Circadian Rapid Eye Movement Sleep Expression is Associated with Brain Microstructural Integrity in Older Adults

Overview

Journal Commun Biol

Specialty Biology

Date 2024 Jun 22

PMID 38909162

Authors

Michele Deantoni

Mathilde Reyt

Marine Dourte

Stella de Haan

Alexia Lesoinne

Gilles Vandewalle

Christophe Phillips

Christian Berthomier

Pierre Maquet

Vincenzo Muto

Gregory Hammad

Christina Schmidt

Marion Baillet

Affiliations

Soon will be listed here.

Abstract

Rapid eye movement sleep (REMS) is increasingly suggested as a discriminant sleep state for subtle signs of age-related neurodegeneration. While REMS expression is under strong circadian control and circadian dysregulation increases with age, the association between brain aging and circadian REMS regulation has not yet been assessed. Here, we measure the circadian amplitude of REMS through a 40-h in-lab multiple nap protocol in controlled laboratory conditions, and brain microstructural integrity with quantitative multi-parameter mapping (MPM) imaging in 86 older individuals. We show that reduced circadian REMS amplitude is related to lower magnetization transfer saturation (MTsat), longitudinal relaxation rate (R1) and effective transverse relaxation rate (R2*) values in several white matter regions mostly located around the lateral ventricles, and with lower R1 values in grey matter clusters encompassing the hippocampus, parahippocampus, thalamus and hypothalamus. Our results further highlight the importance of considering circadian regulation for understanding the association between sleep and brain structure in older individuals.

References

Birkl C, Doucette J, Fan M, Hernandez-Torres E, Rauscher A . Myelin water imaging depends on white matter fiber orientation in the human brain. Magn Reson Med. 2020; 85(4):2221-2231. PMC: 7821018. DOI: 10.1002/mrm.28543. View

Snaidero N, Simons M . Myelination at a glance. J Cell Sci. 2014; 127(Pt 14):2999-3004. DOI: 10.1242/jcs.151043. View

Baillet M, Dilharreguy B, Peres K, Dartigues J, Mayo W, Catheline G . Activity/rest cycle and disturbances of structural backbone of cerebral networks in aging. Neuroimage. 2016; 146:814-820. DOI: 10.1016/j.neuroimage.2016.09.051. View

Wurts S, Edgar D . Circadian and homeostatic control of rapid eye movement (REM) sleep: promotion of REM tendency by the suprachiasmatic nucleus. J Neurosci. 2000; 20(11):4300-10. PMC: 6772655. View

Palmer J, Duffy S, Meares S, Pye J, Calamante F, Cespedes M . Rest-activity functioning is related to white matter microarchitecture and modifiable risk factors in older adults at-risk for dementia. Sleep. 2021; 44(7). DOI: 10.1093/sleep/zsab007. View

Louie K, Wilson M . Temporally structured replay of awake hippocampal ensemble activity during rapid eye movement sleep. Neuron. 2001; 29(1):145-56. DOI: 10.1016/s0896-6273(01)00186-6. View

Scammell T, Arrigoni E, Lipton J . Neural Circuitry of Wakefulness and Sleep. Neuron. 2017; 93(4):747-765. PMC: 5325713. DOI: 10.1016/j.neuron.2017.01.014. View

McMahon M, Malneedi Y, Worthy D, Schnyer D . Rest-activity rhythms and white matter microstructure across the lifespan. Sleep. 2020; 44(6). PMC: 8193551. DOI: 10.1093/sleep/zsaa266. View

Langkammer C, Krebs N, Goessler W, Scheurer E, Ebner F, Yen K . Quantitative MR imaging of brain iron: a postmortem validation study. Radiology. 2010; 257(2):455-62. DOI: 10.1148/radiol.10100495. View

10.

van Someren E, Oosterman J, Van Harten B, Vogels R, Gouw A, Weinstein H . Medial temporal lobe atrophy relates more strongly to sleep-wake rhythm fragmentation than to age or any other known risk. Neurobiol Learn Mem. 2018; 160:132-138. DOI: 10.1016/j.nlm.2018.05.017. View

11.

Saper C, Scammell T, Lu J . Hypothalamic regulation of sleep and circadian rhythms. Nature. 2005; 437(7063):1257-63. DOI: 10.1038/nature04284. View

12.

Smith S, Elliott L, Alfaro-Almagro F, McCarthy P, Nichols T, Douaud G . Brain aging comprises many modes of structural and functional change with distinct genetic and biophysical associations. Elife. 2020; 9. PMC: 7162660. DOI: 10.7554/eLife.52677. View

13.

Dijk D, Czeisler C . Contribution of the circadian pacemaker and the sleep homeostat to sleep propensity, sleep structure, electroencephalographic slow waves, and sleep spindle activity in humans. J Neurosci. 1995; 15(5 Pt 1):3526-38. PMC: 6578184. View

14.

Rooney W, Johnson G, Li X, Cohen E, Kim S, Ugurbil K . Magnetic field and tissue dependencies of human brain longitudinal 1H2O relaxation in vivo. Magn Reson Med. 2007; 57(2):308-18. DOI: 10.1002/mrm.21122. View

15.

Munch M, Knoblauch V, Blatter K, Schroder C, Schnitzler C, Krauchi K . Age-related attenuation of the evening circadian arousal signal in humans. Neurobiol Aging. 2005; 26(9):1307-19. DOI: 10.1016/j.neurobiolaging.2005.03.004. View

16.

Pase M, Himali J, Grima N, Beiser A, Satizabal C, Aparicio H . Sleep architecture and the risk of incident dementia in the community. Neurology. 2017; 89(12):1244-1250. PMC: 5606917. DOI: 10.1212/WNL.0000000000004373. View

17.

Zhong H, Yu B, Luo D, Yang L, Zhang J, Jiang S . Roles of aging in sleep. Neurosci Biobehav Rev. 2019; 98:177-184. DOI: 10.1016/j.neubiorev.2019.01.013. View

18.

Frisoni G, Fox N, Jack Jr C, Scheltens P, Thompson P . The clinical use of structural MRI in Alzheimer disease. Nat Rev Neurol. 2010; 6(2):67-77. PMC: 2938772. DOI: 10.1038/nrneurol.2009.215. View

19.

Lew C, Petersen C, Neylan T, Grinberg L . Tau-driven degeneration of sleep- and wake-regulating neurons in Alzheimer's disease. Sleep Med Rev. 2021; 60:101541. PMC: 8862638. DOI: 10.1016/j.smrv.2021.101541. View

20.

Van Egroo M, Narbutas J, Chylinski D, Villar Gonzalez P, Maquet P, Salmon E . Sleep-wake regulation and the hallmarks of the pathogenesis of Alzheimer's disease. Sleep. 2019; 42(4). DOI: 10.1093/sleep/zsz017. View