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Developmental microvascular architecture of the rat cerebellar cortex

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Summary

External and internal microvascular architectures of the developing rat cerebellar cortex, from embryonic day 18 to postnatal day 14 and in adults, were studied using a cerebrovascular casting method for scanning electron-microscopic observation.

The external vascularization of the developing cerebellum showed the most significant alteration in vascular morphology at the stage of intensive proliferation of matrix cells in the external granular layer (EGL) from birth to postnatal day 4. It consisted of multiple luminal protrusion of the vessels, septum formation in the lumina, and small, ring-like anastomoses. Moreover, at the end of this stage, these structures of the vessels disappeared and the subarachnoid space was filled with newly-formed microvascular networks. Thereafter, architectural change of the developing pial vessels was mainly accomplished by elongation of each contorted vessel of the network. Concerning internal vascularization, a few vessels connected with the pial vessels were observed in the cerebellar plate forming a loose, simple network in the deeper neural parenchyma before the stage of foliation began. During the period of thickening of the EGL, however, there was no alteration in vascularity of the parenchyma other than the architectural changes proportionate to the newly-formed folia. It was during the synaptogenetic stage in the internal granular layer that the earliest intraneural vascular plexuses were formed. The vascular network in the molecular layer was formed after disappearance of the EGL.

These findings suggest that vascular proliferation correlated with EGL-formation pertains to the pial vessels, and not the intraneural ones, which develop after neuronal cell migration in the developing cerebellum has taken place.

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References

  • Altman J (1966) Autoradiographic and histological studies of postnatal neurogenesis. II. A longitudinal investigation of the kinetics, migration and transformation of cells in corporating tritiated thymidine in infant rats, with special reference to postnatal neurogenesis in some brain regions. J Comp Neurol 128:431–474

    Google Scholar 

  • Altman J (1969) Autoradiographic and histological studies of postnatal neurogenesis. III. Dating the time of production and onset of differentiation of cerebellar microneurons in rats. J Comp Neurol 136:269–294

    Google Scholar 

  • Altman J (1972) Postnatal development of the cerebellar cortex in the rat. I. The external germinal layer and the transitional molecular layer. J Comp Neurol 145:353–398

    Google Scholar 

  • Altman J, Bayer SA (1978a) Prenatal development of the cerebellar system in the rat. I. Cytogenesis and histogenesis of the deep nuclei and the cortex of the cerebellum. J Comp Neurol 179:23–48

    Google Scholar 

  • Altman J, Bayer SA (1978b) Prenatal development of the cerebellar system in the rat. II. Cytogenesis and histogenesis of the inferior olive, potine gray, and the precerebellar reticular nuclei. J Comp Neurol 179:49–76

    Google Scholar 

  • Bär T, Wolff JR (1972) The formation of capillary basement membranes during internal vascularization of the rat's cerebellar cortex. Z Zellforsch 133:231–248

    Google Scholar 

  • Caley DW, Maxwell DS (1970) Development of the blood vessels and extracellular spaces during postnatal maturation of rat cerebral cortex. J Comp Neurol 138:31–48

    Google Scholar 

  • Campbell ACP (1939) Variation in vascularity and oxidase content in different regions of the brain of the cat. Arch Neurol Psychiatry 41:223–242

    Google Scholar 

  • Conradi NG, Eins S, Wolff JR (1979) Postnatal vascular growth in the cerebellar cortex of normal and protein-deprived rats. Acta Neuropathol (Berl) 47:131–137

    Google Scholar 

  • Conradi NG, Engvall J, Wolff JR (1980) Angioarchitectonics of rat cerebellar cortex during pre- and postnatal development. Acta Neuropathol (Berl) 50:131–138

    Google Scholar 

  • Craigie EH (1925) Changes in vascularity in the brain stem and cerebellum of the albino rat between birth and maturity. J Comp Neurol 38:27–48

    Google Scholar 

  • Craigie EH (1955) Vascular patterns of the developing nervous system In: (Waelsch H, ed) Biochemistry of the developing nervous system, Academic Press, New York, pp 28–51

    Google Scholar 

  • Das GD, Nornes HO (1972) Neurogenesis in the cerebellum of the rat: An autoradiographic study. Z Anat Entwickl Gesch 138:155–165

    Google Scholar 

  • Del Cerro MP, Snider RS, Oster ML (1968) Evolution of the extracellular space in immature nervous tissue. Experientia 24:929–930

    Google Scholar 

  • Duvernoy HM, Delon S, Vannson JL (1981) Cortical blood vessels of the human brain. Brain Res Bull 7:519–579

    Google Scholar 

  • Duvernoy H, Delon S, Vannson JL (1983) The vascularization of the human cerebellar cortex. Brain Res Bull 11:419–480

    Google Scholar 

  • Fujita S, Shimada M, Nakamura T (1966) H3-thymidine autoradiographic studies on the cell proliferation and differentiation in the external and the internal granular layers of the mouse cerebellum. J Comp Neurol 128:191–208

    Google Scholar 

  • Gillian LA (1969) The arterial and venous blood supplies to the cerebellum of primates. J Neuropathol Exp Neurol 28:295–307

    Google Scholar 

  • Haddara MA, Nooreddin MA (1966) A quantitative study on the postnatal development of the cerebellar vermis of mouse. J Comp Neurol 128:245–254

