Cited by 514

Vasomotion as a Driving Force for Paravascular Clearance in the Awake Mouse Brain

van Veluw, Susanne J., Hou, Steven S., Calvo-Rodriguez, Maria, Arbel-Ornath, Michal, Snyder, Austin C., Frosch, Matthew P., Greenberg, Steven M., Bacskai, Brian J.·2020·Neuron

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Crossref · 10.1016/j.neuron.2019.10.033

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  • Cerebrospinal fluid flow in perivascular spaces is driven forward by dynamic constriction and enlargement of the cerebral arteries, and thereby the perivascular space volume, rather than a steady perivascular space size.

    “The data so far indicates that CSF flow in the perivascular spaces (PVSs) is driven forward by dynamic constriction and enlargement of the cerebral arteries, and thereby the PVS volume, rather than a steady PVS size27–31.”

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  1. Aldea R, Weller RO, Wilcock DM, Carare RO, and Richardson G (2019). Cerebrovascular smooth muscle cells as the drivers of periarterial lymphatic drainage of the brain. Front. Aging. Neurosci 11, 1. 30740048 PMC6357927
  2. Arbel-Ornath M, Hudry E, Eikermann-Haerter K, Hou S, Gregory JL, Zhao L, Betensky RA, Frosch MP, Greenberg SM, and Bacskai BJ (2013). Interstitial fluid drainage is impaired in ischemic stroke and Alzheimer’s disease mouse models. Acta. Neuropathol 126, 353– 364. 23818064 PMC3810119
  3. Asgari M, de Zélicourt D, and Kurtcuoglu V (2016). Glymphatic solute transport does not require bulk flow. Sci. Rep 8, 38635. PMC5144134 27929105
  4. Bakker EN, Bacskai BJ, Arbel-Ornath M, Aldea R, Bedussi B, Morris AW, Weller RO, and Carare RO (2016) Lymphatic clearance of the brain: perivascular, paravascular and significance for neurodegenerative diseases. Cell. Mol. Neurobiol 36, 181– 194. 26993512 PMC4844641
  5. Benveniste H, Liu X, Koundal S, Sanggaard S, Lee H, and Wardlaw J (2019). The glymphatic system and waste clearance with brain aging: a review. Gerontology 65, 106– 119. 29996134 PMC6329683
  6. Blaise R, Mateo V, Rouxel C, Zaccarini F, Glorian M, Béréziat G, Golubkov VS, and Limon I (2012). Wild-type amyloid beta 1–40 peptide induces vascular smooth muscle cell death independently from matrix metalloprotease activity. Aging Cell 11, 384– 393. 22260497
  7. Brown LA, Key BJ, and Lovick TA (2002). Inhibition of vasomotion in hippocampal cerebral arterioles during increases in neuronal activity. Auton. Neurosci 10, 137– 140. 11871779
  8. Carare RO, Bernardes-Silva M, Newman TA, Page AM, Nicoll JA, Perry VH, and Weller RO (2008). Solutes, but not cells, drain from the brain parenchyma along basement membranes of capillaries and arteries: significance for cerebral amyloid angiopathy and neuroimmunology. Neuropath. Appl. Neurobiol 34, 131– 144. 18208483
  9. Charidimou A, Boulouis G, Gurol ME, Ayata C, Bacskai BJ, Frosch MP, Viswanathan A, and Greenberg SM (2017). Emerging concepts in sporadic cerebral amyloid angiopathy. Brain 140, 1829– 1850. 28334869 PMC6059159
  10. Christie R, Yamada M, Moskowitz M, and Hyman B (2001). Structural and functional disruption of vascular smooth muscle cells in a transgenic mouse model of amyloid angiopathy Am. J. Pathol 158, 1065– 1071. PMC1850363 11238054
  11. Davis J, Cribbs DH, Cotman CW, and Van Nostrand WE (1999). Pathogenic amyloid beta-protein induces apoptosis in cultured human cerebrovascular smooth muscle cells. Amyloid 6, 157– 164. 10524279
  12. Diem AK, MacGregor Sharp M, Gatherer M, Bressloff NW, Carare RO, and Richardson G (2017). Arterial pulsations cannot drive intramural periarterial drainage: significance for Aβ drainage. Front. Neurosci 11, 475. 28883786 PMC5574214
  13. Dirnagl U, Lindauer U, and Villringer A (1993). Nitric oxide synthase blockade enhances vasomotion in the cerebral microcirculation of anesthetized rats. Microvasc. Res 45, 318– 323. 7686608
