Sleep as a Novel Biomarker and a Promising Therapeutic Target for Cerebral Small Vessel Disease: A Review Focusing on Alzheimer’s Disease and the Blood-Brain Barrier
Abstract
:1. Sleep as a Potential Biomarker of Alzheimer’S Disease
2. Slow Wave Activity as a Biomarker of Disruption of Blood-Brain Barrier
3. Slow Sleep Wave Enhancement Is Promising Therapy of Alzheimer’S Disease
4. Conclusions
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
Abbreviations
A | Beta-amyliod |
APQ4 | Aquaporin(s)-4 |
ARAS | reticular ascending system |
BBB | Blood–Brain Barrier |
CSF | Cerebral spinal fluid |
CSVD | Cerebral Small Vessel Disease |
GABAA | Gamma-aminobutyric acid A |
ISF | Interstitial fluid |
NA | Noradrenaline |
NREM | Non repaid eyes movement |
nNOS | Neuronal nitric oxide synthase |
REM | Rapid eye movement |
SWA | Slow wave activity |
tDCS | Transcranial electrical stimulation |
References
- Bellesi, M.; de Vivo, L.; Chini, M.; Gilli, F.; Tononi, G.; Cirelli, C. Sleep loss promotes astrocytic phagocytosis and microglial activation in mouse cerebral cortex. J. Neurosci. 2017, 37, 5263–5273. [Google Scholar] [CrossRef]
- Mullington, J.M.; Simpson, N.S.; Meier-Ewert, H.K.; Haack, M. Sleep loss and inflammation. Best Pract. Res. Clin. Endocrinol. Metab. 2010, 24, 775–784. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hurtado-Alvarado, G.; Pavón, L.; Castillo-García, S.A.; Hernández, M.E.; Domínguez-Salazar, E.; Velázquez-Moctezuma, J.; Gómez-González, B. Sleep loss as a factor to induce cellular and molecular inflammatory variations. Clin. Dev. Immunol. 2013, 2013. [Google Scholar] [CrossRef] [PubMed]
- Lahtinen, A.; Puttonen, S.; Vanttola, P.; Viitasalo, K.; Sulkava, S.; Pervjakova, N.; Joensuu, A.; Salo, P.; Toivola, A.; Härmä, M.; et al. A distinctive DNA methylation pattern in insufficient sleep. Sci. Rep. 2019, 9, 1–9. [Google Scholar] [CrossRef] [Green Version]
- He, J.; Hsuchou, H.; He, Y.; Kastin, A.J.; Wang, Y.; Pan, W. Sleep restriction impairs blood–brain barrier function. J. Neurosci. 2014, 34, 14697–14706. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Everson, C.A.; Bergmann, B.M.; Rechtschaffen, A. Sleep deprivation in the rat: III. Total sleep deprivation. Sleep 1989, 12, 13–21. [Google Scholar] [CrossRef]
- Ross, J.J. Neurological findings after prolonged sleep deprivation. Arch. Neurol. 1965, 12, 399–403. [Google Scholar] [CrossRef]
- Papachristou, C.S. Aristotle’s Theory of ‘Sleep and Dreams’ in the light of Modern and Contemporary Experimental Research. Electron. J. Philos. 2014, 17, 1–47. [Google Scholar] [CrossRef] [Green Version]
- Xie, L.; Kang, H.; Xu, Q.; Chen, M.J.; Liao, Y.; Thiyagarajan, M.; O’Donnell, J.; Christensen, D.J.; Nicholson, C.; Iliff, J.J.; et al. Sleep drives metabolite clearance from the adult brain. Science 2013, 342, 373–377. [Google Scholar] [CrossRef] [Green Version]
- Fultz, N.E.; Bonmassar, G.; Setsompop, K.; Stickgold, R.A.; Rosen, B.R.; Polimeni, J.R.; Lewis, L.D. Coupled electrophysiological, hemodynamic, and cerebrospinal fluid oscillations in human sleep. Science 2019, 366, 628–631. [Google Scholar] [CrossRef]
- Lucey, B.P.; McCullough, A.; Landsness, E.C.; Toedebusch, C.D.; McLeland, J.S.; Zaza, A.M.; Fagan, A.M.; McCue, L.; Xiong, C.; Morris, J.C.; et al. Reduced non–rapid eye movement sleep is associated with tau pathology in early Alzheimer’s disease. Sci. Transl. Med. 2019, 11. [Google Scholar] [CrossRef] [PubMed]
- Lutsey, P.L.; Misialek, J.R.; Mosley, T.H.; Gottesman, R.F.; Punjabi, N.M.; Shahar, E.; MacLehose, R.; Ogilvie, R.P.; Knopman, D.; Alonso, A. Sleep characteristics and risk of dementia and Alzheimer’s disease: The atherosclerosis risk in communities study. Alzheimer Dement 2018, 14, 157–166. [Google Scholar] [CrossRef] [PubMed]
- Mendelsohn, A.R.; Larrick, J.W. Sleep facilitates clearance of metabolites from the brain: Glymphatic function in aging and neurodegenerative diseases. Rejuvenation Res. 2013, 16, 518–523. [Google Scholar] [CrossRef] [PubMed]
- Weldemichael, D.A.; Grossberg, G.T. Circadian rhythm disturbances in patients with Alzheimer’s disease: A review. Int. J. Alzheimer Dis. 2010, 2010. [Google Scholar] [CrossRef] [Green Version]
- McCurry, S.M.; Logsdon, R.G.; Teri, L.; Gibbons, L.E.; Kukull, W.A.; Bowen, J.D.; McCormick, W.C.; Larson, E.B. Characteristics of sleep disturbance in community-dwelling Alzheimer’s disease patients. J. Geriatr. Psychiatry Neurol. 1999, 12, 53–59. [Google Scholar] [CrossRef] [PubMed]
- Tworoger, S.S.; Lee, S.; Schernhammer, E.S.; Grodstein, F. The association of self-reported sleep duration, difficulty sleeping, and snoring with cognitive function in older women. Alzheimer Dis. Assoc. Disord. 2006, 20, 41–48. [Google Scholar] [CrossRef]
