Rapid Eye Movement Sleep, Neurodegeneration, and Amyloid Deposition in Aging.
Journal
Annals of neurology
ISSN: 1531-8249
Titre abrégé: Ann Neurol
Pays: United States
ID NLM: 7707449
Informations de publication
Date de publication:
05 2023
05 2023
Historique:
revised:
09
01
2023
received:
19
10
2021
accepted:
11
01
2023
medline:
17
5
2023
pubmed:
16
1
2023
entrez:
15
1
2023
Statut:
ppublish
Résumé
Rapid eye movement (REM) sleep is markedly altered in Alzheimer's disease (AD), and its reduction in older populations is associated with AD risk. However, little is known about the underlying brain mechanisms. Our objective was to investigate the relationships between REM sleep integrity and amyloid deposition, gray matter volume, and perfusion in aging. We included 121 cognitively unimpaired older adults (76 women, mean age 68.96 ± 3.82 years), who underwent a polysomnography, T1-weighted magnetic resonance imaging, early and late Florbetapir positron emission tomography scans to evaluate gray matter volume, perfusion, and amyloid deposition. We computed indices reflecting REM sleep macro- and microstructural integrity (ie, normalized electroencephalographic spectral power values). Voxel-wise multiple regression analyses were conducted between REM sleep indices and neuroimaging data, controlling for age, sex, education, the apnea-hypopnea index, and the apolipoprotein E ε4 status. Lower perfusion in frontal, anterior and posterior cingulate, and precuneus areas was associated with decreased delta power and electroencephalographic slowing (slow/fast frequencies ratio), and increased alpha and beta power. To a lower extent, similar results were obtained between gray matter volume and delta, alpha, and beta power. In addition, lower REM sleep theta power was more marginally associated with greater diffuse amyloid deposition and lower gray matter volume in fronto-temporal and parieto-occipital areas. These results suggest that alterations of REM sleep microstructure are associated with greater neurodegeneration and neocortical amyloid deposition in older adults. Further studies are warranted to replicate these findings, and determine whether older adults exhibiting REM sleep alterations are more at risk of cognitive decline and belonging to the Alzheimer's continuum. ANN NEUROL 2023;93:979-990.
Substances chimiques
Amyloid beta-Peptides
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
979-990Informations de copyright
© 2023 The Authors. Annals of Neurology published by Wiley Periodicals LLC on behalf of American Neurological Association.
Références
Reinoso-Suárez F, de Andrés I, Rodrigo-Angulo ML, Garzón M. Brain structures and mechanisms involved in the generation of REM sleep. Sleep Med Rev 2001;5:63-77.
Platt B, Riedel G. The cholinergic system, EEG and sleep. Behav Brain Res 2011;221:499-504.
Petit D, Gagnon J-FF, Fantini ML, et al. Sleep and quantitative EEG in neurodegenerative disorders. J Psychosom Res 2004;56:487-496.
Hassainia F, Petit D, Nielsen T, et al. Quantitative EEG and statistical mapping of wakefulness and REM sleep in the evaluation of mild to moderate Alzheimer's disease. Eur Neurol 1997;37:219-224.
Peter-Derex L, Yammine P, Bastuji H, Croisile B. Sleep and Alzheimer's disease. Sleep Med Rev 2015;19:29-38.
Maestri M, Carnicelli L, Tognoni G, et al. Non-rapid eye movement sleep instability in mild cognitive impairment: a pilot study. Sleep Med 2015;16:1139-1145.
Liguori C, Nuccetelli M, Izzi F, et al. Rapid eye movement sleep disruption and sleep fragmentation are associated with increased orexin-a cerebrospinal-fluid levels in mild cognitive impairment due to Alzheimer's disease. Neurobiol Aging 2016;40:120-126.
D'Rozario AL, Chapman JL, Phillips CL, et al. Objective measurement of sleep in mild cognitive impairment: a systematic review and meta-analysis. Sleep Med Rev 2020;52:101308.
Carnicelli L, Maestri M, di Coscio E, et al. A longitudinal study of polysomnographic variables in patients with mild cognitive impairment converting to Alzheimer's disease. J Sleep Res 2019;28:e12821.
Hita-Yanez E, Atienza M, Gil-Neciga E, Cantero J. Disturbed sleep patterns in elders with mild cognitive impairment: the role of memory decline and ApoE ε4 genotype. Curr Alzheimer Res 2012;9:290-297.
Brayet P, Petit D, Frauscher B, et al. Quantitative EEG of rapid-eye-movement sleep: a marker of amnestic mild cognitive impairment. Clin EEG Neurosci 2016;47:134-141.
Song Y, Blackwell T, Yaffe K, et al. Relationships between sleep stages and changes in cognitive function in older men: the MrOS sleep study. Sleep 2015;38:411-421.
Pase MP, Himali JJ, Grima NA, et al. Sleep architecture and the risk of incident dementia in the community. Neurology 2017;89:1244-1250.
Braak H, Braak E. Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol 1991;82:239-259.
Serrano-Pozo A, Frosch MP, Masliah E, Hyman BT. Neuropathological alterations in Alzheimer disease. Cold Spring Harb Perspect Med 2011;1:a006189.
Park S-H, Weber F. Neural and homeostatic regulation of REM sleep. Front Psychol 2020;11:1662.
Peever J, Fuller PM. Neuroscience: a distributed neural network controls REM sleep. Curr Biol 2016;26:R34-R35.
Latreille V, Gaubert M, Dubé J, et al. Age-related cortical signatures of human sleep electroencephalography. Neurobiol Aging 2019;76:106-114.
