Anatomy and Embryology

, Volume 163, Issue 3, pp 331–343 | Cite as

Radial glia in the developing mouse cerebral cortex and hippocampus

  • P. L. Woodhams
  • E. Bascó
  • F. Hajós
  • A. Csillág
  • R. Balázs
Article

Summary

The regional distribution of radial glia in the developing cerebral cortex and the hippocampus of the mouse was studied using silver impregnation and immunocytochemical staining for glial fibrillary acidic protein (GFAP). Whilst the former technique revealed radial fibres at a slightly earlier age, immunocytochemistry gave a better picture of their general distribution and enabled systematic study of the appearance and disappearance of GFAP-positive radial glia throughout the cortex. Although a clear association between migrating neurones and radial glia was evident in the later stages of cortical plate formation, this relationship was not apparent in all cortical regions nor at the very early stages of the formation of the cortical plate. Even after allowing for a delayed appearance of GFAP immunoreactivity in relatively mature radial glia, the uneven distribution of these cells, their appearance after the cortical plate has already been formed, and their regional development in a pattern dissynchronous with that of the cortical plate argue against a general role of these structures in neuronal migration in the mouse, although there are notable phylogenetic differences.

Key words

Cerebral cortex Development Glial fibrillary acidic protein Hippocampus Immunocytochemistry Radial glia 