- Carvalho, D.Z.; Knopman, D.S.; Boeve, B.F.; Lowe, V.J.; Roberts, R.O.; Mielke, M.M.; Przybelski, S.A.; Machulda, M.M.; Petersen, R.C.; Jack, C.R.; et al. Association of excessive daytime sleepiness with longitudinal β-amyloid accumulation in elderly persons without dementia. JAMA Neurol. 2018, 75, 672–680. [Google Scholar] [CrossRef] [Green Version]
- Lucey, B.P.; Bateman, R.J. Amyloid-β diurnal pattern: Possible role of sleep in Alzheimer’s disease pathogenesis. Neurobiol. Aging 2014, 35, S29–S34. [Google Scholar] [CrossRef] [Green Version]
- Carskadon, M.A.; Dement, W.C. Normal human sleep: An overview. Princ. Pract. Sleep Med. 2005, 4, 13–23. [Google Scholar]
- Iber, C. The AASM manual for the scoring of sleep and associated events: Rules. Terminol. Tech. Specif. 2007, 176, 2012. [Google Scholar]
- Borbély, A.A. A two process model of sleep regulation. Hum Neurobiol. 1982, 1, 195–204. [Google Scholar] [PubMed]
- Borb, A.A.; Achermann, P. Sleep homeostasis and models of sleep regulation. J. Biol. Rhythm. 1999, 14, 559–570. [Google Scholar] [CrossRef] [PubMed]
- Lee, Y.F.; Gerashchenko, D.; Timofeev, I.; Bacskai, B.J.; Kastanenka, K.V. Slow Wave Sleep Is a Promising Intervention Target for Alzheimer’s Disease. Front. Neurosci. 2020, 14, 705. [Google Scholar] [CrossRef] [PubMed]
- Hablitz, L.M.; Vinitsky, H.S.; Sun, Q.; Stæger, F.F.; Sigurdsson, B.; Mortensen, K.N.; Lilius, T.O.; Nedergaard, M. Increased glymphatic influx is correlated with high EEG delta power and low heart rate in mice under anesthesia. Sci. Adv. 2019, 5, eaav5447. [Google Scholar] [CrossRef] [Green Version]
- Hauner, K.K.; Howard, J.D.; Zelano, C.; Gottfried, J.A. Stimulus-specific enhancement of fear extinction during slow-wave sleep. Nat. Neurosci. 2013, 16, 1553. [Google Scholar] [CrossRef] [Green Version]
- Keklund, G.; ÅKerstedt, T. Objective components of individual differences in subjective sleep quality. J. Sleep Res. 1997, 6, 217–220. [Google Scholar] [CrossRef]
- Diekelmann, S.; Born, J. The memory function of sleep. Nat. Rev. Neurosci. 2010, 11, 114–126. [Google Scholar] [CrossRef]
- Rasch, B.; Born, J. About sleep’s role in memory. Physiol. Rev. 2013, 93, 681–766. [Google Scholar] [CrossRef]
- Tononi, G.; Cirelli, C. Sleep and the price of plasticity: From synaptic and cellular homeostasis to memory consolidation and integration. Neuron 2014, 81, 12–34. [Google Scholar] [CrossRef] [Green Version]
- Huber, R.; Ghilardi, M.F.; Massimini, M.; Tononi, G. Local sleep and learning. Nature 2004, 430, 78–81. [Google Scholar] [CrossRef]
- ÅKerstedt, T.; Hume, K.; Minors, D.; Waterhouse, J. Good sleep—Its timing and physiological sleep characteristics. J. Sleep Res. 1997, 6, 221–229. [Google Scholar] [CrossRef] [PubMed]
- Hoch, C.C.; Reynolds, C.F., III; Kupfer, D.J.; Berman, S.R.; Houck, P.R.; Stack, J.A. Empirical note: Self-report versus recorded sleep in healthy seniors. Psychophysiology 1987, 24, 293–299. [Google Scholar] [CrossRef] [PubMed]
- Kryger, M.; Steljes, D.; Pouliot, Z.; Neufeld, H.; Odynski, T. Subjective versus objective evaluation of hypnotic efficacy: Experience with zolpidem. Sleep 1991, 14, 399–407. [Google Scholar] [CrossRef] [PubMed]
- Holth, J.K.; Mahan, T.E.; Robinson, G.O.; Rocha, A.; Holtzman, D.M. Altered sleep and EEG power in the P301S Tau transgenic mouse model. Ann. Clin. Transl. Neurol. 2017, 4, 180–190. [Google Scholar] [CrossRef] [PubMed]
- Kastanenka, K.V.; Hou, S.S.; Shakerdge, N.; Logan, R.; Feng, D.; Wegmann, S.; Chopra, V.; Hawkes, J.M.; Chen, X.; Bacskai, B.J. Optogenetic restoration of disrupted slow oscillations halts amyloid deposition and restores calcium homeostasis in an animal model of Alzheimer’s disease. PLoS ONE 2017, 12, e0170275. [Google Scholar] [CrossRef]
- Kastanenka, K.V.; Calvo-Rodriguez, M.; Hou, S.S.; Zhou, H.; Takeda, S.; Arbel-Ornath, M.; Lariviere, A.; Lee, Y.F.; Kim, A.; Hawkes, J.M.; et al. Frequency-dependent exacerbation of Alzheimer’s disease neuropathophysiology. Sci. Rep. 2019, 9, 1–13. [Google Scholar] [CrossRef] [Green Version]
- Kent, B.A.; Strittmatter, S.M.; Nygaard, H.B. Sleep and EEG power spectral analysis in three transgenic mouse models of Alzheimer’s disease: APP/PS1, 3xTgAD, and Tg2576. J. Alzheimer Dis. 2018, 64, 1325–1336. [Google Scholar] [CrossRef]
- Castano-Prat, P.; Perez-Mendez, L.; Perez-Zabalza, M.; Sanfeliu, C.; Giménez-Llort, L.; Sanchez-Vives, M.V. Altered slow (<1 Hz) and fast (beta and gamma) neocortical oscillations in the 3xTg-AD mouse model of Alzheimer’s disease under anesthesia. Neurobiol. Aging 2019, 79, 142–151. [Google Scholar]
