Summary
This report gives the results of the first electron-microscopic examination of the cell layers covering the outer brain surface and the inner surface of the cartilaginous skull in the skate, Raja erinacea. The perivascular glial blood-brain barrier — a characteristic of elasmobranchs — extends to the outer surface of the brain. This outer barrier layer is surrounded, in turn, by a subarachnoid compartment (depth: 30–40 μm), containing loose connective tissue and blood vessels; by an arachnoid-like epithelium (10–15 cell layers), impermeable to horseradish peroxidase; and, by perimeningeal fluid, a fluid with a slow turnover rate and a protein composition different from plasma. The inside of the skull, facing the perimeningeal fluid, is covered by a multilayered (10–15 layers) cuboidal epithelium, also impermeable to horseradish peroxidase. Closely apposed cells in the luminal layer of this epithelium have apical microvilli and numerous vesicular profiles, containing material of moderate electron density. These observations may explain, in terms of structure, the regulated protein content of perimeningeal fluid and the restricted exchange of solutes between brain and perimeningeal fluid in elasmobranchs.
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References
Brightman MW, Reese TS (1969) Junctions between intimately apposed cell membranes in the vertebrate brain. J Cell Biol 40:648–679
Brightman MW, Reese TS, Olsson Y, Klatzo I (1971) Morphologic aspects of the blood-brain barrier to peroxidase in elasmobranchs. Prog Neuropathol 1:146–161
Bundgaard M, Cserr HF (1981) A glial blood-brain barrier in elasmobranchs. Brain Res 226:61–73
Butt AM (1987) The presence of a subarachnoid space in the elasmobranch brain — macro and microscopic evidence using large molecular weight fluorescent markers. Biol Bull 173:421
Cserr HF, Bundgaard M (1984) Blood-brain interfaces in vertebrates: a comparative approach. Am J Physiol 246:R277-R288
Cserr HF, Bradbury N, Gomez DG (1979) Drainage of interstitial fluid from brain in the little skate (Raja erinacea). Bull Mt Desert Isl Biol Lab 19:21
Cserr HF, Mackie K, Moody E (1980) Exchange of radiolabeled polyethylene glycols between brain and extradural fluid in skates. Bull Mt Desert Isl Biol Lab 20:6–7
Fenstermacher JD, Patlak CS (1977) CNS, CSF, and extradural fluid uptake of various hydrophilic materials in the dogfish. Am J Physiol 232:R45-R53
Forster RP, Goldstein L, Rosen JK (1972) Intrarenal control of urea reabsorption by renal tubules of the marine elasmobranch, Squalus acanthias. Comp Biochem Physiol 42A:3–12
Gotow T, Hashimoto PH (1984) Plasma membrane organization of astrocytes in elasmobranchs with special reference to the brain barrier system. J Neurocytology 13:727–742
Graham RC, Karnovsky MJ (1965) The early stages of absorption of injected horseradish peroxidase in the proximal tubule of mouse kidney. J Histochem Cytochem 14:291–302
Holmes WN, Donaldson EM (1969) The body compartments and the distribution of electrolytes. In: Hoar WS, Randall DJ (eds) Fish Physiology, vol 1. Academic Press, New York, pp 45–49
Ichimura T, Fraser PA, Cserr HF (1991) Distribution of extracellular tracers in perivascular spaces of the rat brain. Brain Res (in press)
Jones HC (1979) Comparative aspects of the cerebrospinal fluid systems in vertebrates. Sci Prog Oxford 66:171–190
Karnovsky MJ (1971) Use of ferrocyanide-reduced osmium tetroxide in electron microscopy. Proceedings of the 11th Annual Meeting of the American Society for Cell Biology, p 146A
Klatzo I, Steinwall O (1965) Observation on cerebrospinal fluid pathways and behaviour of the blood-brain barrier in sharks. Acta Neuropathol 5:161–175
Klika E (1967) The ultrastructure of meninges in vertebrates. Acta Univ Carol [Med] (Praha) 13:53–71
Momose Y, Kohno K, Ito R (1988) Ultrastructural study on the meninx of the goldfish brain. J Comp Neurol 270:327–336
Moody E, Bradbury M, Cserr H (1981) Intracranial pressure dynamics in skates. Bull Mt Desert Isl Biol Lab 21:5–6
Nabeshima S, Reese TS, Landis DMD, Brightman MW (1975) Junctions in the meninges and marginal glia. J Comp Neurol 164:127–170
Nakao T (1979) Electron microscopic studies on the lamprey meninges. J Comp Neurol 183:429–454
Oppelt WW, Adamson RH, Zubrod CG, Rall DP (1966) Further observations on the physiology of elasmobranch ventricular fluid. Comp Biochem Physiol 17:857–866
Rasmussen L, Rasmussen R (1967) Comparative protein and enzyme profiles of the cerebrospinal fluid, extradural fluid, nervous tissue, and sera of elasmobranchs. In: Gilbert PW, Matthewson RF, Rall DP (eds) Sharks, skates and rays. Johns Hopkins Press, Baltimore, pp 361–379
Roomet A, Fenstermacher JD (1975) Ventricular fluid production and absorption in Squalus acanthias. Comp Biochem Physiol 51A:897–901
Zubrod CG, Rall DP (1959) Distribution of drugs between blood and cerebrospinal fluid in the various vertebrate classes. J Pharmacol Exp Therap 125:194–197
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Bundgaard, M., Cserr, H.F. Barrier membranes at the outer surface of the brain of an elasmobranch, Raja erinacea . Cell Tissue Res 265, 113–120 (1991). https://doi.org/10.1007/BF00318145
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DOI: https://doi.org/10.1007/BF00318145