Abstract
The classic model of cerebrospinal fluid (CSF) formation, transport across the central nervous system, and absorption is based on the circulation theory. This model, where CSF is thought to be secreted by the choroid plexus, and to circulate from the ventricles into the cisterns and the subarachnoid spaces (SAS), is no longer considered reliable. Several studies indicate that CSF can be produced and absorbed throughout the entire CSF system, notably the ependyma, the perineural SAS, and the Virchow-Robin spaces (VRS). The discovery of the expression of aquaporin 1 (AQP1) in the choroidal plexus and aquaporin 4 (AQP4) in the end-feet of astrocytes underlying pia mater, has shed new light into the mechanisms of fluid exchange between intracranial compartments. In this emerging model, CSF has a direct correlation with the brain interstitial fluid (ISF), the blood circulation, and the lymphatic system. These new insights into the physiology and homeostasis of CSF, together with the new advances in neuroimaging, especially in MRI techniques, might have relevant implications for understanding the mechanisms at the base of brain pathologies.
References
Achiron A, Faibel M et al (2002) Sandlike appearance of Virchow-Robin spaces in early multiple sclerosis: a novel neuroradiologic marker. AJNR Am J Neuroradiol 23:376–380
Agre P, Bonhivers M, Borgnia MJ (1998) The Aquaporins, blueprints for cellular plumbing systems. J Biol Chem 273(24):14659–14662
Alcolado R, Weller RO, Parrish EP et al (1988) The cranial arachnoid and pia mater in man: anatomical and ultrastructural observations. Neuropathol Appl Neurobiol 14:1–17
Ames A 3rd, Sakanoue M, Endo S (1964) Na, K, Ca, Mg, and C1 concentrations in choroid plexus fluid and cisternal fluid compared with plasma ultrafiltrate. J Neurophysiol 27:672–681
Badaut J, Ashwal S, Adami A et al (2011) Brain water mobility decreases after astrocytic aquaporin-4 inhibition using RNA interference. J Cereb Blood Flow Metab 31:819–831
Barkhof F, Kouwenhoven M, Scheltens P (1994) Phase-contrast cine MR imaging of normal aqueductal CSF flow. Effect of aging and relation to CSF void on modulus MR. Acta Radiol 35:123–130
Bateman GA, Brown KM (2012) The measurement of CSF flow through the aqueduct in normal and hydrocephalic children: from where does it come, to where does it go? Childs Nerv Syst 28:55–63
Bateman GA, Napier BD (2011) External hydrocephalus in infants: six cases with MR venogram and flow quantification correlation. Childs Nerv Syst 27:2087–2096
Bechmann I, Priller J, Kovac A et al (2001) Immune surveillance of mouse brain perivascular spaces by blood-borne macrophages. Eur J Neurosci 14: 1651–1658
Becker NH, Novikoff AB, Zimmerman HM (1967) Fine structure observations of the uptake of intravenously injected peroxidase by the rat choroid plexus. J Histochem Cytochem 15:160–165
Benga G (2003) Birth of water channel proteins-the aquaporins. Cell Biol Int 27(9):701–709
Bering EA Jr (1959) Cerebrospinal fluid production and its relationship to cerebral metabolism and cerebral blood flow. Am J Phys 197:825–828
Bering EA Jr, Sato O (1963) Hydrocephalus: changes in formation and absorption of cerebrospinal fluid within the cerebral ventricles. J Neurosurg 20:1050–1063
Borgnia M, Nielsen S, Engel A et al (1999) Cellular and molecular biology of the aquaporin water channels. Annu Rev Biochem 68:425–458