  14. Dumas A, Dierksen GA, Gurol ME, Halpin A, Martinez-Ramirez S, Schwab K, Rosand J, Viswanathan A, Salat DH, Polimeni JR, (2012). Functional magnetic resonance imaging detection of vascular reactivity in cerebral amyloid angiopathy. Ann. Neurol 72, 76– 81. 22829269 PMC3408630
  15. Filosa JA, Bonev AD, and Nelson MT (2004). Calcium dynamics in cortical astrocytes and arterioles during neurovascular coupling. Circ. Res 95, e73– 81. 15499024
  16. Hablitz LM, Vinitsky HS, Sun Q, Stæger FF, Sigurdsson B, Mortensen KN, Lilius TO, and Nedergaard M (2019). Increased glymphatic influx is correlated with high EEG delta power and low heart rate in mice under anesthesia. Sci. Adv 5, eaav5447. 30820460 PMC6392807
  17. He Y, Wang M, Chen X, Pohmann R, Polimeni JR, Scheffler K, Rosen BR, Kleinfeld D, and Yu X (2018). Ultra-slow single-vessel BOLD and CBV-based fMRI spatiotemporal dynamics and their correlation with neuronal intracellular Calcium signals. Neuron 97, 925– 939. 29398359 PMC5845844
  18. Iadecola C, Zhang F, Niwa K, Eckman C, Turner SK, Fischer E, Younkin S, Borchelt DR, Hsiao KK, and Carlson GA (1999). SOD1 rescues cerebral endothelial dysfunction in mice overexpressing amyloid precursor protein. Nat. Neurosci 2, 157– 161. 10195200
  19. Iadecola C (2017). The neurovascular unit coming of age: a journey through neurovascular coupling in health and disease. Neuron 96, 17– 42. 28957666 PMC5657612
  20. Jankowsky JL, Slunt HH, Ratovitski T, Jenkins NA, Copeland NG, and Borchelt DR (2001). Co-expression of multiple transgenes in mouse CNS: a comparison of strategies. Biomol. Eng 17, 157– 165. 11337275
  21. Jäkel L, Van Nostrand WE, Nicoll JAR, Werring DJ, and Verbeek MM (2017). Animal models of cerebral amyloid angiopathy. Clin. Sci 131, 2469– 2488. 28963121
  22. Kelly P, Hudry E, Hou SS, and Bacskai BJ (2018). In vivo two photon imaging of astrocytic structure and function in Alzheimer’s disease. Front. Aging. Neurosci 10, 219. 30072889 PMC6060286
  23. Kimbrough IF, Robel S, Roberson ED, and Sontheimer H (2015). Vascular amyloidosis impairs the gliovascular unit in a mouse model of Alzheimer’s disease. Brain 138, 3716– 3733. 26598495 PMC5006220
  24. Kuchibhotla KV, Wegmann S, Kopeikina KJ, Hawkes J, Rudinskiy N, Andermann ML, Spires-Jones TL, Bacskai BJ, and Hyman BT (2014). Neurofibrillary tangle-bearing neurons are functionally integrated in cortical circuits in vivo. Proc. Natl. Acad. Sci. U. S. A 111, 510– 514. 24368848 PMC3890777
  25. Love S, Chalmers K, Ince P, Esiri M, Attems J, Jellinger K, Yamada M, McCarron M, Minett T, Matthews F, (2014). Development, appraisal, validation and implementation of a consensus protocol for the assessment of cerebral amyloid angiopathy in post-mortem brain tissue. Am. J. Neurodegener. Dis 3, 19– 32. 24754000 PMC3986608
  26. Mateo C, Knutsen PM, Tsai PS, Shih AY, and Kleinfeld D (2017). Entrainment of arteriole vasomotor fluctuations by neural activity is a basis of Blood-Oxygenation-Level-Dependent “resting-state” connectivity. Neuron 96, 936– 948. 29107517 PMC5851777
  27. Mestre H, Tithof J, Du T, Song W, Peng W, Sweeney AM, Olveda G, Thomas JH, Nedergaard M, and Kelley DH (2018). Flow of cerebrospinal fluid is driven by arterial pulsations and is reduced in hypertension. Nat. Commun 9, 4878. 30451853 PMC6242982
  28. Niwa K, Younkin L, Ebeling C, Turner SK, Westaway D, Younkin S, Ashe KH, Carlson GA, and Iadecola C (2000). Abeta 1–40-related reduction in functional hyperemia in mouse neocortex during somatosensory activation. Proc. Natl. Acad. Sci. U. S. A 97, 9735– 9740. 10944232 PMC16934
  29. Noordmans HJ, van Blooijs D, Siero JCW, Zwanenburg JJM, Klaessens JHGM, and Ramsey NF (2018). Detailed view on slow sinusoidal, hemodynamic oscillations on the human brain cortex by Fourier transforming oxy/deoxy hyperspectral images. Hum. Brain. Mapp 39, 3558– 3573. 29693304 PMC6099526
  30. Osol G, and Halpern W (1988). Spontaneous vasomotion in pressurized cerebral arteries from genetically hypertensive rats. Am. J. Physiol 254, H28– 33. 3337256
