Skip to main content
Log in

Morphological indications for considerable diffuse reabsorption of cerebrospinal fluid in spinal meninges particularly in the areas of meningeal funnels

An electronmicroscopical study including tracing experiments in rats

  • Original Articles
  • Published:
Anatomy and Embryology Aims and scope Submit manuscript

Abstract

Transmission and scanning electron microscopical observations in the rat indicate a considerable capacity of the spinal meninges to reabsorb cerebrospinal fluid. The density of blood vessels and lymphatics in the duramater is extremely high, particularly in the areas of meningeal funnels and spinal nerve root sleeves. Arterioles with closely related unmyelinated nerve fibres, many fenestrated capillaries and venules predetermine these areas as sites where absorption processes could take place. At certain sites of the meningeal angle region, the arachnoid membrane, mostly multilayered, is reduced to only three or four layers. Intercellular discontinuities and cytoplasmic fenestrations occurring in the arachnoid lining cell layer result in direct communications between the subarachnoid space and cisterns of the arachnoid “reticular layer”. These cisterns are partly fluid-filled, partly occupied by a net of collagen fibre bundles. Some cisterns harbour macrophages that often project filiform processes through the lining cell layer into the subarachnoid space, contacting cerebrospinal fluid. Desmosomes and gap junctions are present in all layers of the arachnoid. However, tight junctions and the continuous electrondense intercellular gap, known to occur normally within the “arachnoid barrier layer”, were not seen in many sites of the meningeal angle region. Numerous arachnoid cells display a high degree of vesiculation. Cationized ferritin, introduced in vivo into the rat subarachnoid space, passes inter- and intracellularly from the cerebrospinal fluid compartment through the arachnoid membrane, reaching durai blood vessels and lymphatics. Tracer could be visualized both in the cytoplasm of the endothelium and on the luminal surface of the cells. Tracer also passed through pial cell layers into pial vessels, through leptomeningeal sheaths into vessels crossing the subarachnoid space, into the connective tissue compartment and into vessels of spinal dorsal root ganglia. In the angle region, a particularly large number of macrophages can be found on the surface of leptomeninges, within the arachnoid reticular layers, and in close relation to dural and epidural capillaries, venules and lymphatics. Their possible role in the process of cerebrospinal fluid reabsorption is discussed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Andres KH (1967) Über die Feinstruktur der Arachnoidea und Dura mater von Mammalia. Z Zellforsch 79:272–295

    Google Scholar 

  • Andres KH, Düring M von, Muszynski K, Schmidt RF (1987) Nerve fibres and their terminals of the dura mater encephali of the rat. Anat Embryol 175:289–301

    Google Scholar 

  • Arnold W, Ritter R, Wagner WH (1973) Quantitative studies on the drainage of the cerebrospinal fluid into the lymphatic system. Acta Otolaryngol 76:156–161

    Google Scholar 

  • Becker NH, Hirano A, Zimmerman HM (1968) Observations on the distribution of exogenous peroxidase in the rat cerebrum. J Neuropathol Exp Neurol 27:439–452

    Google Scholar 

  • Bowsher D (1957) Pathways of absorption of protein from the cerebrospinal fluid: an autoradiographic study in the cat. Anat Rec 128:23–40

    Google Scholar 

  • Bradbury MWB, Cserr HF, Westrop RJ (1981) Drainage of cerebral interstitial fluid into deep cervical lymph of the rabbit. Am J Physiol 9:F329-F336

    Google Scholar 

  • Braun JS, Kaissling B, Le Hir M, Zenker W (1993) Cellular components of the immune barrier in the spinal meninges and dorsal root ganglia of the normal rat: immunohistochemical (MHC class II) and electron-microscopic observations. Cell Tissue Res 273:209–217

    CAS  PubMed  Google Scholar 

  • Brierley JB, Field EJ (1948) The connexions of the spinal sub-arachnoid space with the lymphatic system. J Anat 82:153–166

