Skip to main content
Key Specialties
Cardiology Diabetology Endocrinology Gastroenterology Geriatrics and Gerontology Gynecology and Obstetrics Hematology Infectious Disease Internal Medicine Nephrology Neurology Oncology Pediatrics Respiratory Medicine Rheumatology Surgery
Congress Coverage
2024 ACC Congress 2023 ESMO Congress 2023 EASD Congress 2023 ERS Congress 2023 ESC Congress
Clinical Collections
Advances in Alzheimer’s

Keynote webinar | Spotlight on medication adherence

LIVE: Thursday 27th June 2024, 18:00-19:30 (CEST)
Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.
ADVANCED SEARCH
Log in
Top
Fluids and Barriers of the CNS
Published in: Fluids and Barriers of the CNS 1/2020

Open Access 01-12-2020 | Research

Functional hyperemia drives fluid exchange in the paravascular space

Authors: Ravi Teja Kedarasetti, Kevin L. Turner, Christina Echagarruga, Bruce J. Gluckman, Patrick J. Drew, Francesco Costanzo

Published in: Fluids and Barriers of the CNS | Issue 1/2020

Login to get access

Abstract

The brain lacks a conventional lymphatic system to remove metabolic waste. It has been proposed that directional fluid movement through the arteriolar paravascular space (PVS) promotes metabolite clearance. We performed simulations to examine if arteriolar pulsations and dilations can drive directional CSF flow in the PVS and found that arteriolar wall movements do not drive directional CSF flow. We propose an alternative method of metabolite clearance from the PVS, namely fluid exchange between the PVS and the subarachnoid space (SAS). In simulations with compliant brain tissue, arteriolar pulsations did not drive appreciable fluid exchange between the PVS and the SAS. However, when the arteriole dilated, as seen during functional hyperemia, there was a marked exchange of fluid. Simulations suggest that functional hyperemia may serve to increase metabolite clearance from the PVS. We measured blood vessels and brain tissue displacement simultaneously in awake, head-fixed mice using two-photon microscopy. These measurements showed that brain deforms in response to pressure changes in PVS, consistent with our simulations. Our results show that the deformability of the brain tissue needs to be accounted for when studying fluid flow and metabolite transport.
Appendix
Available only for authorised users
Literature
1.
Cserr HF, Harling-Berg CJ, Knopf PM. Drainage of brain extracellular fluid into blood and deep cervical lymph and its immunological significance. Brain Pathol. 1992;2:269–76.PubMed
2.
Bradbury MW, Cserr HF, Westrop RJ. Drainage of cerebral interstitial fluid into deep cervical lymph of the rabbit. Am J Physiol Ren Fluid Electrolyte Physiol. 1981;9:329–36.
3.
Louveau A, Da Mesquita S, Kipnis J. Lymphatics in neurological disorders: a neuro-lympho-vascular component of multiple sclerosis and Alzheimer’s disease? Neuron. 2016;91:957–73.PubMedPubMedCentral
4.
Louveau A, et al. Structural and functional features of central nervous system lymphatic vessels. Nature. 2015;523:337–41.PubMedPubMedCentral
5.
Aspelund A, et al. A dural lymphatic vascular system that drains brain interstitial fluid and macromolecules. J Exp Med. 2015;212:991–9.PubMedPubMedCentral
6.
Weller RO, Kida S, Zhang E-T. Pathways of fluid drainage from the brain—morphological aspects and immunological significance in rat and man. Brain Pathol. 1992;2:277–84.PubMed
7.
Qiuhang Z, et al. Lymphatic drainage of the skull base: comparative anatomic and advanced imaging studies in the rabbit and human with implications for spread of nasopharyngeal carcinoma. Lymphology. 2010;43:98–109.PubMed
8.