- Mander, B.A.; Rao, V.; Lu, B.; Saletin, J.M.; Lindquist, J.R.; Ancoli-Israel, S.; Jagust, W.; Walker, M.P. Prefrontal atrophy, disrupted NREM slow waves and impaired hippocampal-dependent memory in aging. Nat. Neurosci. 2013, 16, 357. [Google Scholar] [CrossRef]
- Mander, B.A.; Marks, S.M.; Vogel, J.W.; Rao, V.; Lu, B.; Saletin, J.M.; Ancoli-Israel, S.; Jagust, W.J.; Walker, M.P. β-amyloid disrupts human NREM slow waves and related hippocampus-dependent memory consolidation. Nat. Neurosci. 2015, 18, 1051–1057. [Google Scholar] [CrossRef] [Green Version]
- Westerberg, C.E.; Mander, B.A.; Florczak, S.M.; Weintraub, S.; Mesulam, M.M.; Zee, P.C.; Paller, K.A. Concurrent impairments in sleep and memory in amnestic mild cognitive impairment. J. Int. Neuropsychol. Soc. JINS 2012, 18, 490. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Winer, J.R.; Mander, B.A.; Helfrich, R.F.; Maass, A.; Harrison, T.M.; Baker, S.L.; Knight, R.T.; Jagust, W.J.; Walker, M.P. Sleep as a potential biomarker of tau and β-amyloid burden in the human brain. J. Neurosci. 2019, 39, 6315–6324. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Mestre, H.; Kostrikov, S.; Mehta, R.I.; Nedergaard, M. Perivascular spaces, glymphatic dysfunction, and small vessel disease. Clin. Sci. 2017, 131, 2257–2274. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Iliff, J.J.; Wang, M.; Liao, Y.; Plogg, B.A.; Peng, W.; Gundersen, G.A.; Benveniste, H.; Vates, G.E.; Deane, R.; Goldman, S.A.; et al. A paravascular pathway facilitates CSF flow through the brain parenchyma and the clearance of interstitial solutes, including amyloid β. Sci. Transl. Med. 2012, 4, 147ra111. [Google Scholar] [CrossRef] [Green Version]
- Iliff, J.J.; Chen, M.J.; Plog, B.A.; Zeppenfeld, D.M.; Soltero, M.; Yang, L.; Singh, I.; Deane, R.; Nedergaard, M. Impairment of glymphatic pathway function promotes tau pathology after traumatic brain injury. J. Neurosci. 2014, 34, 16180–16193. [Google Scholar] [CrossRef] [Green Version]
- Achariyar, T.M.; Li, B.; Peng, W.; Verghese, P.B.; Shi, Y.; McConnell, E.; Benraiss, A.; Kasper, T.; Song, W.; Takano, T.; et al. Glymphatic distribution of CSF-derived apoE into brain is isoform specific and suppressed during sleep deprivation. Mol. Neurodegener. 2016, 11, 1–20. [Google Scholar] [CrossRef] [Green Version]
- Hipólide, D.C.; Moreira, K.M.; Barlow, K.B.; Wilson, A.A.; Nobrega, J.N.; Tufik, S. Distinct effects of sleep deprivation on binding to norepinephrine and serotonin transporters in rat brain. Prog. Neuro-Psychopharmacol. Biol. Psychiatry 2005, 29, 297–303. [Google Scholar] [CrossRef]
- Irwin, M.; Thompson, J.; Miller, C.; Gillin, J.C.; Ziegler, M. Effects of sleep and sleep deprivation on catecholamine and interleukin-2 levels in humans: Clinical implications. J. Clin. Endocrinol. Metab. 1999, 84, 1979–1985. [Google Scholar] [CrossRef]
- Kato, M.; Phillips, B.G.; Sigurdsson, G.; Narkiewicz, K.; Pesek, C.A.; Somers, V.K. Effects of sleep deprivation on neural circulatory control. Hypertension 2000, 35, 1173–1175. [Google Scholar] [CrossRef] [Green Version]
- O’Donnell, J.; Zeppenfeld, D.; McConnell, E.; Pena, S.; Nedergaard, M. Norepinephrine: A neuromodulator that boosts the function of multiple cell types to optimize CNS performance. Neurochem. Res. 2012, 37, 2496–2512. [Google Scholar] [CrossRef] [Green Version]
- Cipolla, M.J.; Li, R.; Vitullo, L. Perivascular innervation of penetrating brain parenchymal arterioles. J. Cardiovasc. Pharmacol. 2004, 44, 1–8. [Google Scholar] [CrossRef] [PubMed]
- Lee, H.; Xie, L.; Yu, M.; Kang, H.; Feng, T.; Deane, R.; Logan, J.; Nedergaard, M.; Benveniste, H. The effect of body posture on brain glymphatic transport. J. Neurosci. 2015, 35, 11034–11044. [Google Scholar] [CrossRef] [PubMed]
- Selkoe, D.J. Early network dysfunction in Alzheimer’s disease. Science 2019, 365, 540–541. [Google Scholar] [CrossRef] [PubMed]
- Busche, M.A.; Eichhoff, G.; Adelsberger, H.; Abramowski, D.; Wiederhold, K.H.; Haass, C.; Staufenbiel, M.; Konnerth, A.; Garaschuk, O. Clusters of hyperactive neurons near amyloid plaques in a mouse model of Alzheimer’s disease. Science 2008, 321, 1686–1689. [Google Scholar] [CrossRef] [Green Version]
- Cirrito, J.R.; Yamada, K.A.; Finn, M.B.; Sloviter, R.S.; Bales, K.R.; May, P.C.; Schoepp, D.D.; Paul, S.M.; Mennerick, S.; Holtzman, D.M. Synaptic activity regulates interstitial fluid amyloid-β levels in vivo. Neuron 2005, 48, 913–922. [Google Scholar] [CrossRef] [Green Version]