    Google Scholar 

  • Brightman MW (1968) The intracerebral movement of proteins injected into blood and cerebrospinal fluid of mice. Prog Brain Res 29:19–40

    Google Scholar 

  • Brightman MW, Reese TS (1969) Junctions between intimately apposed cell membranes in the vertebrate brain. J Cell Biol 40:648–677

    Google Scholar 

  • Butler A (1984) Correlated physiologic and structural studies of CSF absorption. In: Shapiro K, Marmarou A, Portnoy H (eds) Hydrocephalus. Raven Press, New York, pp 41–57

    Google Scholar 

  • Cloyd MW, Low FN (1974) Scanning electron microscopy of the subarachnoid space in the dog. I. Spinal cord levels. J Comp Neurol 153:325–368

    Google Scholar 

  • Cserr HF, Harling-Berg CJ, Knopf PM (1992) Drainage of brain extracellular fluid into blood and deep cervical lymph and its immunological significance. Brain Pathol 2:269–276

    Google Scholar 

  • Danon D, Goldstein L, Marikovsky Y, Skutelsky E (1972) Use of cationized ferritin as a label of negative charges on cell surfaces. J Ultrastruct Res 38:500–510

    Google Scholar 

  • Dijkstra CD, Döpp EA, Joling P, Kraal G (1985) The heterogeneity of mononuclear phagocytes in lymphoid organs: distinct macrophage subpopulations in the rat recognized by monoclonal antibodies ED1, ED2 and ED3. Immunology 54:589–599

    CAS  PubMed  Google Scholar 

  • Du Boulay GH (1966) Pulsatile movements in the CSF pathways. Br J Radiol 39:255–262

    Google Scholar 

  • Du Boulay G, O'Connell J, Currie J, Bostick T, Verity P (1972) Further investigations on pulsatile movements in the cerebrospinal fluid pathways. Acta Radiol Diagn Stockh 13:496–523

    Google Scholar 

  • Düring M von, Bauersachs M, Böhmer B, Veh RW, Andres KH (1990) Neuropeptide Y- and substance P-like immunoreactive nerve fibers in the rat dura mater encephali. Anat Embryol 182:363–373

    Google Scholar 

  • Epstein DL, Rohen JW (1991) Morphology of the trabecular meshwork and inner-wall endothelium after cationized ferritin perfusion in the monkey eye. Invest Ophthalmol Vis Sci 32:160–171

    Google Scholar 

  • Esiri MM, Gay D (1990) Immunological and neuropathological significance of the Virchow-Robin space. J Neurol Sci 100:3–8

    Google Scholar 

  • Földi M (1993) Lymphostatische Enzephalopathie und Ophthalmopathie. In: Földi M, Kubik S (eds) Lehrbuch der Lymphologie. Fischer, Stuttgart, pp 364–369

    Google Scholar 

  • Földi M, Gellért A, Kozma M, Poberai M, Zoltán ÖT, Csanda E (1966) New contributions to the anatomical connections of the brain and the lymphatic system. Acta Anat 64:498–505

    Google Scholar 

  • Földi M, Csillik B, Zoltán ÖT (1968) Lymphatic drainage of the brain. Experientia 24:1283–1287

    Google Scholar 

  • Foley F (1921) Resorption of the cerebrospinal fluid by the choroid plexuses under the influence of intravenous injection of hypertonic salt solutions. Arch Neurol Psychiatry 5:744–745

    Google Scholar 

  • Frederickson RG, Low FN (1969) Blood vessels and tissue space associated with the brain of the rat. Am J Anat 125:123–145

    Google Scholar 

  • Galkin WS (1930) Zur Methodik der Injektion des Lymphsystems vom Subarachnoidalraum aus (Bedeutung der Injektionsstelle). Z Gesamte Exp Med 72:482–495

    Google Scholar 

  • Haines DE, Frederickson RG (1991) The meninges. In: Al-Mefty O (ed) Meningiomas. Raven Press, New York, pp 9–25