Boulton M, Flessner M, Armstrong D et al (1998) Determination of volumetric cerebrospinal fluid absorption into extracranial lymphatics in sheep. Am J Phys 274:R88–R96
Bradbury MW, Cserr HF, Westrop RJ (1981) Drainage of cerebral interstitial fluid into deep cervical lymph of the rabbit. Am J Phys 240:F329–F336
Bradley WG Jr (2016) Magnetic resonance imaging of normal pressure hydrocephalus. Semin Ultrasound CT MR 37:120–128
Bradley WG Jr, Kortman KE, Burgoyne B (1986) Flowing cerebrospinal fluid in normal and hydrocephalic states: appearance on MR images. Radiology 159:611–616
Bradley WG Jr, Whittemore AR, Kortman KE et al (1991) Marked cerebrospinal fluid void: indicator of successful shunt in patients with suspected normal-pressure hydrocephalus. Radiology 178:459–466
Bradley WG Jr, Scalzo D, Queralt J et al (1996) Normal-pressure hydrocephalus: evaluation with cerebrospinal fluid flow measurements at MR imaging. Radiology 198:523–529
Brierley JB, Field EJ, Yoffey JM (1949) Passage of Indian ink particles from the cranial subarachnoid space. J Anat 83:77
Brinker T, Ludemann W, Berens V et al (1997) Dynamic properties of lymphatic pathways for the absorption of cerebrospinal fluid. Acta Neuropathol (Berl) 94:493–498
Brinker T, Stopa E, Morrison J et al (2014) A new look at cerebrospinal fluid circulation. Fluids Barriers CNS 11:10
Bulat M, Klarica M (2011) Recent insights into a new hydrodynamics of the cerebrospinal fluid. Brain Res Rev 65:99–112
Carare R, Bernardes-Silva M, Newman T et al (2008) Solutes, but not cells, drain from the brain parenchyma along basement membranes of capillaries and arteries: significance for cerebral amyloid angiopathy and neuroimmunology. Neuropathol Appl Neurobiol 34:131–144
Chazal J, Tanguy A, Irthum B et al (1985) Dilatation of the subarach- noid pericerebral space and absorption of cerebrospinal fluid in the infant. Anat Clin 7:61–66
Conforti R, Cirillo M, Saturnino PP et al (2014) Dilated Virchow-Robin spaces and multiple sclerosis: 3T magnetic resonance study. Radiol Med 119:408–414
Cotugno D (1764) De ischiade nervosa commentarius. Simonios, Napoli
Courtice FC, Simmonds WJ (1951) The removal of protein from the subarachnoid space. Aust J Exp Biol Med Sci 29:255–263
Cserr HF (1971) Physiology of the choroid plexus. Physiol Rev 51:273–311
Cushing H (1925) The third circulation and its channels. Lancet 2:851–857
d’Avella D, Baroni A, Mingrino S et al (1980) An electron microscope study of human arachnoid villi. Surg Neurol 14:41–47
d’Avella D, Cicciarello R, Albiero F et al (1983) Scanning electron microscope study of human arachnoid villi. J Neurosurg 59(4):620–626
Dandy WE (1919) Experimental hydrocephalus. Ann Surg 70:129–142
Davson H (1966) Formation and drainage of the cerebrospinal fluid. Sci Basis Med Annu Rev 1:238–259
Davson H, Segal MB (1996) Physiology of the cerebrospinal fluid and blood-brain barriers, vol 832. CRC Press, London
de Rougemont J, Ames A III, Nesbett FB et al (1960) Fluid formed by choroid plexus; a technique for its collection and a comparison of its electrolyte composition with serum and cisternal fluids. J Neurophysiol 23:485–495
Di Rocco C, Di Trapani G, Pettorossi VE et al (1979) On the pathology of experimental hydrocephalus induced by artificial increase in endoventricular CSF pulse pressure. Childs Brain 5(2):81–95
Dohrmann GJ, Bucy PC (1970) Human choroid plexus: a light and electron microscopic study. J Neurosurg 33:506–516
Egnor M, Zheng L, Rosiello A et al (2002) A model of pulsations in communicating hydrocephalus. Pediatr Neurosurg 36(6):281–303