    Google Scholar 

  • Ikuta F, Yoshida Y, Ohama E, Oyanagi K, Takeda S, Yamazaki K, Watabe K (1983a) Revised pathophysiology on BBB damage. The edema as an ingeniously provided condition for cell motility and lesion repair. Acta Neuropathol [Suppl] (Berl) 8:103–110

    Google Scholar 

  • Ikuta F, Ohama E, Yoshida, Y, Takeda S, Oyanagi K (1983b) Mitosis of the astrocyte in the cerebral lesion: Its significance on the production of reactive astrocytes and lesion-repair. Shinkei Kenkyu no Shinpo (Tokyo) 28:839–856

    Google Scholar 

  • Inoue M, Oda SI (1980) Strain specific variation in the folial pattern of the mouse cerebellum. J Comp Neurol 190:357–362

    Google Scholar 

  • Jacobson M (1978) Developmental neurobiology. 2nd ed., New York, Plenum, pp 76–93

    Google Scholar 

  • Koppel H, Lewis PD, Wigglesworth JS (1982) A study of the vascular supply to the external granular layer of the postnatal rat cerebellum. J Anat 134:73–84

    Google Scholar 

  • Lewis OJ (1957) The form and development of the blood vessels of the mammalian cerebral cortex. J Anat 91:40–46

    Google Scholar 

  • Lierse VW (1963) Über die Beeinflussung der Hirnangioarchitektur durch die Morphogenese. Acta Anat 53:1–54

    Google Scholar 

  • Mareš V, Lodin Z (1970) The cellular kinetics of the mouse cerebellum. II. The function of the external granular layer in the process of gyrification. Brain Res 23:343–352

    Google Scholar 

  • Mareš V, Lodin Z, Šrajer J (1970) The cellular kinetics of the developing mouse cerebellum. I. The generation cycle, growth fraction and rate of proliferation of the external granular layer. Brain Res 23:323–342

    Google Scholar 

  • Mugnaini E, Forstrønen PF (1967) Ultrastructural studies on the cerebellar histogenesis. I. Differentiation of granule cells and development of gromeruli in the chick embryo. Z Zellforsch 77:115–143

    Google Scholar 

  • Padget DH (1948) The development of the cranial arteries in the human embryo. Contrib Embryol 32:205–261

    Google Scholar 

  • Phelps CH (1972) The development of glio-vascular relationships in the rat spinal cord. An electron microscopic study. Z Zellforsch 128:555–563

    Google Scholar 

  • Press MF (1977) Lead enceophalopathy in neonatal Long-Evans rats: Morphologic studies. J Neuropathol Exp Neurol 36:169–195

    Google Scholar 

  • Robain O, Bideau I, Farkas E (1981) Developmental changes of synapses in the cerebellar cortex of the rat. A quantiative analysis. Brain Res 206:1–8

    Google Scholar 

  • Sidman RL, Rakic P (1973) Neuronal migration, with special reference to developing human brain: A review. Brain Res 62:1–35

    Google Scholar 

  • Sievers J, Mangold U, Berry M, Allen C, Schlossberger HG (1981) Experimental studies on cerebellar foliation. I. A qualitative morphological analysis of cerebellar fissuration defects after neonatal treatment with 6-OHDA in the rat. J Comp Neurol 203:751–769

    Google Scholar 

  • Streeter GL (1918) The developmental alterations in the vascular system of the brain of the human embryo. Contrib Embryol 8:5–38

    Google Scholar 

  • Strong LH (1964) The early embryonic pattern of internal vascularization of the mammalian cerebral cortex. J Comp Neurol 123:121–138

    Google Scholar 

  • Vernadakis A, Woodbury DM (1965) Cellular and extracellular spaces in developing rat brain. Radioactive uptake studies with chloride and inulin. Arch Neurol 12:284–293

    Google Scholar 

  • Wolff JR (1978) Ontogenic aspects of cortical architecture: Lamination. In: Architectonics of the cerebral cortex (Brazier MAB, Petsche H eds), Raven Press, New York, pp 159–173

    Google Scholar 

  • Wolff JR, Goerz C, Bär T, Güldner FH (1975) Common morphogenetic aspects of various organotypic microvascular patterns. Microvasc Res 10:373–395

    Google Scholar 

  • Yoshida Y (1983) Stereoscopic vascular morphology in experimental gliomas and its relationship with normal vascularization in the developmental stage. Brain and Nerve (Tokyo), 35:619–627

    Google Scholar 

  • Yoshida Y, Ikuta F (1984) Three-dimensional architecture of cerebral microvessels with a scanning electronmicroscope: A cerebrovascular casting method for fetal and adult rats. J Cereb Blood Flow Metab 4:290–296

    Google Scholar 

  • Yoshida Y, Ikuta F, Nagata T (1981) On the microvascular architecture of the rat cerebellar cortices. In: Ikuta F (ed) Annu Rep Res Committ of “Cerebral Disorders Caused by Hypoenergic and Hypoxic Conditions: Morphological and Chemical Studies”. Ministry of Health and Welfare of Japan, Niigata, 137–155

    Google Scholar 

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Yoshida, Y., Ikuta, F., Watabe, K. et al. Developmental microvascular architecture of the rat cerebellar cortex. Anat Embryol 171, 129–138 (1985). https://doi.org/10.1007/BF00341407

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