Timely coupling of sleep spindles and slow waves linked to early amyloid-β burden and predicts memory decline

Sleep alteration is a hallmark of ageing and emerges as a risk factor for Alzheimer’s disease (AD). While the fine-tuned coalescence of sleep microstructure elements may influence age-related cognitive trajectories, its association with AD processes is not fully established. Here, we investigated wh...

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Main Authors: Daphne Chylinski, Maxime Van Egroo, Justinas Narbutas, Vincenzo Muto, Mohamed Ali Bahri, Christian Berthomier, Eric Salmon, Christine Bastin, Christophe Phillips, Fabienne Collette, Pierre Maquet, Julie Carrier, Jean-Marc Lina, Gilles Vandewalle
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2022-05-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/78191
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author Daphne Chylinski
Maxime Van Egroo
Justinas Narbutas
Vincenzo Muto
Mohamed Ali Bahri
Christian Berthomier
Eric Salmon
Christine Bastin
Christophe Phillips
Fabienne Collette
Pierre Maquet
Julie Carrier
Jean-Marc Lina
Gilles Vandewalle
author_facet Daphne Chylinski
Maxime Van Egroo
Justinas Narbutas
Vincenzo Muto
Mohamed Ali Bahri
Christian Berthomier
Eric Salmon
Christine Bastin
Christophe Phillips
Fabienne Collette
Pierre Maquet
Julie Carrier
Jean-Marc Lina
Gilles Vandewalle
author_sort Daphne Chylinski
collection DOAJ
description Sleep alteration is a hallmark of ageing and emerges as a risk factor for Alzheimer’s disease (AD). While the fine-tuned coalescence of sleep microstructure elements may influence age-related cognitive trajectories, its association with AD processes is not fully established. Here, we investigated whether the coupling of spindles and slow waves (SW) is associated with early amyloid-β (Aβ) brain burden, a hallmark of AD neuropathology, and cognitive change over 2 years in 100 healthy individuals in late-midlife (50–70 years; 68 women). We found that, in contrast to other sleep metrics, earlier occurrence of spindles on slow-depolarisation SW is associated with higher medial prefrontal cortex Aβ burden (p=0.014, r²β*=0.06) and is predictive of greater longitudinal memory decline in a large subsample (p=0.032, r²β*=0.07, N=66). These findings unravel early links between sleep, AD-related processes, and cognition and suggest that altered coupling of sleep microstructure elements, key to its mnesic function, contributes to poorer brain and cognitive trajectories in ageing.
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spelling doaj.art-85aa5a33addb4f68a514adaa12d065552022-12-22T02:05:34ZengeLife Sciences Publications LtdeLife2050-084X2022-05-011110.7554/eLife.78191Timely coupling of sleep spindles and slow waves linked to early amyloid-β burden and predicts memory declineDaphne Chylinski0https://orcid.org/0000-0002-7319-0859Maxime Van Egroo1Justinas Narbutas2Vincenzo Muto3Mohamed Ali Bahri4Christian Berthomier5Eric Salmon6https://orcid.org/0000-0003-2520-9241Christine Bastin7https://orcid.org/0000-0002-4556-9490Christophe Phillips8https://orcid.org/0000-0002-4990-425XFabienne Collette9Pierre Maquet10Julie Carrier11https://orcid.org/0000-0001-5311-2370Jean-Marc Lina12Gilles Vandewalle13https://orcid.org/0000-0003-2483-2752GIGA-Cyclotron Research Centre-In Vivo Imaging, University of Liège, Liège, BelgiumGIGA-Cyclotron Research Centre-In Vivo Imaging, University of Liège, Liège, BelgiumGIGA-Cyclotron Research Centre-In Vivo Imaging, University of Liège, Liège, Belgium; Psychology and Cognitive Neuroscience Research Unit, University of Liège, Liège, BelgiumGIGA-Cyclotron Research Centre-In Vivo Imaging, University of Liège, Liège, BelgiumGIGA-Cyclotron