Enzmann DR, Pelc NJ (1991) Normal flow patterns of intracranial and spinal cerebrospinal fluid defined with phase-contrast cine MR imaging. Radiology 178: 467–474
Erlich SS, McComb JG, Hyman S et al (1986) Ultrastructural morphology of the olfactory pathway for cerebrospinal fluid drainage in the rabbit. J Neurosurg 64:466–473
Foldi M, Csillik B, Zoltan OT (1968) Lymphatic drainage of the brain. Experientia 24:1283–1287
Gomez DG, Di Benedetto AT, Pavese AM et al (1981) Development of arachnoid villi and granulations in man. Acta Anat 111:247–258
Greitz D (1993) Cerebrospinal fluid circulation and associated intracranial dynamics. A radiologic investigation using MR imaging and radionuclide cisternography. Acta Radiol Suppl 386:1–23
Greitz D (2007) Paradigm shift in hydrocephalus research in legacy of Dandy’s pioneering work: rationale for third ventriculostomy in communicating hydrocephalus. Childs Nerv Syst 23:487–489
Hadaczek P, Yamashita Y, Mirek H et al (2006) The “Perivascular pump” driven by arterial pulsation is a powerful mechanism for the distribution of therapeutic molecules within the brain. Mol Ther 14:69–78
Hassin GB (1947) The cerebrospinal fluid pathways (a critical note). J Neuropathol Exp Neurol 6:172–176
Hassin GB, Oldberg E, Tinsley M (1937) Changes in the brain in plexectomized dogs with commentson the cerebrospinal fluid. Arch Neurol Psychiatry 38:1224–1239
Haughton VM, Korosec FR, Medow JE et al (2003) Peak systolic and diastolic CSF velocity in the foramen magnum in adult patients with Chiari I malformations and in normal control participants. AJNR Am J Neuroradiol 24(2):169–176
Hayashi N, Matsumae M, Yatsushiro S et al (2015) Quantitative analysis of cerebrospinal fluid pressure gradients in healthy volunteers and patients with normal pressure hydrocephalus. Neurol Med Chir (Tokyo) 55(8):657–662
Hutchings M, Weller RO (1986) Anatomical relationships of the pia mater to cerebral blood vessels in man. J Neurosurg 65:316–325
Ichimura T, Fraser PA, Cserr HF (1991) Distribution of extracellular tracers in perivascular spaces of the rat brain. Brain Res 545:103–113
Igarashi H, Tsujita M, Kwee IL et al (2014) Water influx into cerebrospinal fluid (CSF) is primarily controlled by aquaporin-4, not by aquaporin-1: O-17 JJVCPE MRI study in knockout mice. Neuroreport 25:39–43
Iliff JJ, Wang M, Liao Y et al (2012) A paravascular pathway facilitates CSF flow through the brain parenchyma and the clearance of interstitial solutes, including amyloid. Sci Transl Med 4:147ra111
Iliff JJ, Chen MJ, Plog BA et al (2014) Impairment of glymphatic pathway function promotes tau pathology after traumatic brain injury. J Neurosci 34: 16180–16193
Iskandar BJ, Quigley M, Haughton VM (2004) Foramen magnum cerebrospinal fluid flow characteristics in children with Chiari I malformation before and after craniocervical decompression. J Neurosurg 101(2 Suppl):169–178
Johanson CE, Stopa EG, McMillan PN (2011) The blood-cerebrospinal fluid barrier: structure and functional significance. Methods Mol Biol 686:101–131
Jung JS, Ratan VB, Preston GM et al (1994) Molecular characterization of an aquaporin cDNA from brain: candidate osmoreceptor and regulator of water balance. Proc Natl Acad Sci 91:13052–13056
Kahle KT, Kulkarni AV, Limbrick DD Jr et al (2016) Hydrocephalus in children. Lancet 387:788–799