- Cirrito, J.R.; Kang, J.E.; Lee, J.; Stewart, F.R.; Verges, D.K.; Silverio, L.M.; Bu, G.; Mennerick, S.; Holtzman, D.M. Endocytosis is required for synaptic activity-dependent release of amyloid-β in vivo. Neuron 2008, 58, 42–51. [Google Scholar] [CrossRef] [Green Version]
- Yamamoto, K.; Tanei, Z.i.; Hashimoto, T.; Wakabayashi, T.; Okuno, H.; Naka, Y.; Yizhar, O.; Fenno, L.E.; Fukayama, M.; Bito, H.; et al. Chronic optogenetic activation augments Aβ pathology in a mouse model of Alzheimer disease. Cell Rep. 2015, 11, 859–865. [Google Scholar] [CrossRef] [Green Version]
- Wu, J.W.; Hussaini, S.A.; Bastille, I.M.; Rodriguez, G.A.; Mrejeru, A.; Rilett, K.; Sanders, D.W.; Cook, C.; Fu, H.; Boonen, R.A.; et al. Neuronal activity enhances tau propagation and tau pathology in vivo. Nat. Neurosci. 2016, 19, 1085–1092. [Google Scholar] [CrossRef]
- Araque, A.; Parpura, V.; Sanzgiri, R.P.; Haydon, P.G. Tripartite synapses: Glia, the unacknowledged partner. Trends Neurosci. 1999, 22, 208–215. [Google Scholar] [CrossRef]
- Newman, E.A. New roles for astrocytes: Regulation of synaptic transmission. Trends Neurosci. 2003, 26, 536–542. [Google Scholar] [CrossRef]
- Galea, E.; Morrison, W.; Hudry, E.; Arbel-Ornath, M.; Bacskai, B.J.; Gómez-Isla, T.; Stanley, H.E.; Hyman, B.T. Topological analyses in APP/PS1 mice reveal that astrocytes do not migrate to amyloid-β plaques. Proc. Natl. Acad. Sci. USA 2015, 112, 15556–15561. [Google Scholar] [CrossRef] [Green Version]
- Kuchibhotla, K.V.; Lattarulo, C.R.; Hyman, B.T.; Bacskai, B.J. Synchronous hyperactivity and intercellular calcium waves in astrocytes in Alzheimer mice. Science 2009, 323, 1211–1215. [Google Scholar] [CrossRef] [Green Version]
- Robinson, S.R. Neuronal expression of glutamine synthetase in Alzheimer’s disease indicates a profound impairment of metabolic interactions with astrocytes. Neurochem. Int. 2000, 36, 471–482. [Google Scholar] [CrossRef]
- Szabó, Z.; Héja, L.; Szalay, G.; Kékesi, O.; Füredi, A.; Szebényi, K.; Dobolyi, Á.; Orbán, T.I.; Kolacsek, O.; Tompa, T.; et al. Extensive astrocyte synchronization advances neuronal coupling in slow wave activity in vivo. Sci. Rep. 2017, 7, 1–18. [Google Scholar] [CrossRef] [PubMed]
- Poskanzer, K.E.; Yuste, R. Astrocytic regulation of cortical UP states. Proc. Natl. Acad. Sci. USA 2011, 108, 18453–18458. [Google Scholar] [CrossRef] [Green Version]
- Poskanzer, K.E.; Yuste, R. Astrocytes regulate cortical state switching in vivo. Proc. Natl. Acad. Sci. USA 2016, 113, E2675–E2684. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Pandey, P.K.; Sharma, A.K.; Gupta, U. Blood brain barrier: An overview on strategies in drug delivery, realistic in vitro modeling and in vivo live tracking. Tissue Barriers 2016, 4, e1129476. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Semyachkina-Glushkovskaya, O.; Abdurashitov, A.; Dubrovsky, A.; Bragin, D.; Bragina, O.; Shushunova, N.; Maslyakova, G.; Navolokin, N.; Bucharskaya, A.; Tuchind, V.; et al. Application of optical coherence tomography for in vivo monitoring of the meningeal lymphatic vessels during opening of blood–brain barrier: Mechanisms of brain clearing. J. Biomed. Opt. 2017, 22, 121719. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Semyachkina-Glushkovskaya, O.; Chehonin, V.; Borisova, E.; Fedosov, I.; Namykin, A.; Abdurashitov, A.; Shirokov, A.; Khlebtsov, B.; Lyubun, Y.; Navolokin, N.; et al. Photodynamic opening of the blood-brain barrier and pathways of brain clearing. J. Biophotonics 2018, 11, e201700287. [Google Scholar] [CrossRef] [PubMed]
- Lipsman, N.; Meng, Y.; Bethune, A.J.; Huang, Y.; Lam, B.; Masellis, M.; Herrmann, N.; Heyn, C.; Aubert, I.; Boutet, A.; et al. Blood–brain barrier opening in Alzheimer’s disease using MR-guided focused ultrasound. Nat. Commun. 2018, 9, 1–8. [Google Scholar] [CrossRef] [Green Version]
- Jordão, J.F.; Thévenot, E.; Markham-Coultes, K.; Scarcelli, T.; Weng, Y.Q.; Xhima, K.; O’Reilly, M.; Huang, Y.; McLaurin, J.; Hynynen, K.; et al. Amyloid-β plaque reduction, endogenous antibody delivery and glial activation by brain-targeted, transcranial focused ultrasound. Exp. Neurol. 2013, 248, 16–29. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Leinenga, G.; Götz, J. Scanning ultrasound removes amyloid-β and restores memory in an Alzheimer’s disease mouse model. Sci. Transl. Med. 2015, 7, 278ra33. [Google Scholar] [CrossRef] [Green Version]
- Burgess, A.; Dubey, S.; Yeung, S.; Hough, O.; Eterman, N.; Aubert, I.; Hynynen, K. Alzheimer disease in a mouse model: MR imaging–guided focused ultrasound targeted to the hippocampus opens the blood-brain barrier and improves pathologic abnormalities and behavior. Radiology 2014, 273, 736–745. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kiviniemi, V.; Korhonen, V.; Kortelainen, J.; Rytky, S.; Keinänen, T.; Tuovinen, T.; Isokangas, M.; Sonkajärvi, E.; Siniluoto, T.; Nikkinen, J.; et al. Real-time monitoring of human blood-brain barrier disruption. PLoS ONE 2017, 12, e0174072. [Google Scholar] [CrossRef]
