Summary
In the suboptic necrotic centres (SONCs) of the chick embryo diencephalon floor, large numbers of cells die in Hamburger and Hamilton's (HH) developmental stages 14–23. Until recently, it was thought that in these centres, the fragments of dead cells were phagocytosed exclusively by neighboring healthy cells but not by specialized macrophages. We now report morphological evidence of macrophage-like cells within the SONCs of the chick embryo. The distinctive features of these cells are their more or less spherical shape, a nucleus with a thin band of heterochromatin just beneath the nuclear envelope, and cytoplasm showing abundant digestive vacuoles and mitochondria with an electron-lucent matrix. These cells are capable of undergoing mitosis, and selectively stain with the histochemical technique for acid phosphatase. The macrophage-like cells are rare in SONCs in stages HH14-20 and become much more abundant in developmental stages just before the disappearance of these necrotic centres, suggesting that they phagocytose debris from the last cells to die in the SONCs. Acid phosphatase-positive mesenchymal cells with morphological features similar to those of macrophage-like cells are seen in intimate relationship with the basal surface of the SONCs in places where the basal lamina is sometimes missing. These observations suggest that macrophage-like cells in the SONCs arise from the underlying mesenchyme.
Free macrophage-like cells with mitotic capacity are also seen in the ventricular lumen adjacent to the apical surface of the diencephalon floor in zones related to the presumptive optic pathways. These cells phagocytose cell debris shed from both the SONCs and from the partially disorganized areas in the neuroepithelium. In these latter we have identified mesenchymal cells with morphological features similar to the macrophage-like cells in the process of traversing the neuroepithelium from the mesenchymal compartment toward the ventricular lumen, thus suggesting that the intraventricular macrophage-like cells arise from the mesenchyme underlying the diencephalon floor.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Ashwell, K. W. S., Holländer, H., Streit, W. &Stone, J. (1989) The appearance and distribution of microglia in the developing retina of the rat.Visual Neuroscience 2, 437–48.
Beaulation, J. &Lockshin, R. A. (1982) The relation of programmed cell death to development and reproduction: comparative studies and an attempt at classification.International Review of Cytology 79, 215–35.
Boya, J., Calvo, J. &Carbonell, A. L. (1987a) Appearance of microglial cells in the postnatal rat retina.Archivum Histologicum Japonicum 50, 223–8.
Boya, J., Carbonell, A. L., Calvo, J. &Borregón, A. (1987b) Ultrastructural study on the origin of rat microglial cells.Acta Anatomica 130, 329–35.
Bronner-Fraser, M. (1988) Guidance of neural crest migration during the early development of the peripheral nervous system. InThe Making of the Nervous System (edited byParnavelas, J. G., Stern, C. D. &Stirling, R. V.)pp. 105–27. Oxford: Oxford University Press.
Burstone, M. S. (1962)Enzyme histochemistry and its application in the study of neoplasm. New York: Academic Press.
Chamberlain, J. G. (1974) Scanning electron microscopy of epiplexus cells (macrophages) in the fetal rat brain.American Journal of Anatomy 139, 443–7.
Cuadros, M. A. (1986)Análisis morfológico e histocjuímico de los procesos de muerte celular en la diferenciación inicial de la retina del embrión de polio. Doctoral Thesis. University of Granada.
Cuadros, M. A. &Rios, A. (1988) Spatial and temporal correlation between early nerve fiber growth and neuro-epithelial cell death in the chick embryo retina.Anatomy and Embryology 178, 543–51.
Cunningham, T. J., Mohler, I. M. &Giordano, D. L. (1982) Naturally occurring neuron death in the ganglion cell layer of the neonatal rat: morphology and evidence for regional correspondence with neuron death in superior coloiculus.Developmental Brain Research 2, 203–15.
Erickson, C. A. (1986) Morphogenesis of the neural crest. InDevelopmental Biology. A Comprehensive Synthesis. Vol.2:The Cellular Basis of Morphogenesis (edited byBrowder, L. W.) pp. 481–543. New York: Plenum Press.
García-Porrero, J. A. &Ojeda, J. L. (1979) Cell death and phagocytosis in the neuroepithelium of the developing retina. A TEM and SEM study.Experientia 35, 375–6.
García-Porrero, J. A., Colvée, E. &Ojeda, J. L. (1984a) Cell death in the dorsal part of the chick optic cup. Evidence for a new necrotic area.Journal of Embryology and Experimental Morphology 80, 241–9.
Garci'a-Porrero, J. A., Colvée, E. &Ojeda, J. L. (1984b) The mechanisms of cell death and phagocytosis in the early chick lens morphogenesis: a scanning electron microscopy and cytochemical approach.Anatomical Record 208, 123–36.
Giulian, D. &Baker, T. J. (1985) Peptides released by ameboid microglia regulate astroglial proliferation.Journal of Cell Biology 101, 2411–5.
Giulian, D. &Lachman, L. B. (1985) Interleukin-1 stimulates astroglial proliferation after brain injury.Science 228, 497–9.
Hamburger, V. &Hamilton, H. L. (1951) A series of normal stages in the development of the chick embryo.Journal of Morphology 88, 49–92.
Hinchliffe, J. R. (1981) Cell death in embryogenesis. InCell Death in Biology and Pathology (edited byBowen, I. D. &Lockshin, R. A.) pp. 35–78. London: Chapman & Hall.