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References

  1. Altman J (1969) Autoradiographic and histological studies of postnatal neurogenesis III Dating the time of production and onset of differentiation of cerebellar microneurones in rats. J Comp Neurol 136:269–294Google Scholar
  2. Angevine JB, Sidman RL (1962) Autoradiographic study of histogenesis in the cerebral cortex of the mouse. Anat Rec 142:210Google Scholar
  3. Antanitus DW, Choi BH, Lapham LW (1976) The demonstration of glial fibrillary acidic protein in the cerebrum of the human fetus by indirect immunofluorescence. Brain Res 103:613–616Google Scholar
  4. Bartlett PF, Nobel MD, Pruss RM, Raff MC, Rattray S, Williams CA (1981) Rat neural antigen-2 (RAN-2): a cell surface antigen on astrocytes, ependymal cells, Müller cells and lepto-meninges defined by monoclonal antibody. Brain Res 204:339–351Google Scholar
  5. Bascó E, Hajós F, Fülöp Z (1977) Proliferation of Bergmann-glia in the developing rat cerebellum. Anat Embryol 151:219–222Google Scholar
  6. Bascó E, Woodhams PL, Hajós F, Balázs R (1981) Immunocytochemical demonstration of glial fibrillary acidic protein in mouse tanycytes. Anat Embryol 162:217–222Google Scholar
  7. Bayer SA (1980) Development of the hippocampal region in the rat. II Morphogenesis during embryonic and early postnatal life. J Comp Neurol 190:115–134Google Scholar
  8. Bayer S, Altman J (1974) Hippocampal development in the rat: cytogenesis and morphogenesis examined with autoradiography and low-level X-irradiation. J Comp Neurol 158:55–80Google Scholar
  9. Bignami A, Dahl D (1973) Differentiation of astrocytes in the cerebral cortex and the pyramidal tracts of the newborn rat: An immunofluorescence study with antibodies to a protein specific to astrocytes. Brain Res 49:393–402Google Scholar
  10. Bignami A, Dahl D (1974a) Astrocyte-specific protein and radial glia in the cerebral cortex of new-born rat. Nature (Lond.) 252:55–56Google Scholar
  11. Bignami A, Dahl D (1974) Astrocyte-specific protein and nueroglial differentiation: An immunofluorescence study with antibodies to the glial fibrillary acidic protein. J Comp Neurol 153:27–38Google Scholar
  12. Caviness VS, Pinto-Lord MC, Everard P (1981) The development of laminated pattern in the mammalian neocortex. In: TG Connelly, LL Brinkley, BM Carlson (eds). Morphogenesis and pattern formation. Raven Press, New York, pp 103–126Google Scholar
  13. Chiu F-C, Norton WT, Fields KL (1981) The cytoskeleton of primary astrocytes in culture contains actin, glial fibrillary acidic protein, and the fibroblast-type filament protein, vimentin. J Neurochem 37:147–155Google Scholar
  14. Choi B, Lapham L (1978) Radial glia in the human fetal cerebrum: A combined Golgi, immunofluorescent and electron microscopic study. Brain Res 148:295–311Google Scholar
  15. Choi B, Lapham L (1980) Evolution of Bergmann glia in developing human fetal cerebellum: a Golgi, electron microscopic and immunofluorescent study. Brain Res 190:369–383Google Scholar
  16. Dahl D, Rueger DC, Bignami A, Weber K, Osborn M (1981) Vimentin, the 57,000 dalton protein of fiboblast filaments, is a major cyto-skeletal component in immature glia. Eur J Cell Biol (in press)Google Scholar
  17. Del Cerro M, Swarz J (1976) Prenatal development of Bergmann-glial fibres in rodent cerebellum. J Neurocytol 5:699–676Google Scholar
  18. Fleischhauer K (1972) Ependyma and subependymal layer. In: GH Bourne (ed) The structure and functions of nervous tissue VI. Academic Press, New York/London, pp 1–46Google Scholar
  19. Garber BB, Huttenlocher PR, Larramendi LHM (1980) Self assembly of cortical plate cells in vitro within mouse cerebral aggregates. Golgi and electron microscopic analysis. Brain Res 201:255–278Google Scholar
  20. Golgi C (1885) Sulla fina anatomia degli organi centrali del sistema nervoso. Republished in: Opera Omnia, Hoepli, Milan, 1903, pp 397–536Google Scholar
  21. Hajós F, Woodhams PL, Bascó E, Csillág A, Balázs R (1981) Proliferation of astroglia in the embryonic mouse forebrain as revealed by stimultaneous immunocytochemistry and autoradiography. Acta Morphol Hung (in press)Google Scholar
  22. His W (1904) Die Entwicklung des menschlichen Gehirns während der ersten Monate. S Hirzel, LeipzigGoogle Scholar
  23. Horstmann ED (1954) Die Faserglia des Selachiergerhirns. Z Zellforsch 39:588–617Google Scholar
  24. Jacobson M (1978) Developmental Neurobiology. Plenum Press, New York/LondonGoogle Scholar
  25. Langenaur C, Sommer I, Schachner M (1980) Subclass of astroglia in mouse cerebellum recognised by monoclonal antibody. Dev Biol 79:377–378Google Scholar
  26. Lenhossék MV (1991) Zur Kenntnis der ersten Entstehung der Nervenzellen und Nervenfasern beim Vogelembryo. Verh X Internat Med Cong Berl Abth 2:115–124Google Scholar
