Summary
The intercellular clefts of the brain and the leptomeninges, and the perivascular spaces were studied with reference to the results obtained in a previous study (Krisch et al. 1983). The spatial relationships of these compartments were analyzed at the electron-microscopic level. Horse-radish peroxidase (HRP) was injected into the brain or into the contralateral ventricle.
The pattern of distribution of HRP depends on the boundary situation in the individual compartments. The inner and outer pial layers accompany the vessels intruding into the brain. In the Virchow-Robin space the pial funnel obliterates within a short distance. The inner arachnoid layer is continuous with the outer arachnoid layer when it covers the vessels traversing the meningeal space. The perivascular compartment is not in communication with the arachnoid space; moreover, the pial funnel within the Virchow-Robin space is sealed off against the arachnoid space.
Thus, blood vessels traversing the meningeal spaces and subsequently penetrating the brain surface are exposed to the common intercellular compartment represented by the intercellular clefts of the brain and the leptomeninges; this compartment does not communicate with the other compartments. The cerebrospinal fluid located in this intercellular compartment is preferentially drained into the upper cervical lymph nodes.
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References
Allen DJ, Didio LJA (1977) Scanning and transmission electron microscopy of the encephalic meninges in dogs. J Submicr Cytol 9:1–22
Allen DJ, Low FN (1975) Scanning electron microscopy of the subarachnoid space in the dog. III. Cranial levels. J Comp Neurol 161:515–540
Anderson DR (1969) Ultrastructure of meningeal sheaths: Normal human and monkey optic nerves. Arch Opthalmol 82:659–674
Andres KH (1967) Über die Feinstruktur der Arachnoidea und Dura mater von Mammalia. Z Zellforsch 79:272–295
Bondareff W, McLone DG (1973) The external glial limiting membrane in Macaca: Ultrastructure of a laminated glioepithelium. Am J Anat 136:277–296
Borison HL, Borison R, McCarthy LE (1980) Brain stem penetration by horseradish peroxidase from the cerebrospinal fluid spaces in the cat. Exp Neurol 69:271–289
Braak E (1975) On the fine structure of the external glial layer in the isocortex of man. Cell Tissue Res 157:367–390
Bradbury MWB, Cserr HF, Westrop RJ (1981) Drainage of cerebral interstitial fluid into deep cervical lymph of the rabbit. Am J Physiol 240:F329-F336
Brightman MW (1968) Intracerebral movement of proteins injected into the blood and cerebrospinal fluid in mice. In: Lajtha A, Ford DH (eds) Brain barrier systems. Prog Brain Res 29:19–37
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
Cordingley GE, Somjen GG (1978) The clearing of excess potassium from extracellular space in spinal cord and cerebral cortex. Brain Res 151:291–306
Csanda G, Komoly S, Horváth S (1983) Morphological data concerning the connection (relation) between the central nervous system and extracranial lymphatics. In: Hossmann KA, Klatzo I (eds) Cerebrovascular transport mechanisms. Springer, Berlin Heidelberg New York p 139
Cserr HF (1975) Bulk flow of cerebral extracellular fluid as a possible mechanism of CSF-brain exchange. In: Cserr HF, Fenstermacher JD, Fencl V (eds) Fluid environment of the brain. Academic Press, New York San Francisco London, pp 215–224
Cserr HF Ostrach LH (1974) Bulk flow of interstitial fluid after intracranial injection of blue dextran 2000. Exp Neurol 45:50–60
Desaga U, Leonhardt H (1976) Bindegewebe in perivaskulären Räumen subependymaler Kapillaren des Rückenmarkes beim Kaninchen. Z Mikrosk Anat Forsch 90:801–15
Dietzel I, Heinemann U, Hofmeier G, Lux HD (1980) Transient changes in the size of the extracellular space in the sensorimotor cortex of cats in relation to stimulus-induced changes in potassium concentration. Exp Brain Res 40:432–439
Ebersolt C, Perez M, Vassent G, Bockaert J (1981) Characteristics of the β1- and β2-adrenergic-sensitive adenylate cyclases in glial cell primary cultures and their comparison with β2-adrenergic-sensitive adenylate cyclase of meningeal cells. Brain Res 213:151–161
