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Sleep and Perivascular Spaces

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Abstract

Purpose of Review

The glymphatic system is hypothesized to act as the brain’s filtration system to remove toxic solutes that accumulate throughout the day. Perivascular spaces (PVSs) play a fundamental role in the ability of the glymphatic system to function, and sleep influences the effectiveness of this system. This article reviews the complexity of the interplay between sleep, the glymphatic system, and PVS.

Recent Findings

New imaging techniques have illuminated the structure of PVS and their associations with differing disease states. Research has shown that sleep may play a key role in the function of PVS and the influence of adenosine, astrocyte, and aquaporin-4 channel in the function of the glymphatic system.

Summary

Emerging data suggest that differing pathological states such as neuroinflammatory conditions, neurodegenerative diseases, and cognitive dysfunction may be associated with underlying glymphatic system dysfunction, and sleep disorders could be a potential intervention target.

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Data Availability

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References

Papers of particular interest, published recently, have been highlighted as: • Of importance •• Of major importance

  1. Loukas M, Bellary SS, Kuklinski M, Ferrauiola J, Yadav A, Shoja MM, et al. The lymphatic system: A historical perspective. Clin Anat. 2011;24:807–16.

    Article  PubMed  Google Scholar 

  2. Pollay M. The function and structure of the cerebrospinal fluid outflow system. Cerebrospinal Fluid Res. 2010;7:9.

    Article  PubMed  PubMed Central  Google Scholar 

  3. Iliff JJ, Wang M, Liao Y, Plogg BA, Peng W, Gundersen GA, 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.

    Article  PubMed  PubMed Central  Google Scholar 

  4. Kwee RM, Kwee TC. Virchow-Robin spaces at MR imaging. Radiographics. 2007;27:1071–86.

    Article  PubMed  Google Scholar 

  5. Wardlaw JM, Benveniste H, Nedergaard M, Zlokovic BV, Mestre H, Lee H, et al. Perivascular spaces in the brain: Anatomy, physiology and pathology. Nat Rev Neurol. 2020;16:137–53.

    Article  PubMed  Google Scholar 

  6. Zhou Y, Cai J, Zhang W, Gong X, Yan S, Zhang K, et al. Impairment of the glymphatic pathway and putative meningeal lymphatic vessels in the aging human. Ann Neurol. 2020;87:357–69.

    Article  CAS  PubMed  Google Scholar 

  7. Eide PK, Vinje V, Pripp AH, Mardal KA, Ringstad G. Sleep deprivation impairs molecular clearance from the human brain. Brain. 2021;144:863–74.

    Article  PubMed  Google Scholar 

  8. •• Astara K, Pournara C, de Natale ER, Wilson H, Vavougios GD, Lappas AS, et al. A novel conceptual framework for the functionality of the glymphatic system. J Neurophysiol. 2023;129:1228-36. This paper provides an expansive overview of the glymphatic system.

  9. Rasmussen MK, Mestre H, Nedergaard M. Fluid transport in the brain. Physiol Rev. 2022;102:1025–51.

    Article  CAS  PubMed  Google Scholar 

  10. Yang L, Kress BT, Weber HJ, Thiyagarajan M, Wang B, Deane R, et al. Evaluating glymphatic pathway function utilizing clinically relevant intrathecal infusion of CSF tracer. J Transl Med. 2013;11:107.

    Article  PubMed  PubMed Central  Google Scholar 

  11. Iliff JJ, Chen MJ, Plog BA, Zeppenfeld DM, Soltero M, Yang L, et al. Impairment of glymphatic pathway function promotes tau pathology after traumatic brain injury. J Neurosci. 2014;34:16180–93.

    Article  PubMed  PubMed Central  Google Scholar 

  12. Rasmussen MK, Mestre H, Nedergaard M. The glymphatic pathway in neurological disorders. Lancet Neurol. 2018;17:1016–24.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Brown R, Benveniste H, Black SE, Charpak S, Dichgans M, Joutel A, et al. Understanding the role of the perivascular space in cerebral small vessel disease. Cardiovasc Res. 2018;114:1462–73.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Kiviniemi V, Wang X, Korhonen V, Keinänen T, Tuovinen T, Autio J, et al. Ultra-fast magnetic resonance encephalography of physiological brain activity—glymphatic pulsation mechanisms? J Cereb Blood Flow Metab. 2016;36:1033–45.