  31. Rayshubskiy A, Wojtasiewicz TJ, Mikell CB, Bouchard MB, Timerman D, Youngerman BE, McGovern RA, Otten ML, Canoll P, McKhann GM 2nd., (2014). Direct, intraoperative observation of ~0.1 Hz hemodynamic oscillations in awake human cortex: implications for fMRI. Neuroimage 87, 323– 331. 24185013 PMC3961585
  32. Park L, Zhou J, Zhou P, Pistick R, El Jamal S, Younkin L, Pierce J, Arreguin A, Anrather J, Younkin SG, (2013). Innate immunity receptor CD36 promotes cerebral amyloid angiopathy. Proc. Natl. Acad. Sci. U. S. A 110, 3089– 3094. 23382216 PMC3581946
  33. Park L, Koizumi K, El Jamal S, Zhou P, Previti ML, Van Nostrand WE, Carlson G, and Iadecola C (2014). Age-dependent neurovascular dysfunction and damage in a mouse model of cerebral amyloid angiopathy. Stroke 45, 1815– 1821. 24781082 PMC4284427
  34. Peca S, McCreary CR, Donaldson E, Kumarpillai G, Shobha N, Sanchez K, Charlton A, Steinback CD, Beaudin AE, Flück D, (2013). Neurovascular decoupling is associated with severity of cerebral amyloid angiopathy. Neurology 81, 1659– 1665. 24097810 PMC3812103
  35. Peng W, Achariyar TM, Li B, Liao Y, Mestre H, Hitomi E, Regan S, Kasper T, Peng S, Ding F, (2016). Suppression of glymphatic fluid transport in a mouse model of Alzheimer’s disease. Neurobiol. Dis 93, 215– 225. 27234656 PMC4980916
  36. Smith AJ, Yao X, Dix JA, Jin BJ, and Verkman AS (2017). Test of the ‘glymphatic’ hypothesis demonstrates diffusive and aquaporin-4-independent solute transport in rodent brain parenchyma. Elife 6, e27679. 28826498 PMC5578736
  37. Sweeney MD, Sagare AP, and Zlokovic BV (2018). Blood-brain barrier breakdown in Alzheimer’s disease and other neurodegenerative disorders. Nat. Rev. Neurol 14, 133– 150. 29377008 PMC5829048
  38. Van Opstal AM, Van Rooden S, Van Harten T, Ghariq E, Labadie G, Fotiadis P, Gurol ME, Terwindt GM, Wermer MJH, Van Buchem MA, (2017). Cerebrovascular function in presymptomatic and symptomatic individuals with hereditary cerebral amyloid angiopathy: a case-control study. Lancet. Neurol 16, 115– 122. 27989553 PMC5505183
  39. Vinters HV (1987). Cerebral amyloid angiopathy. A critical review. Stroke 18, 311– 324. 3551211
  40. Wang P, and Olbricht WL (2011). Fluid mechanics in the perivascular space. J. Theor. Biol 274, 52– 57. 21241713
  41. Weller RO, Massey A, Kuo YM, and Roher AE (2000). Cerebral amyloid angiopathy: accumulation of A beta in interstitial fluid drainage pathways in Alzheimer’s disease. Ann. N. Y. Acad. Sci 903, 110– 117. 10818495
  42. Weller RO, and Nicoll JA (2003). Cerebral amyloid angiopathy: pathogenesis and effects on the ageing and Alzheimer brain. Neurol. Res 25, 611– 616. 14503015
  43. Weller RO, Boche D, and Nicoll JA (2009). Microvasculature changes and cerebral amyloid angiopathy in Alzheimer’s disease and their potential impact on therapy. Acta. Neuropathol 118, 87– 102. 19234858
  44. Winder AT, Echagarruga C, Zhang Q, and Drew PJ (2017). Weak correlations between hemodynamic signals and ongoing neural activity during the resting state. Nat. Neurosci 20, 1761– 1769. 29184204 PMC5816345
  45. Wojtas AM, Kang SS, Olley BM, Gatherer M, Shinohara M, Lozano PA, Liu CC, Kurti A, Baker KE, Dickson DW, (2017). Loss of clusterin shifts amyloid deposition to the cerebrovasculature via disruption of perivascular drainage pathways. Proc. Natl. Acad. Sci. U. S. A 114, 6962– 6971. PMC5565413 28701379
  46. Zipfel GJ, Han H, Ford AL, and Lee JM (2009). Cerebral amyloid angiopathy: progressive disruption of the neurovascular unit. Stroke 40, S16– 19. 19064794 PMC2680011

Cited by

Sorted by citations

Authors
van Veluw, S. J., Hou, S. S., Calvo-Rodriguez, M., Arbel-Ornath, M., Snyder, A. C., Frosch, M. P., Greenberg, S. M., & Bacskai, B. J.
Venue
Neuron
Publisher
Elsevier BV
Published
2020-02
Volume
105
Issue
3
Pages
549-561.e5
ISSN
0896-6273
Cited by
514
References
11
Language
en
Funders
  • Nederlandse Organisatie voor Wetenschappelijk Onderzoek
  • National Institutes of Health

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