- Pavlov, A.; Dubrovsky, A.; Koronovskii, A., Jr.; Pavlova, O.; Semyachkina-Glushkovskaya, O.; Kurths, J. Extended detrended fluctuation analysis of sound-induced changes in brain electrical activity. Chaos Solitons Fractals 2020, 139, 109989. [Google Scholar] [CrossRef]
- Pavlov, A.; Dubrovsky, A.; Koronovskii, A., Jr.; Pavlova, O.; Semyachkina-Glushkovskaya, O.; Kurths, J. Extended detrended fluctuation analysis of electroencephalograms signals during sleep and the opening of the blood–brain barrier. Chaos Interdiscip. J. Nonlinear Sci. 2020, 30, 073138. [Google Scholar] [CrossRef]
- Shuvaev, A.; Kuvacheva, N.; Morgun, A.; Khilazheva, E.; Salmina, A. The Role of Ion Channels Expressed in Cerebral Endothelial Cells in the Functional Integrity of the Blood-Brain Barrier (Review). Sovrem. Tehnol. V Med. 2016, 8, 241–250. [Google Scholar] [CrossRef]
- Callies, C.; Fels, J.; Liashkovich, I.; Kliche, K.; Jeggle, P.; Kusche-Vihrog, K.; Oberleithner, H. Membrane potential depolarization decreases the stiffness of vascular endothelial cells. J. Cell Sci. 2011, 124, 1936–1942. [Google Scholar] [CrossRef] [Green Version]
- Vanhatalo, S.; Voipio, J.; Kaila, K. Infraslow EEG activity. In Niedermeyer’s Electroencephalography: Basic Principles, Clinical Applications, and Related Fields; Wolters Kluwer/Lippincott Williams & Wilkins: Philadelphia, PA, USA, 2011; pp. 741–747. [Google Scholar]
- Woody, C.; Marshall, W.; Besson, J.; Thompson, H.; Aleonard, P.; Albe-Fessard, D. Brain potential shift with respiratory acidosis in the cat and monkey. Am. J. Physiol. Leg. Content 1970, 218, 275–283. [Google Scholar] [CrossRef]
- Revest, P.A.; Jones, H.C.; Abbott, N.J. The transendothelial DC potential of rat blood-brain barrier vessels in situ. In Frontiers in Cerebral Vascular Biology; Springer: Berlin/Heidelberg, Germany, 1993; pp. 71–74. [Google Scholar]
- Revest, P.A.; Jones, H.C.; Abbott, N.J. Transendothelial electrical potential across pial vessels in anaesthetised rats: A study of ion permeability and transport at the blood-brain barrier. Brain Res. 1994, 652, 76–82. [Google Scholar] [CrossRef]
- Monto, S.; Palva, S.; Voipio, J.; Palva, J.M. Very slow EEG fluctuations predict the dynamics of stimulus detection and oscillation amplitudes in humans. J. Neurosci. 2008, 28, 8268–8272. [Google Scholar] [CrossRef] [PubMed]
- Hiltunen, T.; Kantola, J.; Abou Elseoud, A.; Lepola, P.; Suominen, K.; Starck, T.; Nikkinen, J.; Remes, J.; Tervonen, O.; Palva, S.; et al. Infra-slow EEG fluctuations are correlated with resting-state network dynamics in fMRI. J. Neurosci. 2014, 34, 356–362. [Google Scholar] [CrossRef] [PubMed]
- Brockett, A.T.; Kane, G.A.; Monari, P.K.; Briones, B.A.; Vigneron, P.A.; Barber, G.A.; Bermudez, A.; Dieffenbach, U.; Kloth, A.D.; Buschman, T.J.; et al. Evidence supporting a role for astrocytes in the regulation of cognitive flexibility and neuronal oscillations through the Ca2+ binding protein S100β. PLoS ONE 2018, 13, e0195726. [Google Scholar] [CrossRef] [PubMed]
- Bellot-Saez, A.; Cohen, G.; van Schaik, A.; Ooi, L.; Morley, J.W.; Buskila, Y. Astrocytic modulation of cortical oscillations. Sci. Rep. 2018, 8, 1–13. [Google Scholar] [CrossRef] [Green Version]
- Henneberger, C.; Papouin, T.; Oliet, S.H.; Rusakov, D.A. Long-term potentiation depends on release of D-serine from astrocytes. Nature 2010, 463, 232–236. [Google Scholar] [CrossRef]
- Takata, N.; Mishima, T.; Hisatsune, C.; Nagai, T.; Ebisui, E.; Mikoshiba, K.; Hirase, H. Astrocyte calcium signaling transforms cholinergic modulation to cortical plasticity in vivo. J. Neurosci. 2011, 31, 18155–18165. [Google Scholar] [CrossRef]
- Bellesi, M.; de Vivo, L.; Tononi, G.; Cirelli, C. Effects of sleep and wake on astrocytes: Clues from molecular and ultrastructural studies. BMC Biol. 2015, 13, 66. [Google Scholar] [CrossRef] [Green Version]
- Chang, J.; Wang, R.; Li, C.; Wang, Y.; Chu, X.P. Transcranial Low-Level Laser Therapy for Depression and Alzheimer’s Disease. Neuropsychiatry 2018, 8, 477–483. [Google Scholar] [CrossRef] [Green Version]
- Ding, F.; O’Donnell, J.; Xu, Q.; Kang, N.; Goldman, N.; Nedergaard, M. Changes in the composition of brain interstitial ions control the sleep-wake cycle. Science 2016, 352, 550–555. [Google Scholar] [CrossRef] [Green Version]