Kahlon B, Annertz M, Stahlberg F et al (2007) Is aqueductal stroke volume, measured with cine phase-contrast magnetic resonance imaging scans useful in predicting outcome of shunt surgery in suspected normal pressure hydrocephalus? Neurosurgery 60: 124–130
Key EAH, Retzius MG (1875) Studien in der Anatomie des Nervensystems und des Bindegewebes. Samson and Wallin, Stockholm
Kida S, Pentazis A, Weller RO (1993) Cerebrospinal fluid drains directly from the subarachnoid space into nasal lymphatics in the rat. Anatomy, histology and immunological significance. Neuropathol Appl Neurobiol 19:480–488
Kim DS, Choi JU, Huh R et al (1999) Quantitative assessment of cerebrospinal fluid hydrodynamics using a phase-contrast cine MR image in hydrocephalus. Childs Nerv Syst 15:461–467
Klarica M, Mise B, Vladic A et al (2013) “Compensated hyperosmolarity” of cerebrospinal fluid and the development of hydrocephalus. Neuroscience 248C: 278–289
Koç K, Anik Y, Anik I et al (2007) Chiari 1 malformation with syringomyelia: correlation of phase-contrast cine MR imaging and outcome. Turk Neurosurg 17(3): 183–192
Krahn V (1982) The pia mater at the site of the entry of blood vessels into the central nervous system. Anat Embryol (Berl) 164:257–263
Krisch B (1988) Ultrastructure of the meninges at the site of penetration of veins through the dura mater, with particular reference to Pacchionian granulations. Investigations in the rat and two species of new-world monkeys (Cebus apella, Callitrix jacchus). Cell Tissue Res 251:621–631
Krisch B, Leonhardt H, Oksche A (1984) Compartments and perivascular arrangement of the meninges covering the cerebral cortex of the rat. Cell Tissue Res 238: 459–474
Krueger M, Bechmann I (2010) CNS pericytes: concepts, misconceptions, and a way out. Glia 58:1–10
Lee JH, Lee HK, Kim JK et al (2004) CSF flow quantification of the cerebral aqueduct in normal volunteers using phase contrast cine MR imaging. Korean J Radiol 5:81–86
Lee H, Xie L, Yu M et al (2015) The effect of body posture on brain glymphatic transport. J Neurosci 35: 11034–11044
Levine JE, Povlishock JT, Becker DP (1982) The morphological correlates of primate cerebrospinal fluid absorption. Brain Res 241:31–41
Li X, Kong H, Wu W et al (2009) Aquaporin-4 maintains ependymal integrity in adult mice. Neuroscience 162:67–77
Longatti P (2008) Domenico Felice Cotugno and the rationale of his discovery of CSF. Childs Nerv Syst 24(2): 161–162
Longatti P, Basaldella L, Orvieto E et al (2004) Choroid plexus and aquaporin 1: a novel explanation of cerebrospinal fluid production. Pediatr Neurosurg 40(6): 277–283
MacAulay N, Zeuthen T (2010) Water transport between CNS compartments: contributions of aquaporins and cotransporters. Neuroscience 168:941–956
Macey RI, Karan DM, Farmer RE (1972) Properties of water channels in human red cells. Biomembranes 255(2):502–516
Mascalchi M, Arnetoli G, Inzitari D et al (1993) Cine-MR imaging of aqueductal CSF flow in normal pressure hydrocephalus syndrome before and after CSF shunt. Acta Radiol 34:586–592
Matsushima T (1983) Choroid plexus papillomas and human choroid plexus: a light and electron microscopy study. J Neurosurg 59:1054–1062
McComb JG (1983) Recent research into the nature of cerebrospinal fluid formation and absorption. J Neurosurg 59:369–383
McGirt MJ, Atiba A, Attenello FJ et al (2008) Correlation of hindbrain CSF flow and outcome after surgical decompression for Chiari I malformation. Childs Nerv Syst 24(7):833–840