Smith AJ, Verkman AS. CrossTalk opposing view: going against the flow: interstitial solute transport in brain is diffusive and aquaporin-4 independent. J Physiol. 2019;597(17):4421–4.PubMed
9.
Iliff J, Simon M. The glymphatic system supports convective exchange of cerebrospinal fluid and brain interstitial fluid that is mediated by perivascular aquaporin-4. J Physiology. 2019;597(17):4417.
10.
Abbott NJ, Pizzo ME, Preston JE, Janigro D, Thorne RG. The role of brain barriers in fluid movement in the CNS: is there a ‘glymphatic’ system? Acta Neuropathol. 2018;135:1–21.
11.
Smith AJ, Yao X, Dix JA, Jin BJ, Verkman AS. Test of the’glymphatic’ hypothesis demonstrates diffusive and aquaporin-4-independent solute transport in rodent brain parenchyma. Elife. 2017;6:1–16.
12.
Jin B-J, Smith AJ, Verkman AS. Spatial model of convective solute transport in brain extracellular space does not support a “glymphatic” mechanism. J Gen Physiol. 2016;148:489–501.PubMedPubMedCentral
13.
Asgari M, De Zélicourt D, Kurtcuoglu V. Glymphatic solute transport does not require bulk flow. Sci. Rep. 2016;6:1–11.
14.
15.
Iliff JJ, et al. Cerebral arterial pulsation drives paravascular csf-interstitial fluid exchange in the murine brain. J Neurosci. 2013;33:18190–9.PubMedPubMedCentral
16.
Mestre H, et al. Flow of cerebrospinal fluid is driven by arterial pulsations and is reduced in hypertension. Nat. Commun. 2018;9:4878.PubMedPubMedCentral
17.
18.
Iliff JJ, Wang M, Zeppenfeld DM, Venkataraman A, Plog BA, Liao Y, Deane R, Nedergaard M. Cerebral arterial pulsation drives paravascular CSF–interstitial fluid exchange in the murine brain. J Neurosci. 2013;33(46):18190–9.PubMedPubMedCentral
19.
Wang P, Olbricht WL. Fluid mechanics in the perivascular space. J Theor Biol. 2011;274:52–7.PubMed
20.
Damkier HH, Brown PD, Praetorius J. Cerebrospinal fluid secretion by the choroid plexus. Physiol Rev. 2013;93:1847–92.PubMed
21.
Sweetman B, Linninger AA. Cerebrospinal fluid flow dynamics in the central nervous system. Ann Biomed Eng. 2011;39:484–96.PubMed
22.
23.
Thomas JH. Fluid dynamics of cerebrospinal fluid flow in perivascular spaces. J R Soc Interface. 2019;16(159):20190572.PubMedPubMedCentral
24.
25.
Binder DK, Papadopoulos MC, Haggie PM, Verkman AS. In vivo measurement of brain extracellular space diffusion by cortical surface photobleaching. J Neurosci. 2004;24:8049–56.PubMedPubMedCentral
26.
Norwood JN, et al. Anatomical basis and physiological role of cerebrospinal fluid transport through the murine cribriform plate. Elife. 2019;8:1–32.
27.
Coles JA, Myburgh E, Brewer JM, McMenamin PG. Where are we? The anatomy of the murine cortical meninges revisited for intravital imaging, immunology, and clearance of waste from the brain. Prog Neurobiol. 2017;156:107–48.PubMed
28.
Schley D, Carare-Nnadi R, Please CP, Perry VH, Weller RO. Mechanisms to explain the reverse perivascular transport of solutes out of the brain. J Theor Biol. 2006;238:962–74.PubMed
29.
Goriely A, et al. Mechanics of the brain: perspectives, challenges, and opportunities. Biomech Model Mechanobiol. 2015;14:931–65.PubMedPubMedCentral
30.
31.
Mihai LA, Budday S, Holzapfel GA, Kuhl E, Goriely A. A family of hyperelastic models for human brain tissue. J Mech Phys Solids. 2017;106:60–79.
32.
Budday S, et al. Mechanical characterization of human brain tissue. Acta Biomater. 2017;48:319–40.PubMed
33.
Sweetman B, Xenos M, Zitella L, Linninger AA. Three-dimensional computational prediction of cerebrospinal fluid flow in the human brain. Comput Biol Med. 2011;41:67–75.PubMedPubMedCentral
34.
35.