Horsburgh, G. M. &Sefton, A. J. (1986) The early development of the optic nerve and chiasm in embryonic rat.Journal of Comparative Neurology 243, 547–60.
Hughes, W. F. &Lavelle, A. (1975) The effects of early tectal lesions on development in the retinal ganglion cell layer of chick embryos.Journal of Comparative Neurology 163, 265–84.
Hughes, W. F. &McLoon, S. C. (1979) Ganglion cell death during normal retinal development in the chick: comparisons with cell death induced by early target field destructions.Experimental Neurology 66, 587–601.
Hume, D. A., Perry, V. H. &Gordon, S. (1983) Immuno-histochemical localization of a macrophage-specific antigen in developing mouse retina: phagocytosis of dying neurons and differentiation of microglial cells to form a regular array in the plexiform layers.Journal of Cell Biology 97, 253–7.
Jordan, F. L. &Thomas, W. E. (1988) Brain macrophages: questions of origin and interrelationship.Brain Research Reviews 13, 165–78.
Kallén, B. (1955) Cell degeneration during normal ontogenesis of the rabbit brain.Journal of Anatomy 89, 153–61.
Kallén, B. (1965) Degeneration and regeneration in the vertebrate central nervous system during embryogenesis.Progress in Brain Research 14, 77–96.
Le Douarin, N. M. &Smith, J. (1988) Development of the peripheral nervous system from the neural crest.Annual Review of Cell Biology 4, 375–404.
Linden, R., Cavalcante, L. A. &Barradas, P. C. (1986) Mononuclear phagocytes in the retina of developing rats.Histochemistry 85, 335–9.
Martín-Partido, G., Rodríguez-Gallardo, L., Alvarez, I. S. &Navascués, J. (1988) Cell death in the ventral region of the neural retina during the early development of the chick embryo eye.Anatomical Record 222, 272–81.
McKenna, O. C. &Chairetakis, J. S. (1980) Scanning and transmission electron microscopic study of the supraependymal macrophages in the lateral ventricles of the toad brain.Cell and Tissue Research 207, 321–9.
Navascués, J., Rodríguez-Gallardo, L., García- Marti'nez, V., Alvarez, I. S. &Martín-Partido, G. (1987) Extra-axonal environment and fibre directionality in the early development of the chick embryo optic chiasm: a light and scanning electron microscopic study.Journal of Neurocytology 16, 299–310.
Navascués, J., Martín-Partido, G., Alvarez, I. S. &Rodríguez-Gallardo, L. (1988) Cell death in suboptic necrotic centers of chick embryo diencephalon and their topographic relationship with the earliest optic fiber fascicles.Journal of Comparative Neurology 278, 34–46.
Perry, V. H., Henderson, Z. &Linden, R. (1983) Postnatal changes in retinal ganglion cell and optic axon populations in the pigmented rat.Journal of Comparative Neurology 219, 356–68.
Perry, V. H. &Gordon, S. (1988) Macrophages and microglia in the nervous system.Trends in Neurosciences 11, 273–7.
Poston, M. R., Fredieu, J., Carney, P. R. &Silver, J. (1988) Roles of glia and neural crest cells in creating axon pathways and boundaries in the vertebrate central and peripheral nervous systems. InThe Making of the Nervous System (Edited ByParnavelas, J. G., Stern, C. D. &Stirling, R. V.) pp. 282–313. Oxford: Oxford University Press.
Rager, G. &Rager, U. (1976) Generation and degeneration of retinal ganglion cells in the chicken.Experimental Brain Research 251, 551–3.
Rosenbaum, J. T., O'rourke, L., Davies, G., Wenger, C., David, L. &Robertson, J. E. (1987) Retinal pigment epithelial cells secrete substances that are chemotactic for monocytes.Current Eye Research 6, 793–800.
Schook, P. (1980a) Morphogenetic movements during the early development of the chick eye. A light microscopic and spatial reconstructive study.Acta morphologica neerlando-scandinavica 18, 1–30.
Schook, P. (1980b) Morphogenetic movements during the early development of the chick eye. A structural and spatial reconstructive study. B. Invagination of the optic vesicle and fusion of its walls.Acta morphologica neerlando-scandinavica 18, 159–80.
Schook, P. (1982) Cell action and cell interaction during ocular morphogenesis. InOcular Anatomy, Embryology, and Teratology (edited byJakobiek, F. A.) pp. 121–41. New York: Harper & Row.
Sengelaub, D. R. &Finlay, B. L. (1982) Cell death in the mammalian visual system during normal development.Journal of Comparative Neurology 204, 311–7.
Silver, J. &Hughes, A. F. W. (1973) The role of cell death during morphogenesis of the mammalian eye.Journal of Morphology 140, 159–70.
Silver, J., Poston, M. &Rutishauser, U. (1987) Axon pathway boundaries in the developing brain. I. Cellular and molecular determinants that separate the optic and olfactory projections.Journal of Neuroscience 7, 2264–72.
Sturrock, R. R. (1988) An ultrastructural study of intraventricular macrophages in the brains of aged mice.Anatomischer Anzeiger 165, 283–90.
Young, R. W. (1984) Cell death during differentiation of the retina in the mouse.Journal of Comparative Neurology 229, 362–73.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
MartÍn-Partido, G., NavascuÉs, J. Macrophage-like cells in the presumptive optic pathways in the floor of the diencephalon of the chick embryo. J Neurocytol 19, 820–832 (1990). https://doi.org/10.1007/BF01186813
Received:
Revised:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF01186813