    Google Scholar 

  • Hassin GB (1947) The cerebrospinal fluid pathways. J Neuropathol Exp Neurol 7:172–193

    Google Scholar 

  • Himango WA, Low FN (1971) The fine structure of a lateral recess of the subarachnoid space in the rat. Anat Rec 171:1–20

    Google Scholar 

  • Howarth F, Cooper ERA (1955) The fate of certain foreign colloids and crystalloids after subarachnoid injection. Acta Anat 25:112–140

    Google Scholar 

  • Jackson RT, Tigges J, Arnold W (1979) Subarachnoid space of the CNS, nasal mucosa, and lymphatic system. Arch Otolaryngol 105:180–184

    Google Scholar 

  • Kaplan HA, Ford DH (1966) The brain vascular system. Elsevier, Amsterdam

    Google Scholar 

  • Keller JT, Marfurt CF (1991) Peptidergic and serotoninergic innervation of the rat dura mater. J Comp Neurol 309:515–534

    Google Scholar 

  • Key EAH, Retzius MG (1875) Studien in der Anatomie des Nerven-systems und des Bindegewebes. Samson & Wallin, Stockholm

    Google Scholar 

  • Kida S, Yamashima T, Kubota T, Ito H, Yamamoto S (1988) A light and electron microscopic and immunohistochemical study of human arachnoid villi. J Neurosurg 69:429–435

    Google Scholar 

  • Kido DK, Gomez DG, Pavese AM Jr, Potts DG (1976) Human spinal arachnoid villi and granulations. Neuroradiology 11:221–228

    Google Scholar 

  • Klika E (1967) The ultrastructure of meninges in vertebrates. Acta Univ Carol Med 13:53–71

    Google Scholar 

  • Koenig H (1958) An autoradiographic study of nucleic acid and protein turnover in the mammalian neuraxis. J Biophys Biochem Cytol 4:785–797

    Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Lefauconnier JM, Bouchaud C, Bernard G (1991) Initial process of diffusion of small molecules from blood vessels to the meninges in young rats. Neurosci Lett 121:9–11

    Google Scholar 

  • Levin E, Sepulveda FV, Yudilevich DL (1974) Pial vessels transport of substances from cerebrospinal fluid to blood. Nature 249:266–268

    Google Scholar 

  • Levine JE, Povlishock JT, Becker DP (1982) The morphological correlates of primate cerebrospinal fluid absorption. Brain Res 241:31–41

    Google Scholar 

  • Magari S (1983) The spinal cord and the lymphatic system. In: Földi M, Casley-Smith JR (ed) Lymphangiology. Schattauer, Stuttgart, pp 509–517

    Google Scholar 

  • Matyszak MK, Lawson LJ, Perry VH, Gordon S (1992) Stromal macrophages of the choroid plexus situated at an interface between the brain and peripheral immune system constitutively express major histocompatibility class II antigens. J Neuroimmunol 40:173–182

    Google Scholar 

  • McCabe JS, Low FN (1969) The subarachnoid angle: an area of transition in peripheral nerve. Anat Rec 164:15–34

    Google Scholar 

  • McComb JG (1983) Recent research into the nature of cerebrospinal fluid formation and absorption. J Neurosurg 59:369–383

    Google Scholar 

  • Milhorat TH, Davis DA, Hammock MK (1975) Experimental intracerebral movement of electron microscopic tracers of various molecular sizes. J Neurosurg 42:315–329

    Google Scholar 

  • Mott FW (1910) The Oliver-Sharpey Lectures on the cerebrospinal fluid. Lecture I: the physiology of the cerebrospinal fluid. Lancet 11:1–8

    Google Scholar 

  • Nabeshima S, Reese TS, Landis DMD, Brightman MW (1975) Junctions in the meninges and marginal glia. J Comp Neurol 164:127–170

    Google Scholar 

  • Nathanson JA, Chun LLY (1989) Immunological function of the blood-cerebrospinal fluid barrier. Proc Natl Acad Sci USA 86:1684–1688

