Summary
The shape and fine structure of ventricular (primitive ependymal) cells during their generation cycle was studied. Interphase cells are radially oriented bipolar elements with processes spanning the thickness of the brain wall. Zonular junctional complexes joining internal processes at the ventricle consist of gap junctions and wider intermediate junctions. The external limiting layer consists of expanded end-feet in simple apposition; they resemble axonal growth cones and contain a feltwork of 60 Å microfilaments, elements of smooth endoplasmic reticulum but no microtubules. During prophase, nuclei of ventricular cells move to a juxtaventricular position, while their external processes remain fully extended. The internal processes of such cells contain numerous longitudinally arranged microtubules and microfilaments. Subsequent to nuclear migration, in prometaphase or metaphase, the cell withdraws or pinches off its external process and becomes nearly spherical. During telophase an asymmetrical furrow formation results in a thin connector (midbody) between daughter cells which is adjacent to the ventricle and attached there by the junctional complex. Either before or after complete separation, an external process starts regrowing towards the external limiting layer, eventually resulting in a bipolar interphase cell again. Microfilaments are present in telophase cells before outgrowth of external processes and in growing tips of external processes.
References
Allenspach, A. L., Roth, L. E.: Structural variations during mitosis in the chick embryo. J. Cell Biol. 33, 179–196 (1967).
Angevine, J. B., Jr., Sidman, R. L.: Autoradiographic study of cell migration during histogenesis of cerebral cortex in the mouse. Nature (Lond.) 192, 766–768 (1961).
— —: Autoradiographic study of histogenesis in the cerebral cortex of the mouse. Anat. Rec. 142, 210 (1962).
Bennett, M. V. L., Pappas, G. D., Giménez, M., Nakajima, Y.: Physiology and ultrastructure of electrotonic junctions. IV. Medullary electromotor nuclei in Gymnotid fish. J. Neurophysiol. 30, 236–300 (1967).
Berry, M., Rogers, A. W.: The migration of neuroblasts in the developing cerebral cortex. J. Anat. (Lond.) 99, 691–709 (1965).
Boulder Committee: Embryonic vertebrate central nervous system: revised terminology. Anat. Rec. 166, 257–262 (1970).
Brightman, M. W., Reese, T. S.: Junctions between intimately apposed cell membranes in the vertebrate brain. J. Cell Biol. 40, 648–677 (1969).
Brinkley, B. R., Stubblefield, E., Hsu, T. C.: The effects of Colcemid inhibition and reversal on the fine structure of the mitotic appartus of Chinese hamster cells in vitro. J. Ultrastruct. Res. 19, 1–18 (1967).
Buckley, I. K., Porter, K. R.: Cytoplasmic fibrils in living cultured cells. A light and electron microscope study. Protoplasma (Wien) 64, 349–380 (1967).
Caley, D. W., Maxwell, D. S.: Development of the blood vessels and extracellular spaces during postnatal maturation of rat cerebral cortex. J. comp. Neurol. 138, 31–18 (1970).
Cloney, R. A.: Cytoplasmic filaments and morphogenesis: the role of the notochord in ascidian metamorphosis. Z. Zellforsch. 100, 31–53 (1969).
Cobb, J. L. S., Bennett, T.: An ultrastructural study of mitotic division in differentiated gastric smooth muscle cells. Z. Zellforsch. 108, 177–189 (1970).
Del Cerro, M. P., Snider, R., Oster, M. L.: Evolution of the extracellular space in immature nervous tissue. Experientia (Basel) 24, 929–930 (1968).
Duckett, S.: The germinal layer of the growing human brain during early fetal life. Anat. Rec. 161, 231–246 (1968).
Duncan, D.: Electron microscope study of the embryonic neural tube and notochord. Tex. Rep. Biol. Med. 15, 367–377 (1957).
Farquhar, M. G., Palade, G. E.: Junctional complexes in various epithelia. J. Cell Biol. 17, 375–412 (1963).
Flickinger, C. J.: The fine structure and development of the seminal vesicle and prostate in the fetal rat. Z. Zellforsch. 109, 1–14 (1970).