    Article  CAS  PubMed  Google Scholar 

  15. Mestre H, Tithof J, Du T, Song W, Peng W, Sweeney AM, et al. Flow of cerebrospinal fluid is driven by arterial pulsations and is reduced in hypertension. Nat Commun. 2018;9:4878.

    Article  PubMed  PubMed Central  Google Scholar 

  16. Mateo C, Knutsen PM, Tsai PS, Shih AY, Kleinfeld D. Entrainment of arteriole vasomotor fluctuations by neural activity is a basis of blood-oxygenation-level-dependent “resting-state” connectivity. Neuron. 2017;96:936–948.e3.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. van Veluw SJ, Hou SS, Calvo-Rodriguez M, Arbel-Ornath M, Snyder AC, Frosch MP, et al. Vasomotion as a driving force for paravascular clearance in the awake mouse brain. Neuron. 2020;105:549–561.e5.

    Article  PubMed  Google Scholar 

  18. Tithof J, Kelley DH, Mestre H, Nedergaard M, Thomas JH. Hydraulic resistance of periarterial spaces in the brain. Fluid Barriers CNS. 2019;16:19.

    Article  Google Scholar 

  19. Jia Y, Liu C, Li H, Li X, Wu J, Zhao Y, et al. Enlarged perivascular space and its correlation with polysomnography indicators of obstructive sleep apnea. Nat Sci Sleep. 2021;13:863–72.

    Article  PubMed  PubMed Central  Google Scholar 

  20. Lee HJ, Lee DA, Shin KJ, Park KM. Glymphatic system dysfunction in obstructive sleep apnea evidenced by DTI-ALPS. Sleep Med. 2022;89:176–81.

    Article  PubMed  Google Scholar 

  21. Yildiz S, Grinstead J, Hildebrand A, Oshinski J, Rooney WD, Lim MM, et al. Immediate impact of yogic breathing on pulsatile cerebrospinal fluid dynamics. Sci Rep. 2022;12:10894.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Lee G, Dharmakulaseelan L, Muir RT, Iskander C, Kendzerska T, Boulos MI. Obstructive sleep apnea is associated with markers of cerebral small vessel disease in a dose-response manner: A systematic review and meta-analysis. Sleep Med Rev. 2023;68:101763.

    Article  CAS  PubMed  Google Scholar 

  23. Francis F, Ballerini L, Wardlaw JM. Perivascular spaces and their associations with risk factors, clinical disorders and neuroimaging features: A systematic review and meta-analysis. Int J Stroke. 2019;14:359–71.

    Article  PubMed  Google Scholar 

  24. Carotenuto A, Cacciaguerra L, Pagani E, Preziosa P, Filippi M, Rocca MA. Glymphatic system impairment in multiple sclerosis: Relation with brain damage and disability. Brain. 2022;145:2785–95.

    Article  PubMed  Google Scholar 

  25. Wang J, Tian Y, Qin C, Meng L, Feng R, Xu S, et al. Impaired glymphatic drainage underlying obstructive sleep apnea is associated with cognitive dysfunction. J Neurol. 2023;270:2204–16.

    Article  PubMed  PubMed Central  Google Scholar 

  26. Duering M, Biessels GJ, Brodtmann A, Chen C, Cordonnier C, de Leeuw FE, et al. Neuroimaging standards for research into small vessel disease-advances since 2013. Lancet Neurol. 2023;22:602–18.

    Article  PubMed  Google Scholar 

  27. Ramirez J, Holmes MF, Berezuk C, Kwan D, Tan B, Beaton D, et al. MRI-visible perivascular space volumes, sleep duration and daytime dysfunction in adults with cerebrovascular disease. Sleep Med. 2021;83:83–8.

