Summary
The migration of amacrine neuroblasts toward the prospective amacrine cell layer in the chick embryo retina has been studied, in Golgi-stained sections, between days 5 and 9 of embryogenesis.
Two distinct populations of presumptive amacrine neuroblasts have been identified on the basis of their shape and migratory behavior. One population (smooth amacrine neuroblasts) display smooth, monopolar or bipolar contours, moving freely across the retina without major changes in the original postmitotic shape, and give processes only after reaching the primitive inner plexiform layer. The second population (multipodial amacrine neuroblasts) includes multipolar neuroblasts with abundant filiform and/or lamelliform processes sprouting in various directions; these highly plastic cells begin modifying their shapes at the time of release from the ventricular lining and continue to do so as they move toward their definitive location.
Thus, the well-known heterogeneity of adult amacrine cells seems to be preluded by differences in neuroblastic migratory patterns, suggesting the existence of at least two different subsets of amacrine cell precursors.
Similar content being viewed by others
References
Alberts B, Bray D, Lewis J, Raff M, Roberts K, Watson JD (1983) Molecular biology of the cell. Garland Publishing Inc, New York London
Bunge MB (1977) Initial endocytosis of peroxidase or ferritin by growth cones of cultured nerve cells. J Neurocytol 6:407–439
Carbonetto S (1984) The extracellular matrix of the nervous system. Trends Neurol Sci 7:382–387
Derer P (1974) Histogenèse du neocortex du rat albinos durant la période foetale et neonatale. J Hirnforsch 15:49–74
Genis-Gálvez JM, Puelles L, Prada C (1977) Inverted (displaced) retinal amacrine cells and their embryonic development in the chick. Exp Neurol 56:151–157
Hamburger V, Hamilton HL (1951) A series of normal stages in the development of the chick embryo. J Morphol 88:48–92
Hinds JW, Hinds PL (1974) Early ganglion cell differentiation in the mouse retina: An electron microscopic analysis utilizing serial sections. Dev Biol 37:381–416
Hinds JW, Hinds PL (1976) An E.M. serial section study of the mouse retina at the 15th day of gestation. Anat Rec 184:428
Hinds JW, Hinds PL (1978) Early development of amacrine cells in the mouse retina: An electron microscopic, serial section analysis. J Comp Neurol 179:277–300
Hinds JW, Hinds PL (1979) Differentiation of photoreceptors and horizontal cells in the embryonic mouse retina: An electron microscopic serial section analysis. J Comp Neurol 187:495–512
Hinds JW, Hinds PL (1983) Development of retinal amacrine cells in the mouse embryos: evidence for two modes of formation. J Comp Neurol 213:1–23
Hughes A, Vaney DI (1980) Coronate cells: displaced amacrines of the rabbit retina. J Comp Neurol 189:169–189
Hughes A, Wieniawa-Narkiewicz E (1980) A newly identified population of presumptive microneurones in the cat retinal ganglion cell layer. Nature 284:468–470
Jacobson M (1978) Developmental neurobiology. Plenum Press Inc., New York
Kahn AJ (1974) An autoradiographic analysis of the time of appearance of neurons in the developing chick neural retina. Dev Biol 38:30–40
Koulakoff A, Bizzini B, Berwald-Netter Y (1983) Neuronal acquisition of tetanus toxin binding sites: relationship with the last mitotic cycle. Dev Biol 100:350–357
Le Douarin N (1984) Cell migrations in embryos. Cell 38:353–360
Letourneau PC (1983) Axonal growth and guidance. Trends Neurosci 6:451–455
Masuko S, Shimada Y (1983) Neuronal cell-surface specific antigen(s) is expressed during the terminal mitosis of cells destined to become neuroblasts. Dev Biol 96:396–404