Fujita, S.: The matrix cell and cytogenesis in the developing central nervous system. J. comp. Neurol. 120, 37–42 (1963).
Herman, L., Kauffman, S. L.: The fine structure of the embryonic mouse neural tube with special reference to cytoplasmic microtubules. Develop. Biol. 13, 145–162 (1966).
Hicks, S. P., D'Amato, C. J.: Cell migration to the isocortex in the rat. Anat. Rec. 160, 619–634 (1968).
Hinds, J. W.: Autoradiographic study of histogenesis in the mouse olfactory bulb. Ph. D. Thesis, Harvard University, Cambridge, Mass. 1967.
—: Autoradiographic study of histogenesis in the mouse olfactory bulb. I. Time of origin of neurons and neuroglia. J. comp. Neurol. 134, 287–304 (1968a).
—: Autoradiographic study of histogenesis in the mouse olfactory bulb. II. Cell proliferation and migration. J. comp. Neurol. 134, 305–322 (1968b).
—, Angevine, J. B., Jr.: Autoradiographic study of histogenesis in the area pyriformis and claustrum in the mouse. Anat. Rec. 151, 456–457 (1965).
His, W.: Die Neuroblasten und deren Entstehung im embryonalen Mark. Arch. Anat. Physiol., Anat. Abt. 1889, 249–300 (1889).
Ishikawa, H., Bischoff, R., Holtzer, H.: Formation of arrowhead complexes with heavy meromyosin in a variety of cell types. J. Cell Biol. 43, 312–328 (1969).
Kershman, J.: The medulloblast and the medulloblastoma. A study of human embryos. Arch. Neurol. Psychiat. (Chic.) 40, 937–967 (1938).
Langman, J.: Histogenesis of the central nervous system. In: The structure and function of nervous tissue, vol. I, p. 33–66 (G. H. Bourne, ed.). New York: Academic 1968.
—, Guerrant, R. L., Freeman, B. G.: Behavior of neuro-epithelial cells during closure of the neural tube. J. comp. Neurol. 127, 399–411 (1966).
Lyser, K. M.: Early differentiation of motor neuroblasts in the chick embryo as studied by electron microscopy. I. General aspects. Develop. Biol. 10, 433–466 (1964).
—: Early differentiation of motor neuroblasts in the chick embryo as studied by electron microscopy. II. Microtubules and neurofilaments. Develop. Biol. 17, 117–142 (1968).
Manasek, F. J.: Mitosis in developing cardiac muscle. J. Cell Biol. 37, 191–196 (1968).
Mark, G. E., Strasser, F. F.: Pacemaker activity and mitosis in cultures of newborn rat heart ventricle cells. Exp. Cell Res. 44, 217–233 (1966).
Martin, A. H.: Significance of mitotic spindle fibre orientation in the neural tube. Nature (Lond.) 216, 1133–1134 (1967).
Mazia, D.: Mitosis and the physiology of cell division. In: The cell, vol. III, p. 77–412 (J. Brächet and A. E. Mirsky, eds.). New York: Academic 1961.
Morest, D. K.: Growth of cerebral dendrites and synapses. Anat. Rec. 160, 516 (1968a).
—: The growth of synaptic endings in the mammalian brain: a study of the calyces of the trapezoid body. Z. Anat. Entwickl.-Gesch. 127, 201–220 (1968b).
—: The differentiation of cerebral dendrites: a study of the post-migratory neuroblast in the medial nucleus of the trapezoid body. Z. Anat. Entwickl.-Gesch. 128, 271–289 (1969a).
—: The growth of dendrites in the mammalian brain. Z. Anat. Entwickl.-Gesch. 128, 290–317 (1969b).
—: A study of neurogenesis in the forebrain of opossum pouch young. Z. Anat. Entwickl.-Gesch. 130, 265–305 (1970a).
—: The pattern of neurogenesis in the retina of the rat. Z. Anat. Entwickl.-Gesch. 131, 45–67 (1970b).
