The Function of Sleep: Maintaining the Integrity of Brain Protection and Cleaning Systems
Abstract
Sleep is a vital function for organisms. Pioneering studies carried out in the 1980s showed that sleep is essential to guarantee the survival of the species. Since then, numerous experiments have been carried out to elucidate the function of sleep; Despite the accumulation of evidence, a widely accepted consensus has not been generated in this regard. Our group has proposed that the function of sleep is to maintain reciprocal interactions between systems that maintain homeostasis, the nervous, endocrine and immune systems. In the particular case of the nervous system, the systems responsible for maintaining homeostasis are the blood-brain barrier and the lymphatic system. The blood-brain barrier is located at the level of the brain capillaries, is made up of brain endothelial cells. The barrier phenotype of brain endothelial cells depends on cell-cell interactions with pericytes and on soluble factors released by astroglia. The lymph system promotes the exchange of solutes between the interstitial fluid of the brain and the cerebrospinal fluid at the level of the perivascular spaces. In the last decade, it has been described that both systems present changes in their physiology in response to variations in local synaptic activity; In particular, it has been described that the great changes in brain electrical activity associated with the sleep / wake cycle modify the functioning of both systems. In the case of the lymphatic system, it has been described that during slow sleep the rate of solute exchange from interstitial fluid to cerebrospinal fluid increases. While in the case of the blood-brain barrier, a reduction in the expression of occludent binding proteins has been shown, which is reflected in an increase in the permeability to soluble molecules circulating in the blood.
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Biswas, S., Mishra, P., & Mallick, B.N. (2006) Increased apoptosis in rat brain after rapid eye movement sleep loss. Neuroscience, 142(2), 315-331.
Dash, M. B., Douglas, C. L., Vyazovskiy, V. V., Cirelli, C., & Tononi, G. (2009). Long-Term Homeostasis of Extracellular Glutamate in the Rat Cerebral Cortex across Sleep and Waking States. Journal of Neuroscience, 29(3), 620-629.
DiNuzzo, M., & Nedergaard, M. (2017). Brain energetics during the sleep-wake cycle. CurrentOpinion in Neurobiology, 47, 65-72. https://doi.org/10.1016/j.conb.2017.09.010
Filosa, J. A., & Blanco, V.M. (2007). N eurovascular coupling in the mammalian brain: Neuronal-glial-vascular communication. Experimental Physiology, 92( 4), 641-646.
Gómez-González, B., Domínguez-Salazar, E., Hurtado-Alvarado, G., Esqueda-Leon, E., Santana-Miranda, R., Rojas-Zamorano, J. A., & Velázquez-Moctezuma, J. (2012). Role of sleep in the regulation of the immune system and the pituitary hormones: Sleep, hormones, and cytokines. Annals of the New York Academy of Sciences, 1261(1), 97-106.
Gómez-González, B., Hurtado-Alvarado, G., Esqueda-León, E., Santana-Miranda, R., RojasZamorano, J. Á., & Velázquez-Moctezuma, J. (2013). REM sleep loss and recovery regulates blood-brain barrier function. Current Neurovascular Research, 10(3), 197-207.
Guzman-Marin, R., Suntsova, N., Bashir, T., Nienhuis, R., Szymusiak, R., & McGinty, D. (2008). Rapid eye movement sleep deprivation contributes to reduction of neurogenesis in the hippocampal dentate gyrus of the adult rat. Sleep, 31(2), 167-175.
Hamilton, N. B. (2010). Pericyte-mediated regulation of capillary diameter: a component of neurovascular coupling in health and disease. Frontiers inNeuroenergetics, 2.
He, J., Hsuchou, H., He, Y., Kastin, A. J., Wang, Y., & Pan, W. (2014). Sleep Restriction Impairs Blood-Brain Barrier Function. Journal of Neuroscience, 34(44), 14697-14706.
Hurtado-Alvarado, G., Becerril-Villanueva, E., Contis-Montes de Oca, A., Domínguez-Salazar, E., Salinas-Jazmín, N., Pérez-Tapia, S. M., ... Gómez-González, B. (2018). The yin/yang of inflammatory status: Blood-brain barrier regulation during sleep. Brain, Behavior, and Immunity, 69, 154-166.
Hurtado-Alvarado, G., Velázquez-Moctezuma, J., & Gómez-González, B. (2017). Chronic sleep restriction disrupts interendothelial junctions in the hippocampus and increases blood-brain barrier permeability. Journal of Microscopy, 268(1 ), 28-38.
Hurtado-Alvarado, Gabriela, Domínguez Salazar, E., Velázquez-Moctezuma, J., & Gómez-González, B. (2016). A2A Adenosine Receptor Antagonism Reverts the Blood-Brain Barrier Dysfunction lnduced by Sleep Restriction.PLOS ONE, 11(11), e0167236.
