Divergent Associations of Slow-Wave Sleep versus Rapid Eye Movement Sleep with Plasma Amyloid-Beta.
Journal
Annals of neurology
ISSN: 1531-8249
Titre abrégé: Ann Neurol
Pays: United States
ID NLM: 7707449
Informations de publication
Date de publication:
16 Apr 2024
16 Apr 2024
Historique:
revised:
19
03
2024
received:
06
09
2023
accepted:
20
03
2024
medline:
16
4
2024
pubmed:
16
4
2024
entrez:
16
4
2024
Statut:
aheadofprint
Résumé
Recent evidence shows that during slow-wave sleep (SWS), the brain is cleared from potentially toxic metabolites, such as the amyloid-beta protein. Poor sleep or elevated cortisol levels can worsen amyloid-beta clearance, potentially leading to the formation of amyloid plaques, a neuropathological hallmark of Alzheimer disease. Here, we explored how nocturnal neural and endocrine activity affects amyloid-beta fluctuations in the peripheral blood. We acquired simultaneous polysomnography and all-night blood sampling in 60 healthy volunteers aged 20-68 years. Nocturnal plasma concentrations of amyloid-beta-40, amyloid-beta-42, cortisol, and growth hormone were assessed every 20 minutes. Amyloid-beta fluctuations were modeled with sleep stages, (non)oscillatory power, and hormones as predictors while controlling for age and participant-specific random effects. Amyloid-beta-40 and amyloid-beta-42 levels correlated positively with growth hormone concentrations, SWS proportion, and slow-wave (0.3-4Hz) oscillatory and high-band (30-48Hz) nonoscillatory power, but negatively with cortisol concentrations and rapid eye movement sleep (REM) proportion measured 40-100 minutes previously (all t values > |3|, p values < 0.003). Older participants showed higher amyloid-beta-40 levels. Slow-wave oscillations are associated with higher plasma amyloid-beta levels, whereas REM sleep is related to decreased amyloid-beta plasma levels, possibly representing changes in central amyloid-beta production or clearance. Strong associations between cortisol, growth hormone, and amyloid-beta presumably reflect the sleep-regulating role of the corresponding releasing hormones. A positive association between age and amyloid-beta-40 may indicate that peripheral clearance becomes less efficient with age. ANN NEUROL 2024.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : Dutch Research Council
Pays : Netherlands
Informations de copyright
© 2024 The Authors. Annals of Neurology published by Wiley Periodicals LLC on behalf of American Neurological Association.
Références
Xie L, Kang H, Xu Q, et al. Sleep drives metabolite clearance from the adult brain. Science 2013;342:373–377.
Ooms S, Overeem S, Besse K, et al. Effect of 1 night of total sleep deprivation on cerebrospinal fluid β‐amyloid 42 in healthy middle‐aged men: a randomized clinical trial. JAMA Neurol 2014;71:971–977.
Ju YES, Ooms SJ, Sutphen C, et al. Slow wave sleep disruption increases cerebrospinal fluid amyloid‐β levels. Brain 2017;140:2104–2111.
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.
Liu H, Barthélemy NR, Ovod V, et al. Acute sleep loss decreases CSF‐to‐blood clearance of Alzheimer's disease biomarkers. Alzheimers Dement 2023;19:3055–3064. https://doi.org/10.1002/alz.12930.
Spira AP, Gamaldo AA, An Y, et al. Self‐reported sleep and β‐amyloid deposition in community‐dwelling older adults. JAMA Neurol 2013;70:1537–1543.
Ju YES, Lucey BP, Holtzman DM. Sleep and Alzheimer disease pathology—a bidirectional relationship. Nat Rev Neurol 2014;10:115–119.
Ouanes S, Popp J. High cortisol and the risk of dementia and Alzheimer's disease: a review of the literature. Front Hum Neurosci 2019;11:11. https://doi.org/10.3389/fnagi.2019.00043.
Steiger A, Dresler M, Kluge M, Schüssler P. Pathology of sleep, hormones and depression. Pharmacopsychiatry 2013;46:S30–S35.
Ovod V, Ramsey KN, Mawuenyega KG, et al. Amyloid β concentrations and stable isotope labeling kinetics of human plasma specific to central nervous system amyloidosis. Alzheimers Dement 2017;13:841–849. https://doi.org/10.1016/j.jalz.2017.06.2266.
Lerche S, Brockmann K, Pilotto A, et al. Prospective longitudinal course of cognition in older subjects with mild parkinsonian signs. Alzheimer's Res Ther 2016;8:1–8.
Wen H, Liu Z. Separating fractal and oscillatory components in the power spectrum of neurophysiological signal. Brain Topogr 2016;29:13–26.