—, Morest, R. R.: Perfusion-fixation of the brain with chrome-osmium solutions for the rapid Golgi method. Amer. J. Anat. 118, 811–832 (1966).
Murray, R. G., Murray, A. S., Pizzo, A.: The fine structure of mitosis in rat thymic lymphocytes. J. Cell Biol. 26, 601–620 (1965).
Nanney, D. L., Rudzinska, M. A.: Protozoa. In: The cell, vol. IV, p. 109–150 (J. Brachet and A. E. Mirsky, eds.). New York: Academic 1960.
Payton, B. W., Bennett, M. V. L., Pappas, G. D.: Permeability and structure of junctional membranes at an electrotonic synapse. Science 166, 1641–1643 (1969).
Pearce, T. L., Zwaan, J.: A light and electron microscopic study of cell behavior and microtubules in the embryonic chicken lens using Colcemid. J. Embryol. exp. Morph. 23, 491–507 (1970).
Peters, A., Palay, S. L., Webster, H. de F.: The fine structure of the nervous system. New York: Harper and Row 1970.
Pomerat, C. M.: Rotating nuclei in tissue cultures of adult human nasal mucosa. Exp. Cell Res. 5, 191–196 (1953).
Potter, D. D., Furshpan, E. J., Lennox, E. S.: Connection between cells of the developing squid as revealed by electrophysiological methods. Proc. nat. Acad. Sci. (Wash.) 55, 328–336 (1966).
Pysh, J. J.: Development of the extracellular space in rat inferior colliculus. Anat. Rec. 157, 304 (1967).
Ramón y Cajal, S.: Histologie du système nerveux de l'homme et des vertébrés, vol. I (1952 reprint). Madrid: Instituto Ramón y Cajal 1909.
Revel, J. P., Karnovsky, M. J.: Hexagonal array of subunits in intercellular junctions of the mouse heart and liver. J. Cell Biol. 33, C7-C12 (1967).
Robbing, E., Gonatas, N. K.: The ultrastructure of a mammalian cell during the mitotic cycle. J. Cell Biol. 21, 429–64 (1964).
Sauer, F. C.: Mitosis in the neural tube. J. comp. Neurol. 62, 377–405 (1935).
—: The interkinetic migration of embryonic epithelial nuclei. J. Morph. 60, 1–11 (1936).
—: Some factors in the morphogenesis of vertebrate embryonic epithelia. J. Morph. 61, 563–579 (1937).
Sauer, M. E., Walker, B. E.: Radioautographic study of interkinetic nuclear migration in the neural tube. Proc. Soc. exp. Biol. (N.Y.) 101, 557–560 (1959).
Scharff, M. D., Robbins, E.: Polyribosome disaggregation during metaphase. Science 151, 992–995 (1966).
Schroeder, T. E.: Neurulation in Xenopus laevis. An analysis and model based upon light and electron microscopy. J. Embryol. exp. Morph. 23, 427–462 (1970).
Scott, D. G., Daniel, C. W.: Filaments in the division furrow of mouse mammary cells. J. Cell Biol. 45, 461–466 (1970).
Sechrist, J. W.: Neurocytogenesis. I. Neurofibrils, neurofilaments, and the terminal mitotic cycle. Amer. J. Anat. 124, 117–134 (1969).
Sheffield, J. B., Fischman, D. A.: Intercellular junctions in the developing neural retina of the chick embryo. Z. Zellforsch. 104, 405–418 (1970).
Sheridan, J. D.: Electrophysiological evidence for low-resistance intercellular junctions in the early chick embryo. J. Cell Biol. 37, 650–659 (1968).
Shimada, M., Langman, J.: Cell proliferation, migration and differentiation in the cerebral cortex of the golden hamster. J. comp. Neurol. 139, 227–244 (1970).
Sidman, R. L., Miale, I. L., Feder, N.: Cell proliferation and migration in the primitive ependymal zone; an autoradiographic study of histogenesis in the nervous system. Exp. Neurol. 1, 322–333 (1959).