    Article  PubMed  Google Scholar 

  28. Wang J, Chen X, Liao J, Zhou L, Han H, Tao J, et al. Non breathing-related sleep fragmentation and imaging markers in patients with atherosclerotic cerebral small vessel disease (CSVD): A cross-sectional case-control study. BMC Neurol. 2020;20:98.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Del Brutto OH, Mera RM, Del Brutto VJ, Castillo PR. Enlarged basal ganglia perivascular spaces and sleep parameters A population-based study. Clin Neurol Neurosurg. 2019;182:53–7.

    Article  PubMed  Google Scholar 

  30. Del Brutto OH, Mera RM, Costa AF, Rumbea DA, Recalde BY, Castillo PR. Long coronavirus disease-related persistent poor sleep quality and progression of enlarged perivascular spaces. A longitudinal study. Sleep. 2022;45:zsac168.

    Article  PubMed  Google Scholar 

  31. Aribisala BS, Riha RL, Valdes Hernandez M, Muñoz Maniega S, Cox S, Radakovic R, et al. Sleep and brain morphological changes in the eighth decade of life. Sleep Med. 2020;65:152–8.

    Article  PubMed  Google Scholar 

  32. Aribisala BS, M del C VH, Okely JA, Cox SR, Ballerini L, Dickie DA, et al. Sleep quality, perivascular spaces and brain health markers in ageing—a longitudinal study in the Lothian Birth Cohort 1936. Sleep Med. 2023;106:123–31.

    Article  PubMed  Google Scholar 

  33. Lysen TS, Yilmaz P, Dubost F, Ikram MA, de Bruijne M, Vernooij MW, et al. Sleep and perivascular spaces in the middle-aged and elderly population. J Sleep Res. 2022;31:e13485.

    Article  PubMed  Google Scholar 

  34. Gumeler E, Aygun E, Tezer FI, Saritas EU, Oguz KK. Assessment of glymphatic function in narcolepsy using DTI-ALPS index. Sleep Med. 2023;101:522–7.

    Article  PubMed  Google Scholar 

  35. Xie L, Kang H, Xu Q, Chen MJ, Liao Y, Thiyagarajan M, et al. Sleep drives metabolite clearance from the adult brain. Science. 1979;2013(342):373–7.

    Google Scholar 

  36. • Bojarskaite L, Vallet A, Bjørnstad DM, Gullestad Binder KM, Cunen C, Heuser K, et al. Sleep cycle-dependent vascular dynamics in male mice and the predicted effects on perivascular cerebrospinal fluid flow and solute transport. Nat Commun. 2023;14:953. Key paper in documenting the role sleep plays in perivascular CSF flow and transport of solutes.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Voldsbekk I, Maximov II, Zak N, Roelfs D, Geier O, Due-Tønnessen P, et al. Evidence for wakefulness-related changes to extracellular space in human brain white matter from diffusion-weighted MRI. Neuroimage. 2020;212:–116682.

  38. Demiral ŞB, Tomasi D, Sarlls J, Lee H, Wiers CE, Zehra A, et al. Apparent diffusion coefficient changes in human brain during sleep - Does it inform on the existence of a glymphatic system? Neuroimage. 2019;185:263–73.

    Article  PubMed  Google Scholar 

  39. Berry RB, Brooks R, Gamaldo C, Harding SM, Lloyd RM, Quan SF, et al. AASM Scoring Manual Updates for 2017 (Version 2.4). J Clin Sleep Med. 2017;13:665–6.

    Article  PubMed  PubMed Central  Google Scholar 

  40. Borbély AA, Daan S, Wirz-Justice A, Deboer T. The two-process model of sleep regulation: A reappraisal. J Sleep Res. 2016;25:131–43.

    Article  PubMed  Google Scholar 

  41. •• Helakari H, Korhonen V, Holst SC, Piispala J, Kallio M, Väyrynen T, et al. Human NREM sleep promotes brain-wide vasomotor and respiratory pulsations. J Neurosci. 2022;42:2503–15. Key paper in documenting human NREM sleep.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Baril AA, Pinheiro AA, Himali JJ, Beiser A, Sanchez E, Pase MP, et al. Lighter sleep is associated with higher enlarged perivascular spaces burden in middle-aged and elderly individuals. Sleep Med. 2022;100:558–64.