Gupta S, Soellinger M, Grzybowski DM, Boesiger P, Biddiscombe J, Poulikakos D, Kurtcuoglu V. Cerebrospinal fluid dynamics in the human cranial subarachnoid space: an overlooked mediator of cerebral disease.I. Computational model. J R Soc Interface. 2010;7:1195–204.PubMedPubMedCentral
36.
Linninger AA, et al. Cerebrospinal fluid flow in the normal and hydrocephalic human brain. IEEE Trans Biomed Eng. 2007;54:291–302.PubMed
37.
Fin L, Grebe R. Three dimensional modeling of the cerebrospinal fluid dynamics and brain interactions in the aqueduct of sylvius. Comput Methods Biomech Biomed Eng. 2003;6:163–70.
38.
39.
Brinkman HC. A calculation of the viscous force exerted by a flowing fluid on a dense swarm of particles. Flow Turbul Combust. 1949;1(1):27.
40.
Vafai K, Kim SJ. On the limitations of the Brinkman-Forchheimer-extended Darcy equation. Int J Heat Fluid Flow. 1995;16:11–5.
41.
Armstrong JK, Wenby RB, Meiselman HJ, Fisher TC. The hydrodynamic radii of macromolecules and their effect on red blood cell aggregation. Biophys J. 2004;87:4259–70.PubMedPubMedCentral
42.
Schain AJ, Melo A, Strassman AM, Burstein R. Cortical spreading depression closes the paravascular space and impairs glymphatic flow: implications for migraine headache. J Neurosci. 2017;37:3390–16.
43.
Iliff JJ, Wang M, Liao Y, Plogg BA, Peng W, Gundersen GA, Benveniste H, Vates GE, Deane R, Goldman SA, Nagelhus EA. 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.PubMedPubMedCentral
44.
Bedussi B, et al. Paravascular channels, cisterns, and the subarachnoid space in the rat brain: a single compartment with preferential pathways. J Cereb Blood Flow Metab. 2017;37:1374–85.PubMed
45.
Neeves KB, Lo CT, Foley CP, Saltzman WM, Olbricht WL. Fabrication and characterization of microfluidic probes for convection enhanced drug delivery. J Control Release. 2006;111:252–62.PubMed
46.
Smith JH, Humphrey JAC. Interstitial transport and transvascular fluid exchange during infusion into brain and tumor tissue. Microvasc Res. 2007;73:58–73.PubMed
47.
Støverud KH, Langtangen HP, Haughton V, Mardal KA. CSF pressure and velocity in obstructions of the subarachnoid spaces. Neuroradiol J. 2013;26:218–26.PubMedPubMedCentral
48.
Yetkin F, et al. Cerebrospinal fluid viscosity: a novel diagnostic measure for acute meningitis. South Med J. 2010;103:892–5.PubMed
49.
50.
Shih AY, et al. Two-photon microscopy as a tool to study blood flow and neurovascular coupling in the rodent brain. J Cereb Blood Flow Metab. 2012;32:1277–309.PubMedPubMedCentral
51.
Gao YR, et al. Time to wake up: studying neurovascular coupling and brain-wide circuit function in the un-anesthetized animal. Neuroimage. 2017;153:382–98.PubMed
52.
Potter GM, et al. Enlarged perivascular spaces and cerebral small vessel disease. Int J Stroke. 2015;10:376–81.PubMed
53.
Potter GM, Chappell FM, Morris Z, Wardlaw JM. Cerebral perivascular spaces visible on magnetic resonance imaging: development of a qualitative rating scale and its observer reliability. 2015;2015:224–31.
54.
Albargothy NJ, et al. Convective influx/glymphatic system: tracers injected into the CSF enter and leave the brain along separate periarterial basement membrane pathways. Acta Neuropathol. 2018;136:139–52.PubMedPubMedCentral
55.
Weller RO, Sharp MM, Christodoulides M, Carare RO, Møllgård K. The meninges as barriers and facilitators for the movement of fluid, cells and pathogens related to the rodent and human CNS. Acta Neuropathol. 2018;135:363–85.PubMed
56.
Pizzo ME, et al. Intrathecal antibody distribution in the rat brain: surface diffusion, perivascular transport and osmotic enhancement of delivery. J Physiol. 2018;596:445–75.PubMed
57.
Korogod N, Petersen CCH, Knott GW. Ultrastructural analysis of adult mouse neocortex comparing aldehyde perfusion with cryo fixation. Elife. 2015;4:1–17.