Menick BJ (2001) Phase-contrast magnetic resonance imaging of cerebrospinal fluid flow in the evaluation of patients with Chiari I malformation. Neurosurg Focus 11:E5
Milhorat TH (1974) Failure of choroid plexectomy as treatment for hydrocephalus. Surg Gynecol Obstet 139:505–508
Milhorat TH (1975) The third circulation revisited. J Neurosurg 42:628–645
Mollanji R, Bozanovic-Sosic R, Zakharov A et al (2002) Blocking cerebrospinal fluid absorption through the cribriform plate increases resting intracranial pressure. Am J Physiol Regul Integr Comp Physiol 282:R1593–R1599
Moon HC, Baek HM, Park YS (2016) Comparison of 3 and 7 tesla magnetic resonance imaging of obstructive hydrocephalus caused by tectal glioma. Brain Tumor Res Treat 4(2):150–154
Naidich TP, Altman NR, Conzalez-Arias SM (1993) Phase contrast cine magnetic resonance imaging: normal cerebrospinal fluid oscillation and applications to hydrocephalus. Neurosurg Clin N Am 4:677–705
Nakada T (2014) Virchow-Robin space and aquaporin-4: new insights on an old friend. Croat Med J 55:328–336
Nakada T (2015) The Molecular Mechanisms of Neural Flow Coupling: A New Concept. J Neuroimaging 25:861–865
Neely JD, Christensen BM, Nielsen S et al (1999) Heterotetrameric composition of aquaporin-4 water channels. Biochemistry 38(34):11156–11163
O’Donnell M (1985) NMR blood flow imaging using multiecho, phase contrast sequences. Med Phys 12(1): 59–64
O’Rahilly R, Müller F (1986) The meninges in human development. J Neuropathol Exp Neurol 45:588–608
Oner Z, Sagіr Kahraman A, Kose E et al (2017) Quantitative evaluation of normal aqueductal cerebrospinal fluid flow using phase-contrast cine MRI according to age and sex. Anat Rec (Hoboken) 300(3):549–555
Oreskovic D, Klarica M, Vukic M (2002) The formation and circulation of cerebrospinal fluid inside the cat brain ventricles: a fact or an illusion? Neurosci Lett 327:103–106
Panigrahi M, Reddy BP, Reddy AK et al (2004) CSF flow study in Chiari I malformation. Childs Nerv Syst 20:336–340
Pardridge WM (2011) Drug transport in brain via the cerebrospinal fluid. Fluids Barriers CNS 8:7
Penn RD, Basati S, Sweetman B et al (2011) Ventricle wall movements and cerebrospinal fluid flow in hydrocephalus. J Neurosurg 115:159–164
Pinna G, Alessandrini F, Alfieri A et al (2000) Cerebrospinal fluid flow dynamics study in Chiari I malformation: implications for syrinx formation. Neurosurg Focus 8(3):E3
Pollay M (2010) The function and structure of the cerebrospinal fluid system. Cerebrospinal Fluid Res 7:9
Pollay M, Curl F (1967) Secretion of cerebrospinal fluid by the ventricular ependyma of the rabbit. Am J Phys 213:1031–1038
Pollay M, Stevens A, Estrada E et al (1972) Extracorporeal perfusion of choroid plexus. J Appl Physiol 32: 612–617
Praetorius J, Nielsen S (2006) Distribution of sodium transporters and aquaporin-1 in the human choroid plexus. Am J Physiol Cell Physiol 291:C59–C67
Quigley MF, Iskandar B, Quigley ME et al (2004) Cerebrospinal fluid flow in foramen magnum: temporal and spatial patterns at MR imaging in volunteers and in patients with Chiari I malformation. Radiology 232(1):229–236
Radoš M, Orešković D, Radoš M et al (2014) Long lasting near-obstruction stenosis of mesencephalic aqueduct without development of hydrocephalus – case report. Croat Med J 55:394–398
Rennels ML, Gregory TF, Blaumanis OR et al (1985) Evidence for a ‘paravascular’ fluid circulation in the mammalian central nervous system, provided by the rapid distribution of tracer protein throughout the brain from the subarachnoid space. Brain Res 326:47–63
