Multimodal neuroimaging correlates of spectral power in NREM sleep delta sub-bands in cognitively unimpaired older adults

Author:

Champetier Pierre12ORCID,André Claire1ORCID,Rehel Stéphane12,Ourry Valentin12ORCID,Landeau Brigitte1,Mézenge Florence1,Roquet Daniel1ORCID,Vivien Denis13,de La Sayette Vincent4,Chételat Gaël1,Rauchs Géraldine1ORCID, ,Bejanin Alexandre5,Chauveau Léa5,Chocat Anne5,Collette Fabienne678,Dautricourt Sophie5,De Flores Robin5,Delarue Marion5,Demnitz-King Harriet9,Espérou Hélène10,Fauvel Séverine5,Felisatti Francesca5,Ferrand Devouge Eglantine5111213,Frison Eric14,Gonneaud Julie5,Haudry Sacha5,Hébert Oriane5,Klimecki Olga1516,Kuhn Elizabeth5,Landeau Brigitte5,Lefranc Valérie5,Marchant Natalie9,Mezenge Florence5,Palix Cassandre5,Quillard Anne5,Requier Florence6,Salmon Eric17,Touron Edelweiss5,Turpin Anne-Laure5,Vuilleumier Patrik1819,Whitfield Tim9,Wirth Miranka2021

Affiliation:

1. Normandie Univ, UNICAEN, INSERM, U1237, PhIND “Physiopathology and Imaging of Neurological Disorders,” NeuroPresage Team, Institut Blood and Brain @ Caen-Normandie, GIP Cyceron , 14000 Caen , France

2. Normandie Univ, UNICAEN, PSL Université, EPHE, INSERM, U1077, CHU de Caen, GIP Cyceron, NIMH , 14000 Caen , France

3. Département de Recherche Clinique, CHU Caen-Normandie , Caen , France

4. Service de Neurologie, CHU de Caen , Caen , France

5. Normandie Univ, UNICAEN, INSERM, U1237, PhIND Physiopathology and Imaging of Neurological Disorders, Institut Blood and Brain @ Caen-Normandie , Cyceron, 14000 Caen , France

6. GIGA-CRC In Vivo Imaging, Université de Liège, National Fund for Scientific Research (F.R.S-FNRS) , Liège , Belgium

7. Psychology and Neuroscience of Cognition, University of Liège , Liège , Belgium

8. Fund for Scientific Research FNRS , 1000, Brussels , Belgium

9. Division of Psychiatry, University College London , London , United Kingdom

10. Inserm, pôle de recherche clinique, institut de santé publique , 75013 Paris , France

11. Normandie Univ, UNIROUEN, Department of General Practice , Rouen , France

12. Rouen University Hospital , CIC-CRB 1404, F 76000, Rouen , France

13. CHU Bordeaux, Service d’information médicale , Bordeaux , France

14. EUCLID/F-CRIN Clinical Trials Platform, Univ. Bordeaux, Inserm, Bordeaux Population Health Center , Bordeaux , France

15. Swiss Center for Affective Sciences, Department of Medicine and Department of Psychology, University of Geneva , Geneva , Switzerland

16. Clinical Psychology and Behavioral Neuroscience, Faculty of Psychology, Technische Universität Dresden , 01187, Dresden , Germany

17. Division of Nuclear Medicine, Department of Medical Physics, Cyclotron Research Center, University Hospital of Liège, University of Liège , Liège , Belgium

18. Swiss Center for Affective Sciences, University of Geneva , Geneva , Switzerland

19. Laboratory for Behavioral Neurology and Imaging of Cognition, Department of Neuroscience, Medical School, University of Geneva , Geneva , Switzerland

20. Charité-Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humbold- Universität zu Berlin and Berlin Institute of Health, NeuroCure Clinical Research Center , Berlin , Germany

21. German Center for Neurodegenerative Diseases (DZNE) , Dresden , Germany

Abstract

Abstract Study Objectives In aging, reduced delta power (0.5–4 Hz) during N2 and N3 sleep has been associated with gray matter (GM) atrophy and hypometabolism within frontal regions. Some studies have also reported associations between N2 and N3 sleep delta power in specific sub-bands and amyloid pathology. Our objective was to better understand the relationships between spectral power in delta sub-bands during N2–N3 sleep and brain integrity using multimodal neuroimaging. Methods In-home polysomnography was performed in 127 cognitively unimpaired older adults (mean age ± SD: 69.0 ± 3.8 years). N2–N3 sleep EEG power was calculated in delta (0.5–4 Hz), slow delta (0.5–1 Hz), and fast delta (1–4 Hz) frequency bands. Participants also underwent magnetic resonance imaging and Florbetapir-PET (early and late acquisitions) scans to assess GM volume, brain perfusion, and amyloid burden. Amyloid accumulation over ~21 months was also quantified. Results Higher delta power was associated with higher GM volume mainly in fronto-cingular regions. Specifically, slow delta power was positively correlated with GM volume and perfusion in these regions, while the inverse association was observed with fast delta power. Delta power was neither associated with amyloid burden at baseline nor its accumulation over time, whatever the frequency band considered. Conclusions Our results show that slow delta is particularly associated with preserved brain structure, and highlight the importance of analyzing delta power sub-bands to better understand the associations between delta power and brain integrity. Further longitudinal investigations with long follow-ups are needed to disentangle the associations among sleep, amyloid pathology, and dementia risk in older populations. Clinical Trial Information Name: Study in Cognitively Intact Seniors Aiming to Assess the Effects of Meditation Training (Age-Well). URL: https://clinicaltrials.gov/ct2/show/NCT02977819?term=Age-Well&draw=2&rank=1. See STROBE_statement_AGEWELL in supplemental materials. Registration EudraCT: 2016-002441-36; IDRCB: 2016-A01767-44; ClinicalTrials.gov Identifier: NCT02977819.

Funder

European Union’s Horizon

LECMA-Vaincre Alzheimer

Inserm, Region Normandie

Fonds Européen de Développement Régional

Publisher

Oxford University Press (OUP)

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