    Article  PubMed  Google Scholar 

  43. Lilius TO, Blomqvist K, Hauglund NL, Liu G, Stæger FF, Bærentzen S, et al. Dexmedetomidine enhances glymphatic brain delivery of intrathecally administered drugs. J Control Release. 2019;304:29–38.

    Article  PubMed  Google Scholar 

  44. Benveniste H, Lee H, Ding F, Sun Q, Al-Bizri E, Makaryus R, et al. Anesthesia with dexmedetomidine and low-dose isoflurane increases solute transport via the glymphatic pathway in rat brain when compared with high-dose isoflurane. Anesthesiology. 2017;127:976–88.

    Article  CAS  PubMed  Google Scholar 

  45. Benveniste H, Liu X, Koundal S, Sanggaard S, Lee H, Wardlaw J. The glymphatic system and waste clearance with brain aging: A review. Gerontology. 2019;65:106–19.

    Article  PubMed  Google Scholar 

  46. Su X, Meng ZT, Wu XH, Cui F, Li HL, Wang DX, et al. Dexmedetomidine for prevention of delirium in elderly patients after non-cardiac surgery: A randomised, double-blind, placebo-controlled trial. Lancet. 2016;388:1893–902.

    Article  CAS  PubMed  Google Scholar 

  47. Mestre H, Hablitz LM, Xavier ALR, Feng W, Zou W, Pu T, et al. Aquaporin-4-dependent glymphatic solute transport in the rodent brain. Elife. 2018;7:e40070.

    Article  PubMed  PubMed Central  Google Scholar 

  48. Nedergaard M. Garbage truck of the brain. Science. 2013;340:1529–30.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Nakada T, Kwee IL, Igarashi H, Suzuki Y. Aquaporin-4 functionality and Virchow-Robin space water dynamics: Physiological model for neurovascular coupling and glymphatic flow. Int J Mol Sci. 2017;18:1798.

    Article  PubMed  PubMed Central  Google Scholar 

  50. Marie S, Larsen IU, Landolt HP, Berger W, Nedergaard M, Moos Knudsenid G, et al. Haplotype of the astrocytic water channel AQP4 is associated with slow wave energy regulation in human NREM sleep. PLoS Biol. 2020;18:e3000623.

    Article  Google Scholar 

  51. Rainey-Smith SR, Mazzucchelli GN, Villemagne VL, Brown BM, Porter T, Weinborn M, et al. Genetic variation in Aquaporin-4 moderates the relationship between sleep and brain Aβ-amyloid burden. Transl Psychiatry. 2018;8:47.

    Article  PubMed  PubMed Central  Google Scholar 

  52. Hablitz LM, Plá V, Giannetto M, Vinitsky HS, Stæger FF, Metcalfe T, et al. Circadian control of brain glymphatic and lymphatic fluid flow. Nat Commun. 2020;11:4411.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Reiter RJ, Sharma R, Cucielo MS, Tan DX, Rosales-Corral S, Gancitano G, et al. Brain washing and neural health: Role of age, sleep, and the cerebrospinal fluid melatonin rhythm. Cell Mol Life Sci. 2023;80:88.

    Article  CAS  PubMed  Google Scholar 

  54. Sepehrinezhad A, Stolze Larsen F, Ashayeri Ahmadabad R, Shahbazi A, Sahab NS. The glymphatic system may play a vital role in the pathogenesis of hepatic encephalopathy: A narrative review. Cells. 2023;12:979.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Lopes CR, Cunha RA, Agostinho P. Astrocytes and adenosine A2 A receptors: Active players in Alzheimer’s disease. Front Neurosci. 2021;15:666710.

    Article  PubMed  PubMed Central  Google Scholar 

  56. Porkka-Heiskanen T, Strecker RE, McCarley RW. Brain site-specificity of extracellular adenosine concentration changes during sleep deprivation and spontaneous sleep: An in vivo microdialysis study. Neuroscience. 2000;99:507–17.

    Article  CAS  PubMed  Google Scholar 

  57. Porkka-Heiskanen T, Strecker RE, Thakkar M, Bjørkum AA, Greene RW, McCarley RW. Adenosine: A mediator of the sleep-inducing effects of prolonged wakefulness. Science. 1997;276:1265–7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Huston JP, Haas HL, Boix F, Pfister M, Decking U, Schrader J, et al. Extracellular adenosine levels in neostriatum and hippocampus during rest and activity periods of rats. Neuroscience. 1996;73:99–107.