Oostenveld R, Fries P, Maris E, Schoffelen JM. FieldTrip: open source software for advanced analysis of MEG, EEG, and invasive electrophysiological data. Comput Intell Neurosci 2011;2011:1–9.
Rosenblum Y, Bovy L, Weber FD, et al. Increased aperiodic neural activity during sleep in major depressive disorder. Biol Psychiatry Glob Open Sci 2023;3:1021–1029. https://doi.org/10.1016/j.bpsgos.2022.10.001.
Rosenblum Y, Shiner T, Bregman N, et al. Decreased aperiodic neural activity in Parkinson's disease and dementia with Lewy bodies. J Neurol 2023;3:1–2. https://doi.org/10.1007/s00415-023-11728-9.
Gao R, Peterson EJ, Voytek B. Inferring synaptic excitation/inhibition balance from field potentials. Neuroimage 2017;158:70–78.
Lendner JD, Helfrich RF, Mander BA, et al. An electrophysiological marker of arousal level in humans. Elife 2020;9:e55092.
Benedict C, Blennow K, Zetterberg H, Cedernaes J. Effects of acute sleep loss on diurnal plasma dynamics of CNS health biomarkers in young men. Neurology 2020;94:e1181–e1189.
Huang Y, Potter R, Sigurdson W, et al. β‐Amyloid dynamics in human plasma. Arch Neurol 2012;69:1591–1597.
Grimmer T, Laub T, Hapfelmeier A, et al. The overnight reduction of amyloid β 1‐42 plasma levels is diminished by the extent of sleep fragmentation, sAPP‐β, and APOE ε4 in psychiatrists on call. Alzheimers Dement 2020;16:759–769.
Olsson M, Ärlig J, Hedner J, et al. Sleep deprivation and plasma biomarkers for Alzheimer's disease. Sleep Med 2019;57:92–93.
Chylinski D, Van Egroo M, Narbutas J, et al. Timely coupling of sleep spindles and slow waves linked to early amyloid‐β burden and predicts memory decline. Elife 2022;11:e78191. https://doi.org/10.7554/eLife.78191.
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. https://doi.org/10.1038/nn.4035.
Winer JR, Mander BA, Kumar S, et al. Sleep disturbance forecasts β‐amyloid accumulation across subsequent years. Curr Biol 2020;30:4291–4298. https://doi.org/10.1016/j.cub.2020.08.017.
Wang YR, Wang QH, Zhang T, et al. Associations between hepatic functions and plasma amyloid‐beta levels—implications for the capacity of liver in peripheral amyloid‐beta clearance. Mol Neurobiol 2017;54:2338–2344.
Roberts KF, Elbert DL, Kasten TP, et al. Amyloid‐β efflux from the central nervous system into the plasma. Ann Neurol 2014;76:837–844. https://doi.org/10.1002/ana.24270.
Ungurean G, Behroozi M, Boeger L, et al. Wide‐spread brain activation and reduced CSF flow during avian REM sleep. Nat Comm 2023;14(1):3259.
André C, Champetier P, Rehel S, et al. Rapid eye movement sleep, neurodegeneration, and amyloid deposition in aging. Ann Neurol 2023;93:979–990. https://doi.org/10.1002/ana.26604.
Niethard N, Hasegawa M, Itokazu T, et al. Sleep‐stage‐specific regulation of cortical excitation and inhibition. Curr Biol 2016;26:2739–2749.
Iaccarino HF, Singer AC, Martorell AJ, et al. Gamma frequency entrainment attenuates amyloid load and modifies microglia. Nature 2016;540:230–235.
Helfrich RF, Lendner JD, Knight RT. Aperiodic sleep networks promote memory consolidation. Trends Cogn Sci 2021;25:648–659. https://doi.org/10.1016/j.tics.2021.04.009.
Fultz NE, Bonmassar G, Setsompop K, et al. Coupled electrophysiological, hemodynamic, and cerebrospinal fluid oscillations in human sleep. Science 2019;366:628–631.
Green KN, Billings LM, Roozendaal B, et al. Glucocorticoids increase amyloid‐β and tau pathology in a mouse model of Alzheimer's disease. J Neurosci 2006;26:9047–9056.
Åberg ND, Brywe KG, Isgaard J. Aspects of growth hormone and insulin‐like growth factor‐I related to neuroprotection, regeneration, and functional plasticity in the adult brain. Scientific World Journal 2006;6:53–80.
Blattner MS, Panigrahi SK, Toedebusch CD, et al. Increased cerebrospinal fluid amyloid‐β during sleep deprivation in healthy middle‐aged adults is not due to stress or circadian disruption. J Alzheimers Dis 2020;75:471–482. https://doi.org/10.3233/JAD-191122.
Bu XL, Xiang Y, Jin WS, et al. Blood‐derived amyloid‐β protein induces Alzheimer's disease pathologies. Mol Psychiatry 2018;23:1948–1956.