Summary
The meninges of albino Wistar rat embryos, aged between the 11th embryonic day (ED) and birth, were sectioned using a specially constructed device. This technique permits optimal microanatomical preservation of all tissues covering the convexity of the brain: skin, muscle, cartilage or bone, and the meninges. At ED11, the zone situated between the epidermis and the brain is occupied by a mesenchymal network. At ED12, part of this delicate network develops as a dense outer cellular layer, while the remainder retains its reticular appearance, thus forming an inner layer (the future meningeal tissue). At ED13, the dura mater starts to differentiate. At ED14, the bony anlage of the skull can be identified, and along with the proceeding maturation of dura mater some fibrillar structures resembling skeletal muscle fibers appear in the developing arachnoid space. At ED15–17, a primitive interface zone — dura mater/ arachnoid — is formed, comprised by an outer electronlucent and an inner electron-dense layer marking the outer aspect of the arachnoidal space. At ED18–19, the innermost cellular row of the inner durai layer transforms into neurothelium, which is separated from the darker arachnoidal cells by an electron-dense band. The arachnoidal trabecular zone with the leptomeningeal cells is formed at ED19. By the end of the prenatal period (ED20–21), its innermost part organizes into an inner arachnoidal layer and an outer and inner pial layer. The results from this study indicate (i) that dura mater and leptomeninges develop from an embryonic network of connective tissue-forming cells, and (ii) that the formation of cerebrospinal fluid (CSF)-containing spaces accompanies the differentiation of the meningeal cellular layers.
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
Anderson DR (1969) Ultrastructure of the meningeal sheaths. Arch Ophthalmol 82:659–674
Booz KH (1976) Ependymsekretion im III. Ventrikel der embryonalen Ratte. Verb Anat Ges 70:997–1002
Booz KH, Feising T (1973) Über ein transitorisches, perinatales subependymales Zellsystem der weißen Ratte. Z Anat Entwicklungsgesch 141:275–288
Brightman MW (1977) Morphology of the blood-brain interfaces. Exp Eye Res [Suppl] 25:1–25
Cohen AM, Hay ED (1971) Secretion of collagen by embryonic neuroepithelium at the time of spinal cord — somite interaction. Dev Biol 26:578–605
Conly JM, Ronald AR (1983) CSF as a diagnostic body fluid. Am J Med 28:102–108
Conrad GW, Dessau W, von der Mark K (1980) Synthesis of type III collagen by fibroblasts from the embryonic chick cornea. J Cell Biol 84:501–512
Dermietzel R (1975) Junctions in the central nervous system of the cat. 5. The junctional complex of the pia-arachnoid membrane. Cell Tissue Res 164:309–329
Diehl JM (1978) Occurrence and regional distribution of striated muscle fibers in the rat pineal gland. Cell Tissue Res 190:349–355
Dodson JW, Hay ED (1971) Secretion of collagenous stroma by isolated epithelium grown in vitro. Exp Cell Res 65:215–220
Farrer CB (1907) The embryonic pia. Am J Insan 63:295–299
Fliedner TM, Calvo W (1978) Hematopoietic stem-cell seeding of a cellular matrix: a principle of initiation and regeneration of hematopoiesis. In: Clarkson B, Marks PA, Till JE (eds) Differentiation of normal and neoplastic hematopoietic cells. Cold Spring Harbor Laboratory, pp 757–773
Green HG, Goldberg B, Schwartz M, Brown DD (1968) The synthesis of collagen during the development of Xenopus laevis. Dev Biol 18:391–400
Hall BK (1978) Development and cellular skeletal biology. Academic Press, New York San Francisco London, pp 26–36
Harvey SC, Burr HS (1926) The development of the meninges. Arch Neurol Psychiat 15:545–567
Hay ED (1980) Development of the vertebrate cornea. Int Rev Cytol 63:263–322
Hay ED (1981) Collagen and embryonic development. In: Hay ED (ed) Cell Biology of the Extracellular Matrix, Plenum Publishing Corporation, New York, pp 379–409
Hay ED, Dodson JW (1973) Secretion of collagen by corneal epithelium. I. Morphology of the collagenous products produced by isolated epithelia grown on frozen-killed lense. J Cell Biol 57:190–213
Johnston MC (1966) A radioautographic study of the migration and fate of cranial neural crest cells in the chick embryo. Anat Rec 156:143–156