    Article  CAS  PubMed  Google Scholar 

  59. Reichert CF, Deboer T, Landolt HP. Adenosine, caffeine, and sleep–wake regulation: State of the science and perspectives. J Sleep Res. 2022;31:e13597.

    Article  PubMed  PubMed Central  Google Scholar 

  60. Landolt HP, Rétey JV, Tönz K, Gottselig JH, Khatami R, Buckelmüller I, et al. Caffeine attenuates waking and sleep electroencephalographic markers of sleep homeostasis in humans. Neuropsychopharmacology. 2004;29:1933–9.

    Article  CAS  PubMed  Google Scholar 

  61. Lunsford-Avery JR, Kollins SH, Kansagra S, Wang W, Engelhard MM. Impact of daily caffeine intake and timing on electroencephalogram-measured sleep in adolescents. J Clin Sleep Med. 2022;18:877–84.

    Article  PubMed  PubMed Central  Google Scholar 

  62. Clark I, Landolt HP. Coffee, caffeine, and sleep: A systematic review of epidemiological studies and randomized controlled trials. Sleep Med Rev. 2017;31:70–8.

    Article  PubMed  Google Scholar 

  63. Burke TM, Markwald RR, McHill AW, Chinoy ED, Snider JA, Bessman SC, et al. Effects of caffeine on the human circadian clock in vivo and in vitro. Sci Transl Med. 2015;7:305ra146.

    Article  PubMed  PubMed Central  Google Scholar 

  64. Zhao ZA, Li P, Ye SY, Ning YL, Wang H, Peng Y, et al. Perivascular AQP4 dysregulation in the hippocampal CA1 area after traumatic brain injury is alleviated by adenosine A2A receptor inactivation. Sci Rep. 2017;7:2254.

    Article  PubMed  PubMed Central  Google Scholar 

  65. Butler T, Zhou L, Ozsahin I, Wang XH, Garetti J, Zetterberg H, et al. Glymphatic clearance estimated using diffusion tensor imaging along perivascular spaces is reduced after traumatic brain injury and correlates with plasma neurofilament light, a biomarker of injury severity. Brain Commun. 2023;5:fcad134.

    Article  PubMed  PubMed Central  Google Scholar 

  66. Opel RA, Christy A, Boespflug EL, Weymann KB, Case B, Pollock JM, et al. Effects of traumatic brain injury on sleep and enlarged perivascular spaces. J Cereb Blood Flow Metab. 2019;39:2258–67.

    Article  PubMed  Google Scholar 

  67. Salman MM, Kitchen P, Halsey A, Wang MX, Törnroth-Horsefield S, Conner AC, et al. Emerging roles for dynamic aquaporin-4 subcellular relocalization in CNS water homeostasis. Brain. 2022;145:64–75.

    Article  PubMed  Google Scholar 

  68. Bu OM, Brannick M, Mortimer J, Umasabor-Bubu O, Sebastiao YV, Wen Y, et al. Sleep, Cognitive impairment, and Alzheimer’s disease: A systematic review and meta-analysis. Sleep. 2017;40(1). https://doi.org/10.1093/sleep/zsw032.

  69. Brown BM, Rainey-Smith SR, Villemagne VL, Weinborn M, Bucks RS, Sohrabi HR, et al. The relationship between sleep quality and brain amyloid burden. Sleep. 2016;39:1063–8.

    Article  PubMed  PubMed Central  Google Scholar 

  70. Taoka T, Masutani Y, Kawai H, Nakane T, Matsuoka K, Yasuno F, et al. Evaluation of glymphatic system activity with the diffusion MR technique: Diffusion tensor image analysis along the perivascular space (DTI-ALPS) in Alzheimer’s disease cases. Jpn J Radiol. 2017;35:172–8.