- Pasantes-Morales, H.; Tuz, K. Volume changes in neurons: Hyperexcitability and neuronal death. In Mechanisms and Significance of Cell Volume Regulation; Karger Publishers: Berlin, Germany, 2006; Volume 152, pp. 221–240. [Google Scholar]
- Hübel, N.; Ullah, G. Anions govern cell volume: A case study of relative astrocytic and neuronal swelling in spreading depolarization. PLoS ONE 2016, 11, e0147060. [Google Scholar] [CrossRef] [Green Version]
- Florence, C.M.; Baillie, L.D.; Mulligan, S.J. Dynamic volume changes in astrocytes are an intrinsic phenomenon mediated by bicarbonate ion flux. PLoS ONE 2012, 7, e51124. [Google Scholar] [CrossRef] [PubMed]
- Fellin, T.; Ellenbogen, J.M.; De Pittà, M.; Ben-Jacob, E.; Halassa, M.M. Astrocyte regulation of sleep circuits: Experimental and modeling perspectives. Front. Comput. Neurosci. 2012, 6, 65. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Halassa, M.M.; Florian, C.; Fellin, T.; Munoz, J.R.; Lee, S.Y.; Abel, T.; Haydon, P.G.; Frank, M.G. Astrocytic modulation of sleep homeostasis and cognitive consequences of sleep loss. Neuron 2009, 61, 213–219. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Krueger, M.; Härtig, W.; Reichenbach, A.; Bechmann, I.; Michalski, D. Blood-brain barrier breakdown after embolic stroke in rats occurs without ultrastructural evidence for disrupting tight junctions. PLoS ONE 2013, 8, e56419. [Google Scholar] [CrossRef] [Green Version]
- Zhang, W.; Zhu, L.; An, C.; Wang, R.; Yang, L.; Yu, W.; Li, P.; Gao, Y. The blood brain barrier in cerebral ischemic injury–Disruption and repair. Brain Hemorrhages 2020, 1, 34–53. [Google Scholar] [CrossRef]
- Dunkel, P.; Chai, C.L.; Sperlagh, B.; Huleatt, P.B.; Matyus, P. Clinical utility of neuroprotective agents in neurodegenerative diseases: Current status of drug development for Alzheimer’s, Parkinson’s and Huntington’s diseases, and amyotrophic lateral sclerosis. Expert Opin. Investig. Drugs 2012, 21, 1267–1308. [Google Scholar] [CrossRef]
- Yiannopoulou, K.G.; Papageorgiou, S.G. Current and future treatments for Alzheimer’s disease. Ther. Adv. Neurol. Disord. 2013, 6, 19–33. [Google Scholar] [CrossRef] [Green Version]
- Cummings, J.L.; Tong, G.; Ballard, C. Treatment combinations for Alzheimer’s disease: Current and future pharmacotherapy options. J. Alzheimer Dis. 2019, 67, 779–794. [Google Scholar] [CrossRef] [Green Version]
- Van Dyck, C.H. Anti-amyloid-β monoclonal antibodies for Alzheimer’s disease: Pitfalls and promise. Biol. Psychiatry 2018, 83, 311–319. [Google Scholar] [CrossRef] [Green Version]
- Zhang, Y.; Gruber, R. Focus: Attention Science: Can Slow-Wave Sleep Enhancement Improve Memory? A Review of Current Approaches and Cognitive Outcomes. Yale J. Biol. Med. 2019, 92, 63. [Google Scholar]
- Garcia-Molina, G.; Tsoneva, T.; Jasko, J.; Steele, B.; Aquino, A.; Baher, K.; Pastoor, S.; Pfundtner, S.; Ostrowski, L.; Miller, B.; et al. Closed-loop system to enhance slow-wave activity. J. Neural Eng. 2018, 15, 066018. [Google Scholar] [CrossRef] [PubMed]
- Bellesi, M.; Riedner, B.A.; Garcia-Molina, G.N.; Cirelli, C.; Tononi, G. Enhancement of sleep slow waves: Underlying mechanisms and practical consequences. Front. Syst. Neurosci. 2014, 8, 208. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Tononi, G.; Riedner, B.; Hulse, B.; Ferrarelli, F.; Sarasso, S. Enhancing sleep slow waves with natural stimuli. Medicamundi 2010, 54, 73–79. [Google Scholar]
- Ngo, H.V.V.; Martinetz, T.; Born, J.; Mölle, M. Auditory closed-loop stimulation of the sleep slow oscillation enhances memory. Neuron 2013, 78, 545–553. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Papalambros, N.A.; Santostasi, G.; Malkani, R.G.; Braun, R.; Weintraub, S.; Paller, K.A.; Zee, P.C. Acoustic enhancement of sleep slow oscillations and concomitant memory improvement in older adults. Front. Hum. Neurosci. 2017, 11, 109. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Weigenand, A.; Mölle, M.; Werner, F.; Martinetz, T.; Marshall, L. Timing matters: Open-loop stimulation does not improve overnight consolidation of word pairs in humans. Eur. J. Neurosci. 2016, 44, 2357–2368. [Google Scholar] [CrossRef]
- Leminen, M.M.; Virkkala, J.; Saure, E.; Paajanen, T.; Zee, P.C.; Santostasi, G.; Hublin, C.; Müller, K.; Porkka-Heiskanen, T.; Huotilainen, M.; et al. Enhanced memory consolidation via automatic sound stimulation during non-REM sleep. Sleep 2017, 40, zsx003. [Google Scholar] [CrossRef] [Green Version]
- Santostasi, G.; Malkani, R.; Riedner, B.; Bellesi, M.; Tononi, G.; Paller, K.A.; Zee, P.C. Phase-locked loop for precisely timed acoustic stimulation during sleep. J. Neurosci. Methods 2016, 259, 101–114. [Google Scholar] [CrossRef] [Green Version]