    Google Scholar 

  • Rennels ML, Gregory TI, Baumanis OR, Fujimoto IC, Grady PA (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

    Google Scholar 

  • Schroth G, Klose U (1992) Cerebrospinal fluid flow. Neuroradiology 35:1–24

    Google Scholar 

  • Schwalbe G (1869) Der Arachnoidalraum ein Lymphraum und sein Zusammenhang mit dem Perichorioidalraum. Centralbl Med Wissensch 30:465–467

    Google Scholar 

  • Spector R, Johanson CE (1989) The mammalian choroid plexus. Scientific American 261:48–53

    Google Scholar 

  • Speransky AD (1950) Grundlagen der Theorie der Medizin. Saenger, Berlin

    Google Scholar 

  • Tarlov IM, Perlmutter I, Berman AJ (1951) Paralysis caused by penicillin injection; mechanism of complication — a warning. J Neuropathol Exp Neurol 10:158–166

    Google Scholar 

  • Tripathi R (1974) Tracing the bulk outflow route of cerebrospinal fluid by transmission and scanning electron microscopy. Brain Res 80:503–506

    Google Scholar 

  • Turner PT, Harris AB (1974) Ultrastructure of exogenous peroxidase in cerebral cortex. Brain Res. 74:305–326

    Google Scholar 

  • Upton ML, Weller RO (1985) The morphology of cerebrospinal fluid drainage pathways in human arachnoid granulations. J Neurosurg 63:867–875

    Google Scholar 

  • Villegas JC, Broadwell RD (1993) Transcytosis of protein through the mammalian cerebral epithelium and endothelium. II. Adsorptive transcytosis of WGA-HRP and the blood-brain and brain-blood barriers. J Neurocytol 22:67–80

    Google Scholar 

  • Waggener JD, Beggs J (1967) The membranous coverings of neural tissues: an electron microscopy study. J Neuropathol Exp Neurol 26:412–426

    Google Scholar 

  • Wagner HJ, Pilgrim CH, Brandl J (1974) Penetration and removal of cerebral horseradish peroxidase injected into the cerebrospinal fluid: role of cerebral perivascular spaces, endothelium, and microglia. Acta Neuropathol 27:299–315

    Google Scholar 

  • Weed LH (1914) Studies on cerebro-spinal fluid. III. The pathways of escape from the subarachnoid spaces with particular reference to the arachnoid villi. J Med Res 31:51–91

    Google Scholar 

  • Weed LH (1923) The absorption of cerebrospinal fluid into the venous system. Am J Anat 31:191–221

    Google Scholar 

  • Welch K, Friedman V (1960) The cerebrospinal fluid valves. Brain 83:454–469

    Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Yamashima T (1988) Functional ultrastructure of cerebrospinal fluid drainage channels in human arachnoid villi. Neurosurg 22:633–641

    Google Scholar 

  • Zenker W, Rinne B, Bankoul S, Le Hir M, Kaissling B (1992) 5′-Nucleotidase in the spinal meningeal compartments in the rat. Histochemistry 98:135–139

    Google Scholar 

  • Zervas NT, Liszczak TM, Mayberg MR, Black PM (1982) Cerebrospinal fluid may nourish cerebral vessels through pathways in the adventitia that may be analogous to systemic vasa vasorum. J Neurosurg 56:475–481

    Google Scholar 

  • Zhang ET, Inman CBE, Weller RO (1990) Interrelationships of the pia mater and the perivascular (Virchow-Robin) spaces in the human cerebrum. J Anat 170:111–123

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zenker, W., Bankoul, S. & Braun, J.S. Morphological indications for considerable diffuse reabsorption of cerebrospinal fluid in spinal meninges particularly in the areas of meningeal funnels. Anat Embryol 189, 243–258 (1994). https://doi.org/10.1007/BF00239012

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00239012

Key words

Navigation