Edvinsson L, Egund N, Owman C, Sahlin C, Svendgaard NA (1982) Reduced noradrenaline uptake and retention in cerebrovascular nerves associated with angiographically visible vasoconstriction following experimental subarachnoid hemorrhage in rabbits. Brain Res Bull 9:799–805
Földi M (1972) Physiologie und Pathophysiologie des Lymphgefäßsystems. In: Altmann et al. (eds) Handbuch der allgemeinen Pathologie, Vol III/6. Springer, Berlin Heidelberg New York, pp 239–310
Földi M, Gátaí G, Papp N, Eöllös Z, Mézáros A (1960) Abtransport von corpusculären Teilchen aus dem Subarachnoidealraum beim Hund. Z Ges Exp Med 133:110–112
Franck G, Grisar T, Moonen G (1983) Glial and neuronal Na+, K+ pump. Adv Cellul Neurobiol 4:133–159
Frederickson RG, Haller FR (1971) The subarachnoid space interpreted as a special portion of the connective tissue space. Proc North Dakota Acad Sci 24:142–159
Frederickson RG, Low FN (1969) Blood vessels and tissue space associated with the brain of the rat. Am J Anat 125:123–146
Friedman AH, Davis JN (1980) Identification and characterization of adrenergic receptors and catecholamine-stimulated adenylate cyclase in dog pial membranes. Brain Res 183:89–102
Fukuda Y, Honda Y, Schläfke ME, Loeschke HH (1978) Effect of H+ on the membrane potential of silent cells in the ventral and dorsal surface layers of the rat medulla in vitro. Pflügers Arch 376:229–235
Haller FR, Low FN (1971) The fine structure of the peripheral nerve root sheath in the subarachnoid space in the rat and other laboratory animals. Am J Anat 131:1–20
Haller FR, Haller AC, Low FN (1972) The fine structure of cellular layers and connective tissue space at spinal nerve root attachments in the rat. Am J Anat 133:109–124
Haug H (1972) Die postnatale Entwicklung der Gliadeckschicht der Sehrinde der Katze. Eine elektronenmikroskopische Studie über die Ausbildung von Lamellenstapeln. Z Zellforsch 123:544–565
Held H (1909) Über die Neuroglia marginalis der menschlichen Großhirnrinde. Mschr Psychiat Neurol 26 (Erg Heft):360–416
Himango WA, Low FN (1971) The fine structure of a lateral recess of the subarachnoid space in the rat. Anat Rec 171:1–20
His W (1865) Über ein perivasculäres Canalsystem in den nervösen Centralorganen und über dessen Beziehungen zum Lymphsystem. Z wiss Zool 15:127–141
Iida T (1966) Elektronenmikroskopische Untersuchungen am oberflächlichen Anteil des Gehirns bei Hund und Katze. Arch Histol Jpn 27:267–285
Jones EG (1970) On the mode of entry of blood vessels into the cerebral cortex. J Anat 106:507–520
Kaplan GP, Hartman KB, Creveling CR (1981) Localization of catechol-O-methyltransferase in the leptomeninges, choroid plexus and ciliary epithelium: Implications for the separation of central and peripheral catechols. Brain Res 204:353–360
Key A, Retzius G (1875) Studien in der Anatomie des Nervensystems und des Bindegewebes. I. Der feinere Bau der Häute des Gehirns und Rückenmarks. Samson & Wallin, Stockholm
Krahn V (1982) The pia mater at the site of the entry of blood vessels into the central nervous system. Anat Embryol 164:257–263
Krisch B, Leonhardt H, Oksche A (1983) The meningeal compartments of the median eminence and the cortex. A comparative analysis in the rat. Cell Tissue Res 228:597–640
Leonhardt H (1980) Ependym und Circumventrikuläre Organe. In: Oksche A, Vollrath L (eds) Handbuch der mikroskopischen Anatomie des Menschen. Neuroglia I. Nervensystem, 10. Teil. Springer, Berlin Heidelberg New York, pp 177–666
Lopes CAS, Mair WGP (1974) Ultrastructure of the arachnoid membrane in man. Acta Neuropathol (Berl) 28:167–173
McComb JG (1983) Recent research into the nature of cerebrospinal fluid formation and absorption. J Neurosurg 59:369–383
Merchant RE, Low FN (1979) Scanning electron microscopy of the subarachnoid space in the dog: Evidence for a non-hematogenous origin of subarachnoid macrophages. Am J Anat 156:183–206
Millen JW, Woollam DHM (1962) The anatomy of the cerebrospinal fluid. Oxford University Press, London New York Toronto