  27. Levitt P, Rakic P (1980) Immunoperoxidase localization of glial fibrillary acidic protein in radial glial cells and astrocytes of developing rhesus monkey brain. J Comp Neurol 193:815–840Google Scholar
  28. Levitt P, Cooper ML, Rakic P (1981) Coexistence of neuronal and glial precursor cells in the cerebral ventricular zone of the foetal monkey: an ultrastructural immunoperoxidase analysis. J Neurosci 1:27–39Google Scholar
  29. Ludwin SK, Kosek JC, Eng LF (1976) The topographical distribution of S-100 and GFA proteins in the adult rat brain: an immunohistochemical study using horseradish peroxidase-labelled antibodies. J Comp Neurol 165:97–208Google Scholar
  30. Magini G (1888a) Sur la nevroglie et les cellules nerveuses cerebrales chez les foetus. Arch Ital Biol 9:59–60Google Scholar
  31. Magini G (1888b) Nouvelles recherches histologiques sur le cerveau du foetus. Arch Ital Biol 10:383–387Google Scholar
  32. Morest DK (1970) A study of neurogenesis in the forebrain of oppossum pouch young. Z Anat Entwickl Gesch 130:265–305Google Scholar
  33. Nowakowski RS, Rakic P (1979) The mode of migration of neurones to the hippocampus: a Golgi and electron microscopic analysis in foetal rhesus monkey. J Neurocytol 8:697–718Google Scholar
  34. Palay S, Chan-Palay V (1974) Rapid Golgi method-multiple impregnation process. In: Cerebellar cortex. Cytology and organization. Springer-Verlag, Berlin/Heidelberg/New York, p 333Google Scholar
  35. Peters A, Feldman M (1973) The cortical plate and molecular layer of the late rat fetus. Z Anat Entwickl-Gesch 141:3–37Google Scholar
  36. Raedler E, Raedler A (1978) Autoradiographic study of early neurogenesis in rat neocortex. Anat Embryol 154:267–284Google Scholar
  37. Rakic P (1971a) Guidance of neurones migrating to the fetal monkey neocortex. Brain Res 33:471–476Google Scholar
  38. Rakic P (1971b) Neuron-glia relationship during granule cell migration in the developing cerebellar cortex. A Golgi and electron microscopic study in macacus rhesus. J Comp Neurol 141:283–312Google Scholar
  39. Rakic P (1972) Mode of cell migration to the superficial layers of fetal monkey neocortex. J Comp Neurol 145:61–84Google Scholar
  40. Ramon Y, Cajal S (1911) Histologie du systeme nerveux de l'homme et des vertebres, tome 2 Paris Maloine, Reprinted by Consejo Superior de Investigaciones Cientificas, Madrid (1955)Google Scholar
  41. Retzius G (1893) Studien über Ependym and Neuroglia. Biol Untersuch Stockholm 5:9–26Google Scholar
  42. Retzius G (1894) Die Neuroglia des Gehirns beim Menschen und die Saugenthiern. Biol Untersuch Stockholm 6:1–24Google Scholar
  43. Roessmann U, Velasco ME, Sindley SD, Gambetti P (1980) Glial fibrillary acidic protein (GFAP) in ependymal cells during development. An immunocytochemical study. Brain Res 200:13–21Google Scholar
  44. Schimrigk K (1966) Über die Wandstruktur der Seitenventrikel und des dritten Ventrikels beim Menschen. Z Zellforsch Mikrosk Anat 70:1–20Google Scholar
  45. Schlessinger A, Cowan WM, Gottlieb D (1975) An autoradiographic study of the time of origin and pattern of granule cell migration in the dentate gyrus of the rat. J Comp Neurol 159:149–152Google Scholar
  46. Schmechel D, Rakic P (1979) A Golgi study of glial cells in developing monkey telencephalon: Morphogenesis and transformation into astrocytes. Anat Embryol 156:115–152Google Scholar
  47. Shoukimas GM, Hinds JW (1978) The development of the cerebral cortex in the embryonic mouse: an electron microscopic serial section analysis. J Comp Neurol 179:795–835Google Scholar
  48. Sidman RL, Rakic P (1973) Neuronal migration, with special reference to developing human brain: a review. Brain Res 62:1–35Google Scholar
  49. Smart I (1961) The subependymal layer of the mouse brain and its cell production as shown by radioautography after Thymidine-H3 injection. J Comp Neurol 116:325–348Google Scholar
  50. Smart I, Leblond CP (1961) Evidence for division and transformation of neuroglia cells in the mouse brain, as derived from radioautography after injection of Thymidine-H3. J Comp Neurol 116:349–368Google Scholar
  51. Swarz J, Oster-Granite ML (1978) Presence of radial glia in foetal mouse cerebellum. J Neurocytol 7:301–312PubMedGoogle Scholar
  52. Woodhams PL, Cohen J, Mallet J, Balázs R (1980) A preparation enriched in Purkinje cells identified by morphological immunocytochemical criteria. Brain Res 199:435–442CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 1981

Authors and Affiliations

  • P. L. Woodhams
    • 1
  • E. Bascó
    • 2
  • F. Hajós
    • 2
  • A. Csillág
    • 2
  • R. Balázs
    • 1
  1. 1.MRC Developmental Neurobiology UnitInstitute of NeurologyLondonUK
  2. 2.1st Department AnatomySemmelweis University Medical SchoolBudapestHungary

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