Poisnel G, Arenaza-Urquijo E, Collette F, et al. The age-well randomized controlled trial of the Medit-ageing European project: effect of meditation or foreign language training on brain and mental health in older adults. Alzheimer's Dement 2018;4:714-723.
Berry RB, Brooks R, Gamaldo C, et al. AASM scoring manual updates for 2017 (version 2.4). J Clin Sleep Med 2017;13:665-666.
Berthomier C, Drouot X, Herman-Stoïca M, et al. Automatic analysis of single-channel sleep EEG: validation in healthy individuals. Sleep 2007;30:1587-1595.
Chylinski D, Berthomier C, Lambot E, et al. Variability of sleep stage scoring in late midlife and early old age. J Sleep Res 2021;31:e13424.
Taillard J, Sagaspe P, Berthomier C, et al. Non-REM sleep characteristics predict early cognitive impairment in an aging population. Front Neurol 2019;10:197.
Paulson OB, Hasselbalch SG, Rostrup E, et al. Cerebral blood flow response to functional activation. J Cereb Blood Flow Metab 2010;30:2-14.
André C, Rehel S, Kuhn E, et al. Association of sleep-disordered breathing with Alzheimer disease biomarkers in community-dwelling older adults: a secondary analysis of a randomized clinical trial. JAMA Neurol 2020;77:716-724.
Jack CR, Bennett DA, Blennow K, et al. NIA-AA research framework: toward a biological definition of Alzheimer's disease. Alzheimer's Dement 2018;14:535-562.
Mander BA, Marks SM, Vogel JW, et al. β-Amyloid disrupts human NREM slow waves and related hippocampus-dependent memory consolidation. Nat Neurosci 2015;18:1051-1057.
Winer JR, Mander BA, Kumar S, et al. Sleep disturbance forecasts β-amyloid accumulation across subsequent years. Curr Biol 2020;30:4291-4298.e3.
Varga AW, Wohlleber ME, Giménez S, et al. Reduced slow-wave sleep is associated with high cerebrospinal fluid Aβ42 levels in cognitively normal elderly. Sleep 2016;39:2041-2048.
Bubu OM, Umasabor-Bubu OQ, Turner AD, et al. Self-reported obstructive sleep apnea, amyloid and tau burden, and Alzheimer's disease time-dependent progression. Alzheimer's Dement 2021;17:226-245.
Carvalho DZ, St Louis EK, Knopman DS, et al. Association of excessive daytime sleepiness with longitudinal β-amyloid accumulation in elderly persons without dementia. JAMA Neurol 2018;75:672-680.
Spira AP, An Y, Wu MN, et al. Excessive daytime sleepiness and napping in cognitively normal adults: associations with subsequent amyloid deposition measured by PiB PET. Sleep 2018;41:zsy152.
Petit D, Lorrain D, Gauthier S, Montplaisir J. Regional spectral analysis of the REM sleep EEG in mild to moderate Alzheimer's disease. Neurobiol Aging 1993;14:141-145.
Liguori C, Romigi A, Nuccetelli M, et al. Orexinergic system dysregulation, sleep impairment, and cognitive decline in Alzheimer disease. JAMA Neurol 2014;71:1498-1505.
Theofilas P, Ehrenberg AJ, Dunlop S, et al. Locus coeruleus volume and cell population changes during Alzheimer's disease progression: a stereological study in human postmortem brains with potential implication for early-stage biomarker discovery. Alzheimer's Dement 2017;13:236-246.
Oh J, Eser RA, Ehrenberg AJ, et al. Profound degeneration of wake-promoting neurons in Alzheimer's disease. Alzheimer's Dement 2019;15:1253-1263.
Grothe M, Heinsen H, Teipel SJ. Atrophy of the cholinergic basal forebrain over the adult age range and in early stages of Alzheimer's disease. Biol Psychiatry 2012;71:805-813.
Schmitz TW, Nathan SR. Basal forebrain degeneration precedes and predicts the cortical spread of Alzheimer's pathology. Nat Commun 2016;7:13249.
Buzsáki G. Theta oscillations in the hippocampus. Neuron 2002;33:325-340.
dos Santos Moraes WA, Poyares DR, Guilleminault C, et al. The effect of donepezil on sleep and REM sleep EEG in patients with Alzheimer disease: a double-blind placebo-controlled study. Sleep 2006;29:199-205.
DeKosky ST, Ikonomovic MD, Styren SD, et al. Upregulation of choline acetyltransferase activity in hippocampus and frontal cortex of elderly subjects with mild cognitive impairment. Ann Neurol 2002;51:145-155.
Ikonomovic MD, Mufson EJ, Wuu J, et al. Cholinergic plasticity in hippocampus of individuals with mild cognitive impairment: correlation with Alzheimer's neuropathology. J Alzheimers Dis 2003;5:39-48.
Westerberg CE, Mander BA, Florczak SM, et al. Concurrent impairments in sleep and memory in amnestic mild cognitive impairment. J Int Neuropsychol Soc 2012;18:490-500.
Scarpelli S, D'Atri A, Bartolacci C, et al. Oscillatory EEG activity during REM sleep in elderly people predicts subsequent dream recall after awakenings. Front Neurol 2019;10:985.
Landolt H-P, Borbély AA. Age-dependent changes in sleep EEG topography. Clin Neurophysiol 2001;112:369-377.
Bero AW, Yan P, Roh JH, et al. Neuronal activity regulates the regional vulnerability to amyloid-β deposition. Nat Neurosci 2011;14:750-756.
Szelies B, Grond M, Herholz K, et al. Quantitative EEG mapping and PET in Alzheimer's disease. J Neurol Sci 1992;110:46-56.