- Ong, J.L.; Lo, J.C.; Chee, N.I.; Santostasi, G.; Paller, K.A.; Zee, P.C.; Chee, M.W. Effects of phase-locked acoustic stimulation during a nap on EEG spectra and declarative memory consolidation. Sleep Med. 2016, 20, 88–97. [Google Scholar] [CrossRef] [Green Version]
- Ong, J.L.; Patanaik, A.; Chee, N.I.; Lee, X.K.; Poh, J.H.; Chee, M.W. Auditory stimulation of sleep slow oscillations modulates subsequent memory encoding through altered hippocampal function. Sleep 2018, 41, zsy031. [Google Scholar] [CrossRef] [Green Version]
- Moruzzi, G. The Physiological Properties of the Brain Stem Reticular System; Blackwell: Oxford, UK, 1954. [Google Scholar]
- Berlucchi, G. One or many arousal systems? Reflections on some of Giuseppe Moruzzi’s foresights and insights about the intrinsic regulation of brain activity. Arch. Ital. Biol. 1997, 135, 5–14. [Google Scholar] [PubMed]
- Marshall, L.; Mölle, M.; Hallschmid, M.; Born, J. Transcranial direct current stimulation during sleep improves declarative memory. J. Neurosci. 2004, 24, 9985–9992. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Marshall, L.; Helgadóttir, H.; Mölle, M.; Born, J. Boosting slow oscillations during sleep potentiates memory. Nature 2006, 444, 610–613. [Google Scholar] [CrossRef] [PubMed]
- Dorokhov, V.B.; Taranov, A.I.; Narbut, A.M.; Sakharov, D.S.; Gruzdeva, S.S.; Tkachenko, O.N.; Arsen’ev, G.N.; Blochin, I.S.; Putilov, A.A. Effects of Exposure to a Weak Extremely Low Frequency Electromagnetic Field on Daytime Sleep Architecture and Length. Sleep Med. Res. 2019, 10, 97–102. [Google Scholar] [CrossRef] [Green Version]
- Eggert, T.; Dorn, H.; Sauter, C.; Nitsche, M.A.; Bajbouj, M.; Danker-Hopfe, H. No effects of slow oscillatory transcranial direct current stimulation (tDCS) on sleep-dependent memory consolidation in healthy elderly subjects. Brain Stimul. 2013, 6, 938–945. [Google Scholar] [CrossRef]
- Reato, D.; Gasca, F.; Datta, A.; Bikson, M.; Marshall, L.; Parra, L.C. Transcranial electrical stimulation accelerates human sleep homeostasis. PLoS Comput. Biol. 2013, 9, e1002898. [Google Scholar] [CrossRef]
- Massimini, M.; Ferrarelli, F.; Esser, S.K.; Riedner, B.A.; Huber, R.; Murphy, M.; Peterson, M.J.; Tononi, G. Triggering sleep slow waves by transcranial magnetic stimulation. Proc. Natl. Acad. Sci. USA 2007, 104, 8496–8501. [Google Scholar] [CrossRef] [Green Version]
- Lang, N.; Siebner, H.R.; Ward, N.S.; Lee, L.; Nitsche, M.A.; Paulus, W.; Rothwell, J.C.; Lemon, R.N.; Frackowiak, R.S. How does transcranial DC stimulation of the primary motor cortex alter regional neuronal activity in the human brain? Eur. J. Neurosci. 2005, 22, 495–504. [Google Scholar] [CrossRef]
- Walsh, J.K.; Randazzo, A.C.; Stone, K.; Eisenstein, R.; Feren, S.D.; Kajy, S.; Dickey, P.; Roehrs, T.; Roth, T.; Schweitzer, P.K. Tiagabine is associated with sustained attention during sleep restriction: Evidence for the value of slow-wave sleep enhancement? Sleep 2006, 29, 433. [Google Scholar]
- Feld, G.B.; Wilhelm, I.; Ma, Y.; Groch, S.; Binkofski, F.; Mölle, M.; Born, J. Slow wave sleep induced by GABA agonist tiagabine fails to benefit memory consolidation. Sleep 2013, 36, 1317–1326. [Google Scholar] [CrossRef]
- Walsh, J.K.; Snyder, E.; Hall, J.; Randazzo, A.C.; Griffin, K.; Groeger, J.; Eisenstein, R.; Feren, S.D.; Dickey, P.; Schweitzer, P.K. Slow wave sleep enhancement with gaboxadol reduces daytime sleepiness during sleep restriction. Sleep 2008, 31, 659–672. [Google Scholar] [CrossRef] [PubMed]
- Hall, J.M. Memory Encoding and Sleep-Dependent Consolidation during Sleep Restriction with and without Pharmacologically Enhanced Slow Wave Sleep. Ph.D. Thesis, Saint Louis University, St. Louis, MO, USA, 2009. [Google Scholar]
- Walsh, J.K.; Hall-Porter, J.M.; Griffin, K.S.; Dodson, E.R.; Forst, E.H.; Curry, D.T.; Eisenstein, R.D.; Schweitzer, P.K. Enhancing slow wave sleep with sodium oxybate reduces the behavioral and physiological impact of sleep loss. Sleep 2010, 33, 1217–1225. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Vienne, J.; Lecciso, G.; Constantinescu, I.; Schwartz, S.; Franken, P.; Heinzer, R.; Tafti, M. Differential effects of sodium oxybate and baclofen on EEG, sleep, neurobehavioral performance, and memory. Sleep 2012, 35, 1071–1084. [Google Scholar] [CrossRef] [PubMed]
- Göder, R.; Fritzer, G.; Gottwald, B.; Lippmann, B.; Seeck-Hirschner, M.; Serafin, I.; Aldenhoff, J. Effects of olanzapine on slow wave sleep, sleep spindles and sleep-related memory consolidation in schizophrenia. Pharmacopsychiatry 2008, 41, 92–99. [Google Scholar] [CrossRef]
