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Self-reported sleep problems are related to cortical thinning in aging but not memory decline and amyloid-β accumulation – results from the Lifebrain consortium

View ORCID ProfileAnders M. Fjell, Øystein Sørensen, View ORCID ProfileInge K. Amlien, View ORCID ProfileDavid Bartrés-Faz, View ORCID ProfileAndreas M. Brandmaier, View ORCID ProfileNikolaus Buchmann, View ORCID ProfileIlja Demuth, View ORCID ProfileChristian A Drevon, Sandra Düzel, View ORCID ProfileKlaus P. Ebmeier, View ORCID ProfilePaolo Ghisletta, Ane-Victoria Idland, View ORCID ProfileTim C. Kietzmann, View ORCID ProfileRogier A. Kievit, View ORCID ProfileSimone Kühn, View ORCID ProfileUlman Lindenberger, Fredrik Magnussen, Didac Macià, View ORCID ProfileAthanasia M. Mowinckel, View ORCID ProfileLars Nyberg, Claire E. Sexton, Cristina Solé-Padullés, View ORCID ProfileSara Pudas, James M. Roe, Donatas Sederevicius, View ORCID ProfileSana Suri, View ORCID ProfileDidac Vidal-Piñeiro, Gerd Wagner, View ORCID ProfileLeiv Otto Watne, René Westerhausen, Enikő Zsoldos, View ORCID ProfileKristine B. Walhovd, for the Alzheimer’s Disease Neuroimaging Initiative
doi: https://doi.org/10.1101/2020.04.28.065474
Anders M. Fjell
1Center for Lifespan Changes in Brain and Cognition, University of Oslo, Norway
2Department of Radiology and Nuclear Medicine, Oslo University Hospital, Norway
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  • For correspondence: andersmf@psykologi.uio.no
Øystein Sørensen
1Center for Lifespan Changes in Brain and Cognition, University of Oslo, Norway
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Inge K. Amlien
1Center for Lifespan Changes in Brain and Cognition, University of Oslo, Norway
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  • ORCID record for Inge K. Amlien
David Bartrés-Faz
3Departament de Medicina, Facultat de Medicina i Ciències de la Salut, Universitat de Barcelona, and Institut de Neurociències, Universitat de Barcelona, Spain
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Andreas M. Brandmaier
6Center for Lifespan Psychology, Max Planck Institute for Human Development, Berlin, Germany
7Max Planck UCL Centre for Computational Psychiatry and Ageing Research, Berlin, Germany, and London, United Kingdom
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Nikolaus Buchmann
17Department of Cardiology, Charité - University Medicine Berlin Campus Benjamin Franklin, Berlin, Germany
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  • ORCID record for Nikolaus Buchmann
Ilja Demuth
4Charité – Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Lipid Clinic at the Interdisciplinary Metabolism Center, Germany; Charité - Universitätsmedizin Berlin, BCRT - Berlin Institute of Health Center for Regenerative Therapies, Berlin, Germany
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Christian A Drevon
5Vitas AS, Research Park, Gaustadalleen 21, 0349, Oslo
20Department of Nutrition, Institute of Basic Medical Sciences, Faculty of Medicine, University of Oslo, Norway
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Sandra Düzel
6Center for Lifespan Psychology, Max Planck Institute for Human Development, Berlin, Germany
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Klaus P. Ebmeier
8Department of Psychiatry, University of Oxford, United Kingdom
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Paolo Ghisletta
18Faculty of Psychology and Educational Sciences, University of Geneva, Switzerland; Swiss Distance University Institute, Switzerland; Swiss National Centre of Competence in Research LIVES, University of Geneva, Switzerland
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Ane-Victoria Idland
1Center for Lifespan Changes in Brain and Cognition, University of Oslo, Norway
9Oslo Delirium Research Group, Department of Geriatric Medicine, University of Oslo, Norway
10Institute of Basic Medical Sciences, University of Oslo, Norway
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Tim C. Kietzmann
11MRC Cognition and Brain Sciences Unit, University of Cambridge, United Kingdom
19Donders Institute for Brain, Cognition and Behaviour, Radboud University, Nijmegen, the Netherlands
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Rogier A. Kievit
11MRC Cognition and Brain Sciences Unit, University of Cambridge, United Kingdom
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Simone Kühn
6Center for Lifespan Psychology, Max Planck Institute for Human Development, Berlin, Germany
12Department of Psychiatry and Psychotherapy, University Medical Center Hamburg-Eppendorf, Germany
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Ulman Lindenberger
6Center for Lifespan Psychology, Max Planck Institute for Human Development, Berlin, Germany
7Max Planck UCL Centre for Computational Psychiatry and Ageing Research, Berlin, Germany, and London, United Kingdom
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  • ORCID record for Ulman Lindenberger
Fredrik Magnussen
1Center for Lifespan Changes in Brain and Cognition, University of Oslo, Norway
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Didac Macià
3Departament de Medicina, Facultat de Medicina i Ciències de la Salut, Universitat de Barcelona, and Institut de Neurociències, Universitat de Barcelona, Spain
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Athanasia M. Mowinckel
1Center for Lifespan Changes in Brain and Cognition, University of Oslo, Norway
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  • ORCID record for Athanasia M. Mowinckel
Lars Nyberg
13Umeå Center for Functional Brain Imaging, Umeå University, Umeå, Sweden
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Claire E. Sexton
8Department of Psychiatry, University of Oxford, United Kingdom
14Global Brain Health Institute, Department of Neurology, University of California San Francisco, California, USA
15Wellcome Centre for Integrative Neuroimaging, University of Oxford, United Kingdom
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Cristina Solé-Padullés
3Departament de Medicina, Facultat de Medicina i Ciències de la Salut, Universitat de Barcelona, and Institut de Neurociències, Universitat de Barcelona, Spain
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Sara Pudas
13Umeå Center for Functional Brain Imaging, Umeå University, Umeå, Sweden
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James M. Roe
1Center for Lifespan Changes in Brain and Cognition, University of Oslo, Norway
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Donatas Sederevicius
1Center for Lifespan Changes in Brain and Cognition, University of Oslo, Norway
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Sana Suri
8Department of Psychiatry, University of Oxford, United Kingdom
15Wellcome Centre for Integrative Neuroimaging, University of Oxford, United Kingdom
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Didac Vidal-Piñeiro
1Center for Lifespan Changes in Brain and Cognition, University of Oslo, Norway
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  • ORCID record for Didac Vidal-Piñeiro
Gerd Wagner
16Psychiatric Brain and Body Research Group, Department of Psychiatry and Psychotherapy, Jena University Hospital, Jena, Germany
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Leiv Otto Watne
9Oslo Delirium Research Group, Department of Geriatric Medicine, University of Oslo, Norway
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René Westerhausen
1Center for Lifespan Changes in Brain and Cognition, University of Oslo, Norway
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Enikő Zsoldos
8Department of Psychiatry, University of Oxford, United Kingdom
15Wellcome Centre for Integrative Neuroimaging, University of Oxford, United Kingdom
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Kristine B. Walhovd
1Center for Lifespan Changes in Brain and Cognition, University of Oslo, Norway
2Department of Radiology and Nuclear Medicine, Oslo University Hospital, Norway
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Abstract