Møller M, Møllgård K, Lund-Andersen H, Hertz L (1974) Concordance between morphological and biochemical estimates of fluid spaces in rat brain cortex slices. Exp Brain Res 21:299–314
Morse DE, Low FN (1971) Regional variations in the fine structure of the pia mater of the rat. Anat Rec 169:457
Nelson E, Blinzinger K, Hager H (1961) Electron microscopic observations on subarachnoid and perivascular spaces of the Syrian hamster brain. Neurology (Minneap) 11:285–295
Nicholson C, Phillips JM, Gardner-Medwin AR (1979) Diffusion from a iontophoretic point source in the brain: role of tortuosity and volume fraction. Brain Res 169:580–584
Niessing K (1936) Über systemartige Zusammenhänge der Neuroglia im Großhirn und über ihre funktioneile Bedeutung. Gegenbaurs Morph Jb 78:537–584
Niessing K (1952) Über den histologischen Aufbau der Bluthirnschranke. Dtsch Z Nervenheilk 168:485–498
Obersteiner H (1888) Nervöse Zentralorgane. Franz Deuticke, Leipzig u. Wien
Olson MD, Low FN (1971) The fine structure of developing cartilage in the chick embryo. Am J Anat 131:197–216
Palmer GC, Palmer SJ (1983) Adenylate cyclase sensitivity to catecholamines and forskolin in rat pia-arachnoid and cerebral microvessels. Neuropharmacology 22:213–221
Pease CD, Schultz RL (1958) Electron microscopy of rat cranial meninges. Am J Anat 102:301–321
Ramsey HJ (1965) Fine structure of the surface of the cerebral cortex of human brain. J Cell Biol 26:323–333
Rascol M, Izard J (1972) La jonction cortico-pie-mérienne et la pénétration des vaisseaux dans le cortex cérébral chez l'Homme. Structure et ultrastructure. Z Zellforsch 123:337–355
Robin C (1859) Recherches sur quelques particularités de la structure des capillaires de l'encéphale. J Physiol 2:537–548
Rovainen CM, Lemcoe GE, Peterson A (1971) Structure and chemistry of glucose-producing cells in meningeal tissue of the lamprey. Brain Res 30:99–118
Sievers H, Sievers J, Baumgarten HG, König N, Schlossberger HG (1983) Distribution of tritium label in the neonate rat brain following intracisternal or subcutaneous administration of 3H-6-OHDA. An autoradiographic study. Brain Res 275:23–45
Suarez I, Fernandez B (1983) Structure and ultrastructure of the external glial layer in the hypothalamus of the hamster. J Hirnforsch 24:99–109
Thomas H (1966) Licht- und elektronenmikroskopische Untersuchungen an den weichen Hirnhäuten und den Pacchionischen Granulationen des Menschen. Z Mikrosk Anat Forsch 75:270–327
Virchow R (1851) Über die Erweiterung kleinerer Gefäße. Virchows Arch Pathol Anat 3:427–462
Waggener JD, Beggs J (1967) The membranous coverings of neural tissues: An electron microscopy study. J Neuropathol Exp Neurol 26:412–426
Wagner HJ, Pilgrim C, Brandi J (1974) Penetration and removal of horseradish peroxidase injected into the cerebrospinal fluid. Role of cerebral perivascular spaces, endothelium and microglia. Acta Neuropathol (Berl) 27:299–315
Wagner HJ, Barthel J, Pilgrim C (1983) Permeability of the external glial limiting membrane of rat parietal cortex. Anat Embryol 166:427–437
Weed LH (1923) The absorption of the cerebrospinal fluid into the venous system. Am J Anat 31:191–221
Wolff RJ (1977) Morphology of the extravascular space in brain in comparison to other tissues. 9th Europ Conf Microcirculation Antwerp 1976. Bibl Anat No 15, pp 210–212
Wollam DHM, Millen JW (1954) Perivascular spaces of the mammalian central nervous system. Biol Rev Cambridge Philos Soc 29:251–283
Wright PM, Nogueira GJ, Levin E (1971) Role of the pia mater in the transfer of substances in and out of the cerebrospinal fluid. Exp Brain Res 13:294–305
Zervas NT, Liszczak TM, Mayberg MR, Black PMcL (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
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Supported by the Deutsche Forschungsgemeinschaft (Grant Nr. Kr 569/5) and the Stiftung Volkswagenwerk.
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Krisch, B., Leonhardt, H. & Oksche, A. Compartments and perivascular arrangement of the meninges covering the cerebral cortex of the rat. Cell Tissue Res. 238, 459–474 (1984). https://doi.org/10.1007/BF00219861
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DOI: https://doi.org/10.1007/BF00219861