- Lazowski, L.K.; Townsend, B.; Hawken, E.R.; Jokic, R.; du Toit, R.; Milev, R. Sleep architecture and cognitive changes in olanzapine-treated patients with depression: A double blind randomized placebo controlled trial. BMC Psychiatry 2014, 14, 202. [Google Scholar] [CrossRef] [Green Version]
- Benedict, C.; Scheller, J.; Rose-John, S.; Born, J.; Marshall, L. Enhancing influence of intranasal interleukin-6 on slow-wave activity and memory consolidation during sleep. FASEB J. 2009, 23, 3629–3636. [Google Scholar] [CrossRef]
- Gottesmann, C. GABA mechanisms and sleep. Neuroscience 2002, 111, 231–239. [Google Scholar] [CrossRef]
- Sharpley, A.L.; Vassallo, C.M.; Cowen, P.J. Olanzapine increases slow-wave sleep: Evidence for blockade of central 5-HT2C receptors in vivo. Biol. Psychiatry 2000, 47, 468–470. [Google Scholar] [CrossRef]
- Harvey, N.L. The link between lymphatic function and adipose biology. Ann. N. Y. Acad. Sci. 2008, 1131, 82–88. [Google Scholar] [CrossRef] [Green Version]
- Mathias, S.; Wetter, T.C.; Steiger, A.; Lancel, M. The GABA uptake inhibitor tiagabine promotes slow wave sleep in normal elderly subjects. Neurobiol. Aging 2001, 22, 247–253. [Google Scholar] [CrossRef]
- Lancel, M.; Wetter, T.C.; Steiger, A.; Mathias, S. Effect of the GABAA agonist gaboxadol on nocturnal sleep and hormone secretion in healthy elderly subjects. Am. J. Physiol. Endocrinol. Metab. 2001, 281, E130–E137. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lapierre, O.; Montpiaisir, J.; Lamarre, M.; Bedard, M. The effect of gamma-hydroxybutyrate on nocturnal and diurnal sleep of normal subjects: Further considerations on REM sleep-triggering mechanisms. Sleep 1990, 13, 24–30. [Google Scholar] [CrossRef] [PubMed]
- Spath-Schwalbe, E.; Hansen, K.; Schmidt, F.; Schrezenmeier, H.; Marshall, L.; Burger, K.; Fehm, H.L.; Born, J. Acute effects of recombinant human interleukin-6 on endocrine and central nervous sleep functions in healthy men. J. Clin. Endocrinol. Metab. 1998, 83, 1573–1579. [Google Scholar] [CrossRef] [PubMed]
- Benveniste, H.; Lee, H.; Ding, F.; Sun, Q.; Al-Bizri, E.; Makaryus, R.; Probst, S.; Nedergaard, M.; Stein, E.A.; Lu, H. Anesthesia with dexmedetomidine and low-dose isoflurane increases solute transport via the glymphatic pathway in rat brain when compared with high-dose isoflurane. Anesthesiol. J. Am. Soc. Anesthesiol. 2017, 127, 976–988. [Google Scholar] [CrossRef] [PubMed]
- Musizza, B.; Stefanovska, A.; McClintock, P.V.; Paluš, M.; Petrovčič, J.; Ribarič, S.; Bajrović, F.F. Interactions between cardiac, respiratory and EEG-δ oscillations in rats during anaesthesia. J. Physiol. 2007, 580, 315–326. [Google Scholar] [CrossRef] [PubMed]
- Gerashchenko, D.; Wisor, J.P.; Burns, D.; Reh, R.K.; Shiromani, P.J.; Sakurai, T.; Horacio, O.; Kilduff, T.S. Identification of a population of sleep-active cerebral cortex neurons. Proc. Natl. Acad. Sci. USA 2008, 105, 10227–10232. [Google Scholar] [CrossRef] [Green Version]
- Gerashchenko, D.; Schmidt, M.A.; Zielinski, M.R.; Moore, M.E.; Wisor, J.P. Sleep state dependence of optogenetically evoked responses in neuronal nitric oxide synthase-positive cells of the cerebral cortex. Neuroscience 2018, 379, 189–201. [Google Scholar] [CrossRef]
© 2020 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Semyachkina-Glushkovskaya, O.; Postnov, D.; Penzel, T.; Kurths, J. Sleep as a Novel Biomarker and a Promising Therapeutic Target for Cerebral Small Vessel Disease: A Review Focusing on Alzheimer’s Disease and the Blood-Brain Barrier. Int. J. Mol. Sci. 2020, 21, 6293. https://doi.org/10.3390/ijms21176293
Semyachkina-Glushkovskaya O, Postnov D, Penzel T, Kurths J. Sleep as a Novel Biomarker and a Promising Therapeutic Target for Cerebral Small Vessel Disease: A Review Focusing on Alzheimer’s Disease and the Blood-Brain Barrier. International Journal of Molecular Sciences. 2020; 21(17):6293. https://doi.org/10.3390/ijms21176293
Chicago/Turabian StyleSemyachkina-Glushkovskaya, Oxana, Dmitry Postnov, Thomas Penzel, and Jürgen Kurths. 2020. "Sleep as a Novel Biomarker and a Promising Therapeutic Target for Cerebral Small Vessel Disease: A Review Focusing on Alzheimer’s Disease and the Blood-Brain Barrier" International Journal of Molecular Sciences 21, no. 17: 6293. https://doi.org/10.3390/ijms21176293
APA StyleSemyachkina-Glushkovskaya, O., Postnov, D., Penzel, T., & Kurths, J. (2020). Sleep as a Novel Biomarker and a Promising Therapeutic Target for Cerebral Small Vessel Disease: A Review Focusing on Alzheimer’s Disease and the Blood-Brain Barrier. International Journal of Molecular Sciences, 21(17), 6293. https://doi.org/10.3390/ijms21176293