Smart, I.: The subependymal layer of the mouse brain and its cell production as shown by radioautography after thymidine-H3 injection. J. comp. Neurol. 116, 325–347 (1961).
Snider, P. J.: Nuclear movements in Schizophyllum. Symp. Soc. exp. Biol. 22, 261–284 (1968).
Sotelo, C., Palay, S. L.: The fine structure of the lateral vestibular nucleus in the rat. II. Synaptic organization. Brain Res. 18, 93–115 (1970).
Spooner, B. S., Wessells, N. K.: Effects of cytochalsin B upon microfilaments involved in morphogenesis of salivary epithelium. Proc. nat. Acad. Sci. (Wash.) 66, 360–364 (1970).
Stensaas, L. J., Stensaas, S. S.: An electron microscope study of cells in the matrix and intermediate laminae of the cerebral hemisphere of the 45 mm rabbit embryo. Z. Zellforsch. 91, 341–365 (1968).
Sumi, S. M.: The extracellular space in the developing rat brain: its variation with changes in osmolarity of the fixative, method of fixation and maturation. J. Ultrastruct. Res. 29, 398–425 (1969).
Tennyson, V. M.: Electron microscopic observation of the development of the neuroblast in the rabbit embryo. In: Proc. Fifth International Congr. for Electron Microscopy, vol. 2, p. N8. New York: Academic 1962.
—: The fine structure of the axon and growth cone of the dorsal root neuroblast of the rabbit embryo. J. Cell Biol. 44, 62–79 (1970).
Tilney, L. G., Gibbins, J. R.: Microtubules and filaments in the filopodia of the secondary mesenchyme cells of Arbacia punctulata and Echinarachnius parma. J. Cell Sci. 5, 195–210 (1969).
Trelstad, R. L., Hay, E. D., Revel, J. P.: Cell contact during early morphogenesis in the chick embryo. Develop. Biol. 16, 78–106 (1967).
Venable, J. H., Coggeshall, R.: A simplified lead citrate stain for use in electron microscopy. J. Cell Biol. 25, 407–408 (1965).
Watterson, R. L.: Structure and mitotic behavior of the early neural tube. In: Organogenesis, p. 129–160 (R. L. De Haan and H. Ursprung, eds.). New York: Holt, Rinehart, and Winston, 1965.
Weidman, T. A., Kuwabara, T.: Postnatal development of the rat retina. An electron microscopic study Arch. Ophthal. 79, 470–484 (1968).
Woodard, T. M., Jr., Estes, S. B.: Effect of colchicine on mitosis in the neural tube of the forty-eight hour chick embryo. Anat. Rec. 90, 51–54 (1944).
Wrenn, J. T., Wessels, N. K.: Cytochalasin B: effect upon microfilaments involved in morphogenesis of estrogen-induced glands of oviduct. Proc. nat. Acad. Sci. (Wash.) 66, 904–908 (1970).
Yamada, K. M., Spooner, B. S., Wessells, N. K.: Axon growth: roles of microfilaments and microtubules. Proc. nat. Acad. Sci. (Wash.) 66, 1206–1212 (1970).
Zwaan, J., Bryan, P. R., Pearce, T. L.: Interkinetic nuclear migration during the early stage of lens formation in the chicken embryo. J. Embryol. exp. Morph. 21, 71–83 (1969).
Author information
Authors and Affiliations
Additional information
This work was supported by United States Public Health Service Research Grant No. NS-08655 from the National Institutes of Neurological Diseases and Stroke. The authors wish to express their sincere thanks to Drs. Peters, Morest, and Grasso for their critical reading of the manuscript and to Patricia Lowary Hinds for the drawing in this paper.
Rights and permissions
About this article
Cite this article
Hinds, J.W., Ruffett, T.L. Cell proliferation in the neural tube: An electron microscopic and Golgi analysis in the mouse cerebral vesicle. Z. Zellforsch. 115, 226–264 (1971). https://doi.org/10.1007/BF00391127
Received:
Issue Date:
DOI: https://doi.org/10.1007/BF00391127