Kelly AM, Zacks SI (1969) The histogenesis of rat intercostal muscle. J Cell Biol 42:135–153
Klika E (1968) L'ultrastructure des meninges en ontogenese de l'homme. Z Mikrosk Anat Forsch 79:209–222
Klika E, Zajicova A (1972) Differentiation of the meninges in the ontogenesis of Rana temporaria L. Folia Morphol (Praha) 20:60–62
Klika E, Zajicova A (1976) The development of the meninges in chicken embryos. Anat Anz 140:379–386
Krahn V (1982) The pia mater at the site of entry of blood vessels into CNS. Anat Embryol 164:257–263
Krisch B (1986) The functional and structural borders between the CSF- and blood-dominated milieus in the choroid plexuses and the area postrema of the rat. Cell Tissue Res 245:101–115
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 (1983) The meningeal compartments of the median eminence and the cortex. A comparative analysis in the rat. Cell Tissue Res 228:597–640
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
Lash JW, Ostrovsky D, Mittal B, Sanger JW (1985) Alpha actinin distribution and extracellular matrix products during somatogenesis and neurolation in the chick embryo. Cell Motil 5:491–506
Lear M, Harvey SC (1924) The regeneration of the meninges. Ann Surg 80:536–544
Leu HJ (1973) Histologische Altersbestimmung von arteriellen und venösen Thromben und Emboli. VASA 2:265–274
Lipow K, Horoupian DS, Raine CS (1978) On the occurrence of striated muscle within the spinal leptomeninges. Muscle Nerve 1:322–329
Manasek FJ (1975) The extracellular matrix: a dynamic component of the developing embryo. Curr Top Dev Biol 10:35–102
McLone DG, Bondareff W (1975) Developmental morphology of the subarachnoid space and contiguous structures in the mouse. Am J Anat 142:273–294
Millen JW, Woollam DHM (1961) Observations of the nature of pia mater. Brain 84:514–520
Mitro A, Schiebler TH (1972) Über die Entwicklung regionaler Unterschiede im Ependym des 3. Ventrikels der Ratte. Anat Anz 132:1–9
Nabeshima S, Reese TS, Landis D, Brightman MW (1975) Junctions in the meninges and marginal glia. J Comp Neurol 164:127–170
Pease DC, Schultz RL (1958) Electron microscopy of rat cranial meninges. Am J Anat 102:301–321
Raine CS, Horoupian D (1980) Skeletal muscle within the spinal leptomeninges of the mouse. Muscle Nerve 3:187
Sayad WY, Harvey SC (1923) The regeneration of the meninges. Ann Surg 77:129–141
Schachenmayr W (1967) Über die Entwicklung von Ependym und Plexus chorioideus der Ratte. Z Zellforsch Mikrosk Anat 77:25–63
Shabo AL, Maxwell DS (1971) The subarachnoid space following the introduction of a foreign protein: an electron microscopic study with peroxidase. J Neuropathol Exp Neurol 30:506–524
Spatz H (1934) Die Bedeutung der vitalen Färbung für die Lehre vom Stoffaustausch zwischen dem ZNS und dem übrigen Körper. Das morphologische Substrat der Stoffwechselschranken im Zentralorgan. Arch Psychiatr 101:267–358
Spooner BS, Faubian JM (1980) Collagen involvement in branching morphogenesis of embryonic lung and salivary gland. Dev Biol 77:84–102
Sterzi G (1901) Ricerche intorno all' anatomia comparata al lóntogenesi delle meningi e considerazioni sulla fillogenesi. (Part II.) Atti Ist Veneto Sci 60:1101–1372
Tyler MS (1983) Development of frontal bone and cranial meninges in the chick. An experimental study of tissue interactions. Anat Rec 206:61–70
Waggener JD, Beggs J (1967) The membranous coverings of the nervous tissues. An electron microscopic study. J Neuropathol Exp Neurol 26:412–426
Weed LH (1916) The formation of the cranial subarachnoid spaces. Anat Rec 10:475–481
Weston JA (1970) The migration and differentiation of neural crest cells. In: Abercombie M, Brachet J, King TJ (eds) Advances in Morphogenesis, Academic Press, New York, pp 41–114
Zajicova A (1980) Electron microscopic study of the development of the meninges in Mus musculus f. alba. Folia Morphol (Prag) 28:389–392
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Angelov, D.N., Vasilev, V.A. Morphogenesis of rat cranial meninges. Cell Tissue Res. 257, 207–216 (1989). https://doi.org/10.1007/BF00221652
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00221652