raman, Rema
Mack, Wendy J.
Pa, Judy
author_sort Aslanyan, Vahan
collection PubMed
description BACKGROUND AND OBJECTIVES: Sleep and physical activity have gained traction as modifiable risk factors for Alzheimer’s disease. Sleep duration is linked to amyloid-β clearance while physical activity is associated with brain volume maintenance. We investigate how sleep duration and physical activity are associated with cognition by testing if the associations between sleep duration or physical activity to cognition are explained by amyloid-β burden and brain volume, respectively. Additionally, we explore the mediating role of tau deposition in sleep duration—cognition and physical activity—cognition relationships. METHODS: This cross-sectional study obtained data from participants in the Anti-Amyloid Treatment in Asymptomatic Alzheimer’s Disease (A4) study, a randomized clinical trial. In trial screening, cognitively unimpaired participants (age 65–85 years) underwent amyloid PET and brain MRI; APOE genotype and lifestyle questionnaire data were obtained. Cognitive performance was assessed using the Preclinical Alzheimer Cognitive Composite (PACC). Self-reported nightly sleep duration and weekly physical activity were the primary predictors. Regional Aβ and tau pathologies and volumes were the proposed variables influencing relationships between sleep duration or physical activity and cognition. RESULTS: Aβ data were obtained from 4322 participants (1208 with MRI, 59% female, 29% amyloid positive). Sleep duration was associated with a Aβ composite score (β = −0.005, CI: (−0.01, −0.001)) and Aβ burden in the anterior cingulate (ACC) (β = −0.012, CI: (−0.017, −0.006)) and medial orbitofrontal cortices (MOC) (β = −0.009, CI: (−0.014, −0.005)). Composite (β = −1.54, 95% CI:(−1.93, −1.15)), ACC (β = −1.22, CI:(−1.54, −0.90)) and MOC (β = −1.44, CI:(−1.86, −1.02)) Aβ deposition was associated with PACC. Sleep duration—PACC association was explained by Aβ burden in path analyses. Physical activity was associated with hippocampal (β = 10.57, CI: (1.06, 20.08)), parahippocampal (β = 9.3, CI: (1.69, 16.91)), entorhinal (β = 14.68, CI: (1.75, 27.61), and fusiform gyral (β = 38.38, CI: (5.57, 71.18)) volumes, which were positively associated with PACC (p < 0.02 for hippocampus, entorhinal cortex and fusiform gyrus). Physical activity—cognition relationship was explained by regional volumes. PET tau imaging was available for 443 participants. No direct sleep duration—tau burden, physical activity by tau burden, or mediation by regional tau was observed in sleep duration—cognition or physical activity—cognition relationships. DISCUSSION: Sleep duration and physical activity are associated with cognition through independent paths of brain Aβ and brain volume, respectively. These findings implicate neural and pathological mechanisms for the relationships between sleep duration and physical activity on cognition. Dementia risk reduction approaches that emphasize the adequate sleep duration and a physically active lifestyle may benefit those with risk for Alzheimer’s disease.
format Online
Article
Text
id pubmed-10316126
institution National Center for Biotechnology Information
language English
publishDate 2023
publisher Elsevier
record_format MEDLINE/PubMed
spelling pubmed-103161262023-07-04 Protective effects of sleep duration and physical activity on cognitive performance are influenced by β-amyloid and brain volume but not tau burden among cognitively unimpaired older adults Aslanyan, Vahan Ortega, Nancy Fenton, Laura Harrison, Theresa M. Raman, Rema Mack, Wendy J. Pa, Judy Neuroimage Clin Regular Article BACKGROUND AND OBJECTIVES: Sleep and physical activity have gained traction as modifiable risk factors for Alzheimer’s disease. Sleep duration is linked to amyloid-β clearance while physical activity is associated with brain volume maintenance. We investigate how sleep duration and physical activity are associated with cognition by testing if the associations between sleep duration or physical activity to cognition are explained by amyloid-β burden and brain volume, respectively. Additionally, we explore the mediating role of tau deposition in sleep duration—cognition and physical activity—cognition relationships. METHODS: This cross-sectional study obtained data from participants in the Anti-Amyloid Treatment in Asymptomatic Alzheimer’s Disease (A4) study, a randomized clinical trial. In trial screening, cognitively unimpaired participants (age 65–85 years) underwent amyloid PET and brain MRI; APOE genotype and lifestyle questionnaire data were obtained. Cognitive performance was assessed using the Preclinical Alzheimer Cognitive Composite (PACC). Self-reported nightly sleep duration and weekly physical activity were the primary predictors. Regional Aβ and tau pathologies and volumes were the proposed variables influencing relationships between sleep duration or physical