    Article  PubMed  Google Scholar 

  71. Shen T, Yue Y, Ba F, He T, Tang X, Hu X, et al. Diffusion along perivascular spaces as marker for impairment of glymphatic system in Parkinson’s disease. NPJ Parkinsons Dis. 2022;8:174.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Lee DA, Lee HJ, Park KM. Glymphatic dysfunction in isolated REM sleep behavior disorder. Acta Neurol Scand. 2022;145:464–70.

    Article  PubMed  Google Scholar 

  73. Bae YJ, Kim JM, Choi BS, Ryoo N, Song YS, Nam Y, et al. Altered brain glymphatic flow at diffusion-tensor MRI in rapid eye movement sleep behavior disorder. Radiology. 2023;307:e221848.

    Article  PubMed  Google Scholar 

  74. Cai X, Chen Z, He C, Zhang P, Nie K, Qiu Y, et al. Diffusion along perivascular spaces provides evidence interlinking compromised glymphatic function with aging in Parkinson’s disease. CNS Neurosci Ther. 2023;29:111–21.

    Article  CAS  PubMed  Google Scholar 

  75. Kreutzmann JC, Havekes R, Abel T, Meerlo P. Sleep deprivation and hippocampal vulnerability: Changes in neuronal plasticity, neurogenesis and cognitive function. Neuroscience. 2015;309:173–90.

    Article  CAS  PubMed  Google Scholar 

  76. Han F, Brown GL, Zhu Y, Belkin-Rosen AE, Lewis MM, Du G, et al. Decoupling of global brain activity and cerebrospinal fluid flow in Parkinson’s disease cognitive decline. Mov Disord. 2021;36:2066–76.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Wang XX, Cao QC, Teng JF, Wang RF, Yang ZT, Meng- &, et al. MRI-visible enlarged perivascular spaces: Imaging marker to predict cognitive impairment in older chronic insomnia patients. Eur Radiol. 2022;32:5446-5457.

  78. Del Brutto OH, Mera RM, Del Brutto VJ, Castillo PR. Lack of association between periodic limb movements during sleep and neuroimaging signatures of cerebral small vessel disease in stroke-free community-dwelling older adults. The Atahualpa Project. J Stroke Cerebrovasc Dis. 2020;29:104497.

    Article  PubMed  Google Scholar 

  79. • Sangalli L, Boggero IA. The impact of sleep components, quality and patterns on glymphatic system functioning in healthy adults: A systematic review. Sleep Med. 2023;101:322–49. Review on the role of sleep on glymphatic functioning in humans.

    Article  CAS  PubMed  Google Scholar 

  80. Taoka T, Naganawa S. Neurofluid dynamics and the glymphatic system: A neuroimaging perspective. Vol. 21. Korean J Radiol. 2020;21:1199–209.

    Article  PubMed  PubMed Central  Google Scholar 

  81. Örzsik B, Palombo M, Asllani I, Dijk DJ, Harrison NA, Cercignani M. Higher order diffusion imaging as a putative index of human sleep-related microstructural changes and glymphatic clearance. Neuroimage. 2023;274:120124.

    Article  PubMed  Google Scholar 

  82. Steven AJ, Zhuo J, Melhem ER. Diffusion kurtosis imaging: An emerging technique for evaluating the microstructural environment of the brain. AJR Am J Roentgenol. 2014;202:W26–33.

    Article  PubMed  Google Scholar 

  83. Hsu JL, Wei YC, Toh CH, Hsiao IT, Lin KJ, Yen TC, et al. Magnetic resonance images implicate that glymphatic alterations mediate cognitive dysfunction in Alzheimer disease. Ann Neurol. 2023;93:164–74.

    Article  PubMed  Google Scholar 

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Authors and Affiliations

  1. Sleep Disorders Center, Mayo Clinic College of Medicine, Jacksonville, FL, USA

    Brynn K. Dredla & Pablo R. Castillo

  2. School of Medicine and Research Center, Universidad Espíritu Santo—Ecuador, Samborondón, Ecuador

    Oscar H. Del Brutto

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  1. Brynn K. Dredla
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Dredla, B.K., Del Brutto, O.H. & Castillo, P.R. Sleep and Perivascular Spaces. Curr Neurol Neurosci Rep 23, 607–615 (2023). https://doi.org/10.1007/s11910-023-01293-z

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