58.
Kacem K, Lacombe P, Seylaz J, Bonvento G. Structural organization of the perivascular astrocyte endfeet and their relationship with the endothelial glucose transporter: a confocal microscopy study. Glia. 1998;23:1–10.PubMed
59.
Mestre H, et al. Aquaporin-4-dependent glymphatic solute transport in the rodent brain. Elife. 2018;7:1–31.
60.
61.
Leizea I, et al. Real-time visual tracking of deformable objects in robot-assisted surgery. IEEE Comput Graph Appl. 2015;37:56–68.PubMed
62.
Wittek A, Hawkins T, Miller K. On the unimportance of constitutive models in computing brain deformation for image-guided surgery. Biomech Model Mechanobiol. 2009;8:77–84.PubMed
63.
Franceschini G, Bigoni D, Regitnig P, Holzapfel GA. Brain tissue deforms similarly to filled elastomers and follows consolidation theory. J Mech Phys Solids. 2006;54:2592–620.
64.
Streitberger KJ, et al. In vivo viscoelastic properties of the brain in normal pressure hydrocephalus. NMR Biomed. 2011;24:385–92.PubMed
65.
Sack I, Streitberger KJ, Krefting D, Paul F, Braun J. The influence of physiological aging and atrophy on brain viscoelastic properties in humans. PloS One. 2011;6:e23451.PubMedPubMedCentral
66.
Sack I, et al. The impact of aging and gender on brain viscoelasticity. Neuroimage. 2009;46:652–7.PubMed
67.
Nishimura N, Schaffer CB, Friedman B, Lyden PD, Kleinfeld D. Penetrating arterioles are a bottleneck in the perfusion of neocortex. Proc Natl AcadSci U S A. 2007;104:365–70.
68.
Blinder P, Shih AY, Rafie C, Kleinfeld D. Topological basis for the robust distribution of blood to rodent neocortex. Proc Natl Acad Sci. U. S. A. 2010;107:12670–5.PubMedPubMedCentral
69.
Brands PJ, Willigers JM, Ledoux LAFF, Reneman RS, Hoeks APGG. A noninvasive method to estimate pulse wave velocity in arteries locally by means of ultrasound. Ultrasound Med Biol. 1998;24:1325–35.PubMed
70.
Gladdish S, Rajkumar C. Repeatability of non-invasive measurement of intracerebral pulse wave velocity using transcranial Doppler. Crit Care Med. 2002;30:563–9.
71.
Greenshields CJ, Weller HG. A unified formulation for continuum mechanics applied to fluid-structure interaction in flexible tubes. Int J Numer Methods Eng. 2005;64:1575–93.
72.
Winder AT, Echagarruga C, Zhang Q, Drew PJ. Weak correlations between hemodynamic signals and ongoing neural activity during the resting state. Nat Neurosci. 2017;20:1761–9.PubMedPubMedCentral
73.
Drew PJ, Shih AY, Kleinfeld D. Fluctuating and sensory-induced vasodynamics in rodent cortex extend arteriole capacity. Proc Natl Acad Sci. 2011;108:8473–8.PubMedPubMedCentral
74.
Mishra A, et al. Astrocytes mediate neurovascular signaling to capillary pericytes but not to arterioles. Nat Neurosci. 2016;19:1619.PubMedPubMedCentral
75.
Hill RA, et al. Regional blood flow in the normal and ischemic brain is controlled by arteriolar smooth muscle cell contractility and not by capillary pericytes. Neuron. 2015;87:95–110.PubMedPubMedCentral
76.
Rungta RL, Chaigneau E, Osmanski B-F, Charpak S. Vascular compartmentalization of functional hyperemia from the synapse to the pia. Neuron. 2018;99:362–75.PubMedPubMedCentral
77.
Gao YR, Greene SE, Drew PJ. Mechanical restriction of intracortical vessel dilation by brain tissue sculpts the hemodynamic response. Neuroimage. 2015;115:162–76.PubMed
78.
Goense JBM, Logothetis NK. Neurophysiology of the BOLD fMRI signal in awake monkeys. Curr Biol. 2008;18:631–40.PubMed
79.
Hillman EMC. Coupling mechanism and significance of the BOLD signal: a status report. Annu Rev Neurosci. 2014;37:161–81.PubMedPubMedCentral
80.