Ringstad G, Emblem KE, Eide PE (2016) Phase-contrast magnetic resonance imaging reveals net retrograde aqueductal flow in idiopathic normal pressure hydrocephalus. J Neurosurg 124:1850–1857
Robin C (1859) Recherches sur quelques particularites de la structure des capillaires de l’encephale. J Physiol Homme Animaux 2:537–548
Saadoun S, Tait MJ, Reza A et al (2009) AQP4 gene deletion in mice does not alter blood–brain barrier integrity or brain morphology. Neuroscience 161:764–772
Sahuquillo J, Poca MA, Amoros S (2001) Current aspects of pathophysiology and cell dysfunction after severe head injury. Curr Pharm Des 7(15):1475–1503
Schley D, Carare-Nnadi R, Please CP et al (2006) Mechanisms to explain the reverse perivascular transport of solutes out of the brain. J Theor Biol 238:962–974
Schroeder HW, Schweim C, Schweim KH et al (2000) Analysis of aqueductal cerebrospinal fluid flow after endoscopic aqueductoplasty by using cine phase-contrast magnetic resonance imaging. J Neurosurg 93:237–244
Scollato A, Tenenbaum R, Bahl G et al (2008) Changes in aqueductal CSF stroke volume and progression of symptoms in patients with unshunted idiopathic normal pressure hydrocephalus. AJNR Am J Neuroradiol 29(1):192–197
Scollato A, Gallina P, Gautam B et al (2009) Changes in aqueductal CSF stroke volume in shunted patients with idiopathicnormal-pressure hydrocephalus. AJNR Am J Neuroradiol 30(8):1580–1586
Shibukawa S, Tosiaki Miyati T, Niwa T et al (2017) Time-spatial labeling inversion pulse (time-SLIP) with pencil beam pulse: a selective labeling technique for observing cerebrospinal fluid flow dynamics. Magn Reson Med Sci 17:259. Aug 24 [Epub ahead of print]
Silver I, Li B, Szalai J et al (1999) Relationship between intracranial pressure and cervical lymphatic pressure and flow rates in sheep. Am J Phys 277:R1712–R1717
Simmonds WJ (1953) The absorption of labeled erythrocytes from the subarachnoid space of the rabbit. J Exp Biol Med Sci 31:77–83
Singer JR, Crooks LE (1983) Nuclear magnetic resonance blood flow measurements in the human brain. Science 221:654–656
Speake T, Freeman LJ, Brown PD (2003) Expression of aquaporin 1 and aquaporin 4 water channels in rat choroid plexus. Biochim Biophys Acta 1609(1):80–86
Szentistvanyi I, Patlak CS, Ellis RA et al (1984) Drainage of interstitial fluid from different regions of rat brain. Am J Phys 246:F835–F844
Tawfik AM, Elsorogy L, Abdelghaffar R et al (2017) Phase-contrast MRI CSF flow measurements for the diagnosis of normal-pressure hydrocephalus: observer agreement of velocity versus volume parameters. AJR Am J Roentgenol 208(4):838–843
Tennyson VM, Pappas GD (1968) The fine structure of choroid plexus: adult and developmental stages. Prog Brain Res 29:63–85
Tripathi RC (1977) The functional morphology of the outflow systems of ocular and cerebrospinal fluids. Exp Eye Res 25:65–116
Virchow R (1851) Ueber die Erweiterung kleinerer Gefaesse. Arch Pathol Anat Physiol Klin Med 3:427–462
Wagshul ME, Chen JJ, Egnor MR et al (2006) Amplitude and phase of cerebrospinal fluid pulsations: experimental studies and review of the literature. J Neurosurg 104:810–819
Wagshul ME, Eide PK, Madsen JR (2011) The pulsating brain: a review of experimental and clinical studies of intracranial pulsatility. Fluids Barriers CNS 18(8):5
Weed LH (1914a) Studies on cerebro-spinal fluid. No. II: the theories of drainage of cerebro-spinal fluid with an analysis of the methods of investigation. J Med Res 31:21–49
