Summary
An electron-microscopic study has been made of the glial cells in the developing lateral funiculus of the cervical spinal cord in fetal rhesus monkeys. The various macroglial cell types, their precursor cells, and microglia are discussed in detail. An astrocytic lineage is proposed in which glioblasts present in the lateral funiculus give rise to astroblasts that then develop into mature astrocytes. Oligoblasts apparently migrate into the lateral funiculus as such and develop into active oligocytes. The active oligocytes become most predominant during the initial stages of myelinogenesis and are in direct continuity with developing myelin. The active oligocytes develop into mature oligocytes after myelination is completed. Microglia cells are present throughout development as three forms; resting microglia, globose microglia, and active microglia. The globose and active microglia predominates at specific times early in development when degeneration of apparent neuronal processes is taking place. The microglia cells are characterized by dense nuclear chromatin clumps, lipid inclusion bodies, dense vesicles, and, often, intracellular debris.
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References
Blinzinger, K., Kreutzberg, G.: Displacement of synaptic terminals from regenerating motorneurons by microglial cells. Z. Zellforsch. 85, 145–157 (1968).
Blunt, M. J., Baldwin, F., Wendell-Smith, C. P.: Gliogenesis and myelination in kitten optic nerve. Z. Zellforsch. 124, 293–310 (1972).
Bodian, D.: Spontaneous degeneration in the spinal cord of monkey fetuses. Bull. J. Hopk. Hosp. 119, 212–234 (1966).
Caley, D. W., Maxwell, D. S.: An electron microscopic study of the neuroglia during postnatal development of the rat cerebrum. J. comp. Neurol 133, 45–70 (1968).
Hashimoto, P. H.: Gliosome and its relation to astrocytic filaments in cats brain. In: 6th Inter. Congress for Electron Microscopy, Kyoto, (ed. R. Vyeda), vol. 2, p. 467–468. Tokyo: Springer 1966.
Hashimoto, P. H.: Electron microscopic study on gliosome formation in postnatal development of spinal cord in the cat. J. comp. Neurol. 137, 251–266 (1969).
Hildebrand, C.: Ultrastructural and light microscope studies of the developing feline spinal cord white matter. II. Cell death and myelin sheath disintegration in the early postnatal period. Acta physiol. scand., Suppl. 364, 109–144 (1971).
Kershman, J.: Genesis of microglia in the human brain. Arch. Neurol Psychiat. (Chic.) 41, 24–50 (1939).
Kruger, L., Maxwell, D. S.: Electron microscopy of oligodendrocytes in normal rat cerebrum. Amer. J. Anat. 118, 411–436 (1966).
Maxwell, D. S., Kruger, L.: The reactive oligodendrocyte. An electron microscopic study of cerebral cortex following alpha particle irradiation. Amer. J. Anat. 118, 437–460 (1966).
Meller, K., Breipohl, W., Glees, P.: Early cytological differentiation in the cerebral hemisphere of mice. Z. Zellforsch. 75, 525–533 (1966).
Meller, K., Breipohl, W., Glees, P.: The cytology of the developing molecular layer of mouse motor cortex. Z. Zellforsch. 86, 171–183 (1968).
Morales, R., Duncan, D.: Prismatic and other unusual arrays of mitochondrial cristae in astrocytes of cats and hamsters. Anat. Rec. 171, 545–558 (1971).
Mori, S., Leblond, C. P.: Identification of microglia in light and electron microscopy. J. comp. Neurol. 135, 57–80 (1969).
Mori, S., Leblond, C. P.: Electron microscopic identification of three classes of oligodendrocytes and preliminary study of the proliferative activity in the corpus callosum of young rats. J. comp. Neurol. 189, 1–30 (1970).
Mugnaini, E., Walberg, F., Brodal, A.: Mode of termination of primary vestibular fibres in the lateral vestibular nucleus. An experimental electron microscopical study in the cat. Exp. Brain Res. 4, 187–211 (1967).
Penfield, W.: Neuroglia, normal and pathological. In: Cytology and cellular pathology of the nervous system (ed. W. Penfield), vol. 2, p. 421–479. New York: Paul B. Hoeber Inc. 1932.