Logothetis NK. What we can do and what we cannot do with fMRI. Nature. 2008;453:869.PubMed
81.
82.
von Holstein-Rathlou S, Petersen NC, Nedergaard M. Voluntary running enhances glymphatic influx in awake behaving, young mice. Neurosci Lett. 2018;662:253–8.
83.
Bilston LE, Fletcher DF, Brodbelt AR, Stoodley MA. Arterial pulsation-driven cerebrospinal fluid flow in the perivascular space: a computational model. Comput Methods Biomech Biomed Eng. 2003;6:235–41.
84.
Kedarasetti RT, Drew PJ, Costanzo F. Arterial pulsations drive oscillatory flow of CSF but not directional pumping. Sci Rep. 2020;10:10102.PubMedPubMedCentral
85.
Gao XY, Drew XPJ. Effects of voluntary locomotion and calcitonin gene-related peptide on the dynamics of single dural vessels in awake mice. 2016;36:2503–16.
86.
Marmarou A, Shulman K. Compartmental analysis of compliance and outflow resistance of the cerebrospinal fluid system. J Neurosurg. 1975;43(5):523–34.PubMed
87.
Marmarou A, Shulman K, Rosende RM. A nonlinear analysis of the cerebrospinal fluid system and intracranial pressure dynamics. J Neurosurg. 1978;48:332–44.PubMed
88.
Nama N, Huang TJ, Costanzo F. Acoustic streaming: an arbitrary Lagrangian-Eulerian perspective. J Fluid Mech. 2017;825:600–30.PubMedPubMedCentral
89.
Sánchez AL, et al. On the bulk motion of the cerebrospinal fluid in the spinal canal. J Fluid Mech. 2018;841:203–27.
90.
Teichert T, Grinband J, Hirsch J, Ferrera VP. Effects of heartbeat and respiration on macaque fMRI: implications for functional connectivity. Neuropsychologia. 2010;48:1886–94.PubMed
91.
Dagli MS, Ingeholm JE, Haxby JV. Localization of cardiac-induced signal change in fMRI. Neuroimage. 1999;9:407–15.PubMed
92.
Huo BX, Gao YR, Drew PJ. Quantitative separation of arterial and venous cerebral blood volume increases during voluntary locomotion. Neuroimage. 2015;105:369–79.PubMed
93.
Rideout VC, Dick DE. Difference-differential equations for fluid flow in distensible tubes. IEEE Trans Biomed Eng. 1967:171-7.
94.
Müller LO, Toro EF. Enhanced global mathematical model for studying cerebral venous blood flow. J Biomech. 2014;47:3361–72.PubMed
95.
Müller LO, Toro EF. A global multiscale mathematical model for the human circulation with emphasis on the venous system. Int J Numer Method Biomed Eng. 2014;30:681–725.PubMed
96.
Vignon-Clementel IE, Figueroa CA, Jansen KE, Taylor CA. Outflow boundary conditions for three-dimensional finite element modeling of blood flow and pressure in arteries. Comput Methods Appl Mech Eng. 2006;195:3776–96.
97.
Feng G, et al. Imaging neuronal subsets in transgenic mice expressing multiple spectral variants of GFP. Neuron. 2000;28:41–51.PubMed
98.
Grutzendler J, Kasthuri N, Gan W-B. Long-term dendritic spine stability in the adult cortex. Nature. 2002;420:812.PubMed
99.
Xu HT, Pan F, Yang G, Gan WB. Choice of cranial window type for in vivo imaging affects dendritic spine turnover in the cortex. Nat Neurosci. 2007;10:549–51.PubMed
100.
Hatashita S, Hoff JT. The effect of craniectomy on the biomechanics of normal brain. J Neurosurg. 1987;67:573–8.PubMed
101.
Schaller B, et al. Hemodynamic and metabolic effects of decompressive hemicraniectomy in normal brain: an experimental PET-study in cats. Brain Res. 2003;982:31–7.PubMed
102.
Lam MA, et al. The ultrastructure of spinal cord perivascular spaces: implications for the circulation of cerebrospinal fluid. Sci Rep. 2017;7:1–13.
103.
Berliner J, et al. Abnormalities in spinal cord ultrastructure in a rat model of post-traumatic syringomyelia. Fluids Barriers CNS. 2020;17:1–10.
104.
Liu J, et al. Energy dissipation in mammalian collagen fibrils: cyclic strain-induced damping, toughening, and strengthening. Acta Biomater. 2018;80:217–27.PubMedPubMedCentral