Iliff, J. J., Lee, H., Yu, M., Feng, T., Logan, J., Nedergaard, M., & Benveniste, H. (2013). Brain-wide pathway for waste clearance captured by contrast-enhanced MRI. Journal of Clinicallnvestigation, 123(3), 1299-1309.
Jessen, N. A., Munk, A. S. F., Lundgaard, l., & Nedergaard, M. (2015). The Glymphatic System: A Beginner's Guide. Neurochemical Research, 40(12), 2583-2599.
Klingelhofer, J. (2012). Cerebral blood flow velocity in sleep. Perspectives in Medicine, l (1-12), 275-284.
Korth, C. (1995). A co-evolutionary theory of sleep. Medica! Hypotheses, 45, 304
Lehtinen, M. K., Bjomsson, C. S., Dymecki, S. M., Gilbertson, R. J., Holtzman, D. M., & Monuki, E. S. (2013). The Choroid Plexus and Cerebrospinal Fluid: Emerging Roles in Development, Disease, and Therapy. Journal of Neuroscience, 33( 45), 17553-17559.
Leybaert, L., De Bock, M., Van Moorhem, M., Decrock, E., & De Vuyst, E. (2007). Neurobarrier coupling in the brain: Adjusting glucose entry with demand. Journal of NeuroscienceResearch, 85(15), 3213-3220.
Liu, D., He, X., Wu, D., Zhang, Q., Yang, C., Liang, F., ... Xu, G. (2017). Continuous theta burst stimulation facilitates the clearance efficiency of the glymphatic pathway in a mouse model of sleep deprivation. Neuroscience Letters, 653, 189-194.
Mendelsohn, A. R., & Larrick, J. W. (2013). Sleep Facilitates Clearance ofMetabolites from the Brain: Glymphatic Function in Aging and Neurodegenerative Diseases. Rejuvenation Research, 16(6), 518-523.
Mohammed,H. S.,AboulEzz,H. S.,Khadrawy, Y.A., &Noor, N.A. (2011). Neurochemicaland electrophysiological changes induced by
paradoxical sleep deprivation in rats. BehaviouralBrainResearch, 225(1), 39-46.
Nishijima, T., Piriz, J., Duflot, S., Femandez,A. M., Gaitan, G., Gomez-Pinedo, U., ... TorresAleman, l. (2010). Neuronal Activity Orives Localized Blood-Brain-Barrier Transport of Serum Insulin-like Growth Factor-! into the CNS.Neuron, 67(5), 834-846.
Novati, A., Hulshof, H. J., Koolhaas, J. M., Lucassen, P. J., & Meerlo, P. (2011). Chronic sleep restriction causes a decrease in hippocampal volume in adolescent rats, which is not explained by changes in glucocorticoid levels or neurogenesis. Neuroscience, 190, 145-155.
Petzold, G. C., & Murthy, V. N. (2011). Role of Astrocytes in Neurovascular Coupling. Neuron, 71(5), 782-797.
Pollay, M. (2010). Toe function and structure of the cerebrospinal fluid outflow system. Cerebrospinal Fluid Research, 7 ( 1 ), 9. Rechtschaffen, A., Bergmann, B. M., Everson,
C.A., Kushida, C.A., & Gilliland, M.A. (1989). Sleep deprivation in the rat: X. Integration and discussion of the :findings. Sleep, 12(1 ), 68-87.
Reitsma, S., Slaaf, D. W., Vink, H., van Zandvoort, M. A.M. J., & oude Egbrink, M. G. A. (2007). The endothelial glycocalyx: composition, functions, and visualization. Pflügers Archiv - European Journal of Physiology, 454(3), 345-359.
Saper, C. B., Fuller, P.M., Pedersen, N. P., Lu, J., & Scammell, T. E. (2010). Sleep State Switching.Neuron, 68(6), 1023-1042.
Silvani, A., Asti, V., Bojic, T., Ferrari, V., Franzini, C., Lenzi, P., ... Zoccoli, G. (2005). Sleep-Dependent Changes in the Coupling Between Heart Period and Arterial Pressure in Newbom Lambs. Pediatric Research, 57(1 ), 108-114.
Spira, A. P., Gamaldo, A. A., An, Y., Wu, M. N., Simonsick, E. M., Bilgel, M., ... Resnick, S.M. (2013). Self-reported Sleep and ?-Amyloid Deposition in Community-Dwelling Older Adults. JAMANeurology . Stickgold, R. (2005). Sleep-dependent memory consolidation. Nature, 437(7063), 1272-1278.
Wehr, T. A. (1992). A brain-warming function for REM sleep. Neuroscience and Biobehavioral Reviews, 16(3 ), 3 79-3 97.
Xie, L., Kang, H., Xu, Q., Chen, M. J., Liao, Y., Thiyagarajan, M., ... Nedergaard, M. (2013). Sleep Orives Metabolite Clearance from the AdultBrain. Science, 342(6156), 373-377.