Background Older persons with poor sleep are more likely to develop neurodegenerative disease, but the causality underlying this association is unclear. To move towards explanation, we examine whether sleep quality and quantity are similarly associated with brain changes across the adult lifespan.

Methods Associations between self-reported sleep parameters (Pittsburgh Sleep Quality Index;PSQI) and longitudinal cortical change were tested using five samples from the Lifebrain consortium (n=2205, 4363 MRIs, 18-92 years). Analyses were augmented by considering episodic memory change, gene expression from the Allen Human Brain Atlas, and amyloid-beta (Aβ) accumulation (n=1980).

Results PSQI components sleep problems and low sleep quality were related to thinning of the right lateral temporal cortex. The association with sleep problems emerged after 60 years, especially in regions with high expression of genes related to oligodendrocytes and S1 pyramidal neurons. BMI and symptoms of depression had negligible effects. Sleep problems were neither related to longitudinal change in episodic memory function nor to Aβ accumulation, suggesting that sleep-related cortical changes were independent of AD neuropathology and cognitive decline.

Conclusion Worse self-reported sleep in later adulthood was associated with more cortical thinning in regions of high expression of genes related to oligodendrocytes and S1 pyramidal neurons, but not to Aβ accumulation or memory decline. The relationship to cortical brain change suggests that self-reported sleep parameters are relevant in lifespan studies, but small effect sizes, except for a few restricted regions, indicate that self-reported sleep is not a good biomarker of general cortical degeneration in healthy older adults.

Competing Interest Statement

Claire E Sexton reports consulting fees from Jazz Pharmaceuticals and is now a full-time employee of the Alzheimer’s Association. Christian A Drevon is a cofounder, stock-owner, board member and consultant in the contract laboratory Vitas AS, performing personalised analyses of blood biomarkers. The rest of the authors report no conflicts of interest.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Self-reported sleep problems are related to cortical thinning in aging but not memory decline and amyloid-β accumulation – results from the Lifebrain consortium
Anders M. Fjell, Øystein Sørensen, Inge K. Amlien, David Bartrés-Faz, Andreas M. Brandmaier, Nikolaus Buchmann, Ilja Demuth, Christian A Drevon, Sandra Düzel, Klaus P. Ebmeier, Paolo Ghisletta, Ane-Victoria Idland, Tim C. Kietzmann, Rogier A. Kievit, Simone Kühn, Ulman Lindenberger, Fredrik Magnussen, Didac Macià, Athanasia M. Mowinckel, Lars Nyberg, Claire E. Sexton, Cristina Solé-Padullés, Sara Pudas, James M. Roe, Donatas Sederevicius, Sana Suri, Didac Vidal-Piñeiro, Gerd Wagner, Leiv Otto Watne, René Westerhausen, Enikő Zsoldos, Kristine B. Walhovd, for the Alzheimer’s Disease Neuroimaging Initiative
bioRxiv 2020.04.28.065474; doi: https://doi.org/10.1101/2020.04.28.065474
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Self-reported sleep problems are related to cortical thinning in aging but not memory decline and amyloid-β accumulation – results from the Lifebrain consortium
Anders M. Fjell, Øystein Sørensen, Inge K. Amlien, David Bartrés-Faz, Andreas M. Brandmaier, Nikolaus Buchmann, Ilja Demuth, Christian A Drevon, Sandra Düzel, Klaus P. Ebmeier, Paolo Ghisletta, Ane-Victoria Idland, Tim C. Kietzmann, Rogier A. Kievit, Simone Kühn, Ulman Lindenberger, Fredrik Magnussen, Didac Macià, Athanasia M. Mowinckel, Lars Nyberg, Claire E. Sexton, Cristina Solé-Padullés, Sara Pudas, James M. Roe, Donatas Sederevicius, Sana Suri, Didac Vidal-Piñeiro, Gerd Wagner, Leiv Otto Watne, René Westerhausen, Enikő Zsoldos, Kristine B. Walhovd, for the Alzheimer’s Disease Neuroimaging Initiative
bioRxiv 2020.04.28.065474; doi: https://doi.org/10.1101/2020.04.28.065474

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