105.
Haut RC, Little RW. A constitutive equation for collagen fibers. J Biomech. 1972;5:423–30.PubMed
106.
Van Oosten ASG, et al. Uncoupling shear and uniaxial elastic moduli of semiflexible biopolymer networks: compression-softening and stretch-stiffening. Sci Rep. 2016;6:1–9.
107.
Vahabi M, et al. Elasticity of fibrous networks under uniaxial prestress. Soft Matter. 2016;12:5050–60.PubMed
108.
Storm C, Pastore JJ, MacKintosh FC, Lubensky TC, Janmey PA. Nonlinear elasticity in biological gels. Nature. 2005;435(7039):191–4.PubMed
109.
Costanzo F, Miller ST. An arbitrary Lagrangian-Eulerian finite element formulation for a poroelasticity problem stemming from mixture theory. Comput Methods Appl Mech Eng. 2017;323:64–97.
110.
Coussy O. Mechanics and physics of porous solids. New Jersey: Wiley; 2011.
111.
Bowen RM. Incompressible porous media models by use of the theory of mixtures. Int J Eng Sci. 1980;18:1129–48.
112.
Sharp MK, Carare RO, Martin BA. Dispersion in porous media in oscillatory flow between flat plates: applications to intrathecal, periarterial and paraarterial solute transport in the central nervous system. Fluids Barriers CNS. 2019;16(1):13.
113.
Heil M, Bertram CD. A poroelastic fluid-structure interaction model of syringomyelia. J Fluid Mech. 2016;809:360–89.
114.
Chou D, Vardakis JC, Guo L, Tully BJ, Ventikos Y. A fully dynamic multi-compartmental poroelastic system: application to aqueductal stenosis. J Biomech. 2016;49:2306–12.PubMed
115.
Xie L, et al. Sleep drives metabolite clearance from the adult brain. Science. 2013;342:373–7.PubMed
116.
117.
118.
Huo B-X, Smith JB, Drew PJ. Neurovascular coupling and decoupling in the cortex during voluntary locomotion. J Neurosci. 2014;34:10975–81.PubMed
119.
Lamme VA, Zipser K, Spekreijse H. Figure-ground activity in primary visual cortex is suppressed by anesthesia. Proc Natl Acad Sci U S A. 1998;95:3263–8.PubMedPubMedCentral
120.
121.
Aksenov DP, Li L, Miller MJ, Iordanescu G, Wyrwicz AM. Effects of anesthesia on BOLD signal and neuronal activity in the somatosensory cortex. J Cereb Blood Flow Metab. 2015;35:1819–26.PubMedPubMedCentral
122.
Pisauro MA, Dhruv NT, Carandini M, Benucci A. Fast hemodynamic responses in the visual cortex of the awake mouse. J Neurosci. 2013;33:18343–51.PubMedPubMedCentral
123.
Gakuba C, et al. General anesthesia inhibits the activity of the ‘glymphatic system’. Theranostics. 2018;8:710–22.PubMedPubMedCentral
124.
Bergel A, Deffieux T, Demené C, Tanter M, Cohen I. Local hippocampal fast gamma rhythms precede brain-wide hyperemic patterns during spontaneous rodent REM sleep. Nat Commun. 2018;9(1):1–2.
125.
126.
Kudo T, et al. Are cerebrovascular factors involved in Alzheimer’s disease? Neurobiol Aging. 2000;21:215–24.PubMed
127.
la Torre JC. Alzheimer disease as a vascular disorder: nosological evidence. Stroke. 2002;33:1152–62.PubMed
128.
Iadecola C. Neurovascular regulation in the normal brain and in Alzheimer’s disease. Nat Rev Neurosci. 2004;5:347–60.PubMed
129.
Ding J, et al. Large perivascular spaces visible on magnetic resonance imaging, cerebral small vessel disease progression, and risk of dementia: the age, gene/environment susceptibility–Reykjavik study. JAMA Neurol. 2017;74:1105–12.PubMedPubMedCentral
130.
Fernández MA, Formaggia L, Gerbeau J-F, Quarteroni A. The derivation of the equations for fluids and structure. In: Formaggia L, Quarteroni A, Veneziani A, editors. Cardiovascular Mathematics: Modeling and simulation of the circulatory system. Milan: Springer Milan; 2009. p. 77–121. https://​doi.​org/​10.​1007/​978-88-470-1152-6_​3.CrossRef