Weed LH (1914b) Studies on cerebro-spinal fluid. No. III: the pathways of escape from the subarachnoid spaces with particular reference to the Arachnoid Villi. J Med Res 31:51–91
Weed LH (1914c) Studies on cerebro-spinal fluid. No. IV: the dual source of cerebro-spinal fluid. J Med Res 31:93–118
Weed LH (1917) The development of the cerebrospinal spaces in pig and in man. Contrib Embryol Carnegie Inst 5:1–116
Welch K (1963) Secretion of cerebrospinal fluid by choroid plexus of the rabbit. Am J Phys 205:617–624
Welch K (1975) The principles of physiology of the cerebrospinal fluid in relation to hydrocephalus including normal pressure hydrocephalus. Adv Neurol 13: 247–332
Welch K, Friedman V (1960) The cerebrospinal fluid valves. Brain 83:454–469
Welch K, Pollay M (1961) Perfusion of particles through arachnoid villi of the monkey. Am J Phys 201:651–654
Welch K, Pollay M (1963) The spinal arachnoid villi of the monkeys Cercopithecus aethiops and Macaca irus. Anat Rec 145:43–48
Weller RO, Kida S, Zhang ET (1992) Pathways of fluid drainage from the brain–morphological aspects and immunological significance in rat and man. Brain Pathol 2:277–284
Weller RO, Djuanda E, Yow HY et al (2009) Lymphatic drainage of the brain and the pathophysiology of neurological disease. Acta Neuropathol 117:1–14
Weller RO, Galea I, Carare RO et al (2010) Pathophysiology of the lymphatic drainage of the central nervous system: implications for pathogenesis and therapy of multiple sclerosis. Pathophysiology 17:295–306
Whish S, Dziegielewska KM, Møllgård K et al (2015) The inner CSF-brain barrier: developmentally controlled access to the brain via intercellular junctions. Front Neurosci 12(9):16
Whytt R (1768) Observations on the dropsy in the brain. J. Balfour, Edinburgh
Woollam DH, Millen JW (1955) The perivascular spaces of the mammalian central nervous system and their relation to the perineuronal and subarachnoid spaces. J Anat 89:193–200
Xie L, Kang H, Xu Q et al (2013) Sleep drives metabolite clearance from the adult brain. Science 342:373–377
Yamada S, Miyazaki M, Kanazawa H et al (2008) Visualization of cerebrospinal fluid movement with spin labeling at MR imaging: preliminary results in normal and pathophysiologic conditions. Radiology 249: 644–652
Yamada S, Tsuchiya K, Bradley WG et al (2015) Current and emerging MR imaging techniques for the diagnosis and management of CSF flow disorders: a review of phase-contrast and time-spatial labeling inversion pulse. AJNR Am J Neuroradiol 36(4):623–630
Zhang ET, Inman CB, Weller RO (1990) Interrelationships of the pia mater and the perivascular (Virchow-Robin) spaces in the human cerebrum. J Anat 170:111–123
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Section Editor information
Rights and permissions
Copyright information
© 2019 Springer Nature Switzerland AG
About this entry
Cite this entry
Longatti, P., Basaldella, L., Feletti, A., Fiorindi, A. (2019). Cerebrospinal Fluid Circulation. In: Cinalli, G., Ozek, M., Sainte-Rose, C. (eds) Pediatric Hydrocephalus. Springer, Cham. https://doi.org/10.1007/978-3-319-31889-9_39-1
Download citation
DOI: https://doi.org/10.1007/978-3-319-31889-9_39-1
Received:
Accepted:
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-319-31889-9
Online ISBN: 978-3-319-31889-9
eBook Packages: Springer Reference Biomedicine and Life SciencesReference Module Biomedical and Life Sciences