Meller K, Glees P (1965) The differentiation of neuroglia-Müllercells in the retina of chick. Z Zellforsch 66:321–322
Meller K, Tetzlaff W (1975) Neuronal migration during the early development of the cerebral Cortex. Cell Tissue Res 163:313–325
Morest DK (1970) The pattern of neurogenesis in the retina of the rat. Z Anat Entwicklungs-Gesch 131:45–67
Morris VB (1973) Time differences in the formation of the receptor types in the developing chick retina. J Comp Neurol 151:323–330
Nowakowski RS, Rakic P (1979) The mode of migration of neurons to the hippocampus: a Golgi and electron microscopic analysis in foetal rhesus monkey. J Neurocytol 8:697–718
Perry VH, Walker M (1980) Amacrine cells, displaced amacrine cells and interplexiform cells in the retina of the rat. Proc R Soc Lond 208:415–431
Pfenninger KH, Reese RP (1976) From the growth cone to the synapse. In: Barondes SH (ed) Neuronal recognition. Chapman and Hall, London, pp 131–178
Puelles L, Bendala C (1978) Differentiation of neuroblasts in the chick optic tectum up to eight days of incubation: a Golgi study. Neuroscience 3:307–325
Prada C, López-Mascaraque L (1985) Dammar resin prevents the fading of celloidin sections of Golgi impregnated embryonic central nervous system. Mikroskopie 42:146–147
Prada C, Ramírez G (1983) A Golgi study of the cell cycle and early neuron and glia differentiation in the chick retina. In: Grisolía S, Guerri C, Samson F, Norton S, Reinoso-Suárez F (eds) Ramón y Cajal's contribution to the neurosciences. Elsevier Science Publishers, B.V., pp 117–123
Prada C, Puelles L, Genis-Gálvez JM (1981) A Golgi study on the early sequence of differentiation of ganglion cells in the chick embryo retina. Anat Embryol 161:305–317
Rakic P (1972) Mode of cell migration to the superficial layers of fetal monkey neocortex. J Comp Neurol 145:61–87
Rakic P (1981) Neuronal-glial interaction during brain development. Trends Neurosci 4:184–187
Ramón y Cajal S (1909) Histologie du système nerveux de l'homme et des vertebrés. Vol I (1952 reprint). Instituto Ramón y Cajal, Madrid
Ramón y Cajal S (1911) Histologie du système nerveux de l'homme et des vertebrés. Vol. II (1955 reprint). Instituto Ramón y Cajal, Madrid
Ramón y Cajal S (1929) Studies in vertebrate neurogenesis. L. Guth, transl (1960), Charles C Thomas, Springfield, Ill
Shoukimas GM, Hinds JW (1978) The development of the cerebral cortex in the embryonic mouse: an electron microscopic serial section analysis. J Comp Neurol 179:795–830
Stell W, Marshak D, Yamada NB, Karten H (1980) Peptides are in the eye of the beholder. Trends Neurosci 3:292–295
Stensaas LJ (1967) The development of hippocampal and dorsolateral pallial regions of the cerebral hemisphere in fetal rabbits. I. Fifteen millimeter stage, spongioblast morphology. J Comp Neurol 129:59–70
Tapscott SJ, Bennett GS, Holtzer H (1981) Neuronal precursor cells in the chick neural tube express neurofilament proteins. Nature 292:836–838
Thiery JP (1984) Mechanisms of cell migration in the vertebrate embryo. Cell Differ 15:1–15
Trenkner E, Smith D, Segil N (1984) Is cerebellar granule cell migration regulated by an internal clock? J Neurosci 4:2850–2855
Trisler D (1982) Are molecular markers of cell position involved in the formation of neural circuits? Trends Neurosci 5:306–310
Wentworth LE, Hinds JW (1978) Early motoneuron formation in the cervical spinal cord at the mouse: an electron microscopic, serial section analysis. J Comp Neurol 177:611–634
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Prada, C., Puelles, L., Genis-Gálvez, J.M. et al. Two modes of free migration of amacrine cell neuroblasts in the chick retina. Anat Embryol 175, 281–287 (1987). https://doi.org/10.1007/BF00309842
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00309842