131.
Wick T. Fluid-structure interactions using different mesh motion techniques. Comput Struct. 2011;89:1456–67.
132.
Gerbeau J-F, Vidrascu M, Frey P. Fluid–structure interaction in blood flows on geometries based on medical imaging. Comput Struct. 2005;83:155–65.
133.
Eriksson K, Estep D, Hansbo P, Johnson C. Computational differential equations. Cambridge: Cambridge University Press; 1996.
134.
Massi F, Peng JW, Lee JP, Straub JE. Simulation study of the structure and dynamics of the Alzheimer’s amyloid peptide congener in solution. Biophys J. 2001;80:31–44.PubMedPubMedCentral
135.
Tseng BP, et al. Deposition of monomeric, not oligomeric, Aβ mediates growth of Alzheimer’s disease amyloid plaques in human brain preparations. Biochemistry. 1999;38:10424–31.PubMed
136.
137.
Wolfram Research, Inc., Mathematica, Version 12.0, Wolfram Research Inc., Champaign, Illinois (2019).
138.
Matlab, version 9.7.0 (R2019b), The MathWorks Inc., Natick, Massachusetts (2019).
139.
Guizar-Sicairos M, Thurman ST, Fienup JR. Efficient subpixel image registration algorithms. Opt Lett. 2008;33:156.PubMed
140.
Gao YR, Drew PJ. Determination of vessel cross-sectional area by thresholding in Radon space. J Cereb Blood Flow Metab. 2014;34:1180–7.PubMedPubMedCentral
141.
Lindquist MA, Loh JM, Atlas LY, Wager TD. Modeling the hemodynamic response function in fMRI: efficiency, bias and mis-modeling. Neuroimage. 2009;45:S187–98.PubMed
142.
Kong L, Little JP, Cui M. Motion quantification during multi-photon functional imaging in behaving animals. Biomed Opt Express. 2016;7:3686.PubMedPubMedCentral
143.
Glover GH. Deconvolution of impulse response in event-related BOLD fMRI. Neuroimage. 1999;9:416–29.PubMed
144.
Prevost TP, Balakrishnan A, Suresh S, Socrate S. Biomechanics of brain tissue. Acta Biomater. 2011;7:83–95.PubMed
145.
Horton NG, et al. In vivo three-photon microscopy of subcortical structures within an intact mouse brain. Nat Photonics. 2013;7:205–9.PubMedCentral
146.
Vanlandewijck M, et al. A molecular atlas of cell types and zonation in the brain vasculature. Nature. 2018;554:475–80.PubMed
147.
Adams MD, Winder AT, Blinder P, Drew PJ. The pial vasculature of the mouse develops according to a sensory-independent program. Sci Rep. 2018;8:1–12.
148.
Barber TW, Brockway JA, Higgins LS. The density of tissues in and about the head. Acta Neurol Scand. 1970;46:85–92.PubMed
Metadata
Title
Functional hyperemia drives fluid exchange in the paravascular space
Authors
Ravi Teja Kedarasetti
Kevin L. Turner
Christina Echagarruga
Bruce J. Gluckman
Patrick J. Drew
Francesco Costanzo
Publication date
01-12-2020
Publisher
BioMed Central
Published in
Fluids and Barriers of the CNS / Issue 1/2020
Electronic ISSN: 2045-8118
DOI
https://doi.org/10.1186/s12987-020-00214-3

Other articles of this Issue 1/2020

Fluids and Barriers of the CNS 1/2020 Go to the issue

Research

Abnormalities in spinal cord ultrastructure in a rat model of post-traumatic syringomyelia

Research

Autophagy-mediated occludin degradation contributes to blood–brain barrier disruption during ischemia in bEnd.3 brain endothelial cells and rat ischemic stroke models

Research

Permeability of the windows of the brain: feasibility of dynamic contrast-enhanced MRI of the circumventricular organs

Research

Diabetes is associated with familial idiopathic normal pressure hydrocephalus: a case–control comparison with family members

Review

Review: pathophysiology of intracranial hypertension and noninvasive intracranial pressure monitoring

Research

Simvastatin, edaravone and dexamethasone protect against kainate-induced brain endothelial cell damage