activity and cognition. RESULTS: Aβ data were obtained from 4322 participants (1208 with MRI, 59% female, 29% amyloid positive). Sleep duration was associated with a Aβ composite score (β = −0.005, CI: (−0.01, −0.001)) and Aβ burden in the anterior cingulate (ACC) (β = −0.012, CI: (−0.017, −0.006)) and medial orbitofrontal cortices (MOC) (β = −0.009, CI: (−0.014, −0.005)). Composite (β = −1.54, 95% CI:(−1.93, −1.15)), ACC (β = −1.22, CI:(−1.54, −0.90)) and MOC (β = −1.44, CI:(−1.86, −1.02)) Aβ deposition was associated with PACC. Sleep duration—PACC association was explained by Aβ burden in path analyses. Physical activity was associated with hippocampal (β = 10.57, CI: (1.06, 20.08)), parahippocampal (β = 9.3, CI: (1.69, 16.91)), entorhinal (β = 14.68, CI: (1.75, 27.61), and fusiform gyral (β = 38.38, CI: (5.57, 71.18)) volumes, which were positively associated with PACC (p < 0.02 for hippocampus, entorhinal cortex and fusiform gyrus). Physical activity—cognition relationship was explained by regional volumes. PET tau imaging was available for 443 participants. No direct sleep duration—tau burden, physical activity by tau burden, or mediation by regional tau was observed in sleep duration—cognition or physical activity—cognition relationships. DISCUSSION: Sleep duration and physical activity are associated with cognition through independent paths of brain Aβ and brain volume, respectively. These findings implicate neural and pathological mechanisms for the relationships between sleep duration and physical activity on cognition. Dementia risk reduction approaches that emphasize the adequate sleep duration and a physically active lifestyle may benefit those with risk for Alzheimer’s disease. Elsevier 2023-06-24 /pmc/articles/PMC10316126/ /pubmed/37379733 http://dx.doi.org/10.1016/j.nicl.2023.103460 Text en © 2023 Published by Elsevier Inc. https://creativecommons.org/licenses/by-nc-nd/4.0/This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
spellingShingle Regular Article
Aslanyan, Vahan
Ortega, Nancy
Fenton, Laura
Harrison, Theresa M.
Raman, Rema
Mack, Wendy J.
Pa, Judy
Protective effects of sleep duration and physical activity on cognitive performance are influenced by β-amyloid and brain volume but not tau burden among cognitively unimpaired older adults
title Protective effects of sleep duration and physical activity on cognitive performance are influenced by β-amyloid and brain volume but not tau burden among cognitively unimpaired older adults
title_full Protective effects of sleep duration and physical activity on cognitive performance are influenced by β-amyloid and brain volume but not tau burden among cognitively unimpaired older adults
title_fullStr Protective effects of sleep duration and physical activity on cognitive performance are influenced by β-amyloid and brain volume but not tau burden among cognitively unimpaired older adults
title_full_unstemmed Protective effects of sleep duration and physical activity on cognitive performance are influenced by β-amyloid and brain volume but not tau burden among cognitively unimpaired older adults
title_short Protective effects of sleep duration and physical activity on cognitive performance are influenced by β-amyloid and brain volume but not tau burden among cognitively unimpaired older adults
title_sort protective effects of sleep duration and physical activity on cognitive performance are influenced by β-amyloid and brain volume but not tau burden among cognitively unimpaired older adults
topic Regular Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10316126/
https://www.ncbi.nlm.nih.gov/pubmed/37379733
http://dx.doi.org/10.1016/j.nicl.2023.103460
work_keys_str_mv AT aslanyanvahan protectiveeffectsofsleepdurationandphysicalactivityoncognitiveperformanceareinfluencedbybamyloidandbrainvolumebutnottauburdenamongcognitivelyunimpairedolderadults
AT orteganancy protectiveeffectsofsleepdurationandphysicalactivityoncognitiveperformanceareinfluencedbybamyloidandbrainvolumebutnottauburdenamongcognitivelyunimpairedolderadults
AT fentonlaura protectiveeffectsofsleepdurationandphysicalactivityoncognitiveperformanceareinfluencedbybamyloidandbrainvolumebutnottauburdenamongcognitivelyunimpairedolderadults
AT harrisontheresam protectiveeffectsofsleepdurationandphysicalactivityoncognitiveperformanceareinfluencedbybamyloidandbrainvolumebutnottauburdenamongcognitivelyunimpairedolderadults
AT ramanrema protectiveeffectsofsleepdurationandphysicalactivityoncognitiveperformanceareinfluencedbybamyloidandbrainvolumebutnottauburdenamongcognitivelyunimpairedolderadults
AT mackwendyj protectiveeffectsofsleepdurationandphysicalactivityoncognitiveperformanceareinfluencedbybamyloidandbrainvolumebutnottauburdenamongcognitivelyunimpairedolderadults
AT pajudy protectiveeffectsofsleepdurationandphysicalactivityoncognitiveperformanceareinfluencedbybamyloidandbrainvolumebutnottauburdenamongcognitivelyunimpairedolderadults