Research Centre-In Vivo Imaging, University of Liège, Liège, BelgiumPhysip SA, Paris, FranceGIGA-Cyclotron Research Centre-In Vivo Imaging, University of Liège, Liège, Belgium; Psychology and Cognitive Neuroscience Research Unit, University of Liège, Liège, Belgium; Department of Neurology, University Hospital of Liège, Liège, BelgiumGIGA-Cyclotron Research Centre-In Vivo Imaging, University of Liège, Liège, Belgium; Psychology and Cognitive Neuroscience Research Unit, University of Liège, Liège, BelgiumGIGA-Cyclotron Research Centre-In Vivo Imaging, University of Liège, Liège, Belgium; GIGA-In Silico Medicine, University of Liège, Liège, BelgiumGIGA-Cyclotron Research Centre-In Vivo Imaging, University of Liège, Liège, Belgium; Psychology and Cognitive Neuroscience Research Unit, University of Liège, Liège, BelgiumGIGA-Cyclotron Research Centre-In Vivo Imaging, University of Liège, Liège, Belgium; Department of Neurology, University Hospital of Liège, Liège, BelgiumCentre for Advanced Research in Sleep Medicine, Université de Montréal, Montreal, CanadaCentre for Advanced Research in Sleep Medicine, Université de Montréal, Montreal, CanadaGIGA-Cyclotron Research Centre-In Vivo Imaging, University of Liège, Liège, BelgiumSleep alteration is a hallmark of ageing and emerges as a risk factor for Alzheimer’s disease (AD). While the fine-tuned coalescence of sleep microstructure elements may influence age-related cognitive trajectories, its association with AD processes is not fully established. Here, we investigated whether the coupling of spindles and slow waves (SW) is associated with early amyloid-β (Aβ) brain burden, a hallmark of AD neuropathology, and cognitive change over 2 years in 100 healthy individuals in late-midlife (50–70 years; 68 women). We found that, in contrast to other sleep metrics, earlier occurrence of spindles on slow-depolarisation SW is associated with higher medial prefrontal cortex Aβ burden (p=0.014, r²β*=0.06) and is predictive of greater longitudinal memory decline in a large subsample (p=0.032, r²β*=0.07, N=66). These findings unravel early links between sleep, AD-related processes, and cognition and suggest that altered coupling of sleep microstructure elements, key to its mnesic function, contributes to poorer brain and cognitive trajectories in ageing.https://elifesciences.org/articles/78191sleepageingsleep slow wavesmemoryAlzheimer's disease
spellingShingle Daphne Chylinski
Maxime Van Egroo
Justinas Narbutas
Vincenzo Muto
Mohamed Ali Bahri
Christian Berthomier
Eric Salmon
Christine Bastin
Christophe Phillips
Fabienne Collette
Pierre Maquet
Julie Carrier
Jean-Marc Lina
Gilles Vandewalle
Timely coupling of sleep spindles and slow waves linked to early amyloid-β burden and predicts memory decline
eLife
sleep
ageing
sleep slow waves
memory
Alzheimer's disease
title Timely coupling of sleep spindles and slow waves linked to early amyloid-β burden and predicts memory decline
title_full Timely coupling of sleep spindles and slow waves linked to early amyloid-β burden and predicts memory decline
title_fullStr Timely coupling of sleep spindles and slow waves linked to early amyloid-β burden and predicts memory decline
title_full_unstemmed Timely coupling of sleep spindles and slow waves linked to early amyloid-β burden and predicts memory decline
title_short Timely coupling of sleep spindles and slow waves linked to early amyloid-β burden and predicts memory decline
title_sort timely coupling of sleep spindles and slow waves linked to early amyloid β burden and predicts memory decline
topic sleep
ageing
sleep slow waves
memory
Alzheimer's disease
url https://elifesciences.org/articles/78191
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