Peters, A., Paley, S. L., Webster, H.F. de: The fine structure of the nervous system. New York: Harper and Row 1970.
Ramón y Cajal, S.: Études sur la neurogénèse de quelques vertébrés (1929). In trans. by L. Guth as Studies on vertebrate neurogenesis. Springfield, Illinois: Thomas 1960.
Rio-Hortega, P. del: Microglia. In: Cytology and cellular pathology of the nervous system (ed., W. Penfield), vol. 2, p. 483–534. New York: Paul B. Hoeber Inc. 1932.
Skoff, R. P., Vaughn, J. E.: An autoradiographic study of cellular proliferation of degenerating rat optic nerve. J. comp. Neurol. 141, 133–156 (1971).
Smart, I., Leblond, C. P.: Evidence for division and transformations of neuroglia cells in the mouse brain, as derived from radioautography after injection of thymidine-H3. J. comp. Neurol. 116, 349–367 (1961).
Srebro, Z.: The ultrastructure of gliosomes in the brains of amphibia. J. Cell Biol. 26, 313–322 (1965).
Stensaas, L. J., Gilson, B. C.: Ependymal and subependymal cells of the caudo-pallial junction in the lateral ventricle of the neonatal rabbit. Z. Zellforsch. 132, 297–322 (1972).
Stensaas, L. J., Reichert, W. H.: Round and amoeboid microglial cells in the neonatal rabbit brain. Z. Zellforsch. 119, 147–163 (1971).
Stensaas, L. J., Stensaas, S. S.: Astrocytic neuroglial cells, oligodendrocytes and microgliacytes in the spinal cord of the toad. II. Electron microscopy. Z. Zellforsch. 86, 184–213 (1968).
Vaughn, J. E.: An electron microscopic analysis of gliogenesis in rat optic nerves. Z. Zellforsch. 94, 293–324 (1969).
Vaughn, J. E., Hinds, P. L., Skoff, R. P.: Electron microscopic studies of Wallerian degeneration in rat optic nerves. I. The multipotential glia. J. comp. Neurol. 140, 175–206 (1970).
Vaughn, J. E., Peters, A.: Electron microscopy of the early postnatal development of fibrous astrocytes. Amer. J. Anat. 121, 131–152 (1967).
Vaughn, J. E., Peters, A.: A third neuroglial cell type, an electron microscopic study. J. comp. Neurol 133, 269–288 (1968).
Venable, J. H., Coggeshall, R.: A simplified lead citrate stain for use in electron microscopy. J. Cell Biol. 25, 407–408 (1965).
Watson, M. L.: Staining of tissue sections for electron microscopy with heavy metals. J. biophys. biochem. Cytol. 4, 475–578 (1958).
Wechsler, W.: Die Feinstruktur des Neuralrohres und der neuroektodermalen Matrixzellen am Zentralnervensystem von Hühnerembryonen. Z. Zellforsch. 70, 240–268 (1966).
Wechsler, W., Meller, K.: Electron microscopy of neuronal and glial differentiation in the developing brain of the chick. In: Developmental neurology, vol. 26 of Progress in brain research (eds. C. G. Bernhard, J. P. Schadé), p. 93–144. New York: Elsevier Publishing Co. 1967.
Westman, J.: The lateral cervical nucleus in the cat. III. An electron microscopic study after transection of spinal afferents. Exp. Brain Res. 7, 32–50 (1969).
Wong-Riley, M. T. T.: Terminal degeneration and glial reactions in the lateral geniculate nucleus of the squirrel monkey after eye removal. J. comp. Neurol. 144, 61–92 (1972).
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Supported in part by a Parson Trust Endowment Research Grant at the University of South Dakota School of Medicine. The author gratefully acknowledges the help of Dr. Ronald DiGiacomo who was responsible for the surgery involved in the fetal deliveries.
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Phillips, D.E. An electron microscopic study of macroglia and microglia in the lateral funiculus of the developing spinal cord in the fetal monkey. Z.Zellforsch 140, 145–167 (1973). https://doi.org/10.1007/BF00306691
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DOI: https://doi.org/10.1007/BF00306691