Summary
The rostro-caudal gradient of differentiation found in vertebrate embryos has been utilized to examine the sequence of synaptic junction development in the spinal cord of Xenopus laevis at a late embryonic stage. Uniform samples were taken at various points along the cord of a stage 27 embryo and examined in the electron microscope. The general ultrastructure of the cord demonstrated the rostro-caudal gradient of development. The sequence of synaptic junction development was like that in the cervical region (Hayes and Roberts, 1973). “Membrane-vesicle clusters” and “immature” synaptic junctions were found most caudally followed by synaptic junctions, first with cleft and subsynaptic membrane density, then with only cleft density and finally, most rostrally, with cleft, subsynaptic membrane, and subsynaptic cytoplasmic density. Mature synaptic junctions were found in increasing numbers from the mid to anterior trunk cord and could mediate alternating trunk flexions made by the embryos at this stage of development. “Membrane-vesicle clusters” were found near processes containing irregular vesicles and also near membrane outlines. These may be signs of dendritic growth. “Membrane-vesicle clusters” were also found in varicosities, facing the space around the spinal cord and in nerve fibres peripherally between the skin and myotomes. This suggests an association of early stages in synaptogenesis with axon growth. This and other possible inferences about axon and dendrite growth in relation to synaptogenesis are discussed.
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References
Bodian, D., Melby, E. C., Taylor, N.: Development of fine structure of spinal cord in monkey fetuses II. Pre-reflex period to period of long intersegmental reflexes. J. comp. Neurol. 133, 113–166 (1968)
Bunge, M. B.: Fine structure of nerve fibres and growth cones of isolated sympathetic neurons in culture. J. Cell Biol. 56, 713–735 (1973)
Foelix, R. F., Oppenheim, R. W.: Synaptogenesis in the avian embryo: ultrastructure and possible behavioural correlates. In: Studies on the development of behaviour and the nervous system, vol. 1, Behavioural embryology, p. 103–139. New York: Academic Press 1973
Glees, P., Sheppard, B. L.: Electron microscope studies of the synapse in developing chick spinal cord. Z. Zellforsch. 62, 356–362 (1964)
Grainger, F., James, D. W.: Association of glial cells with the terminal parts of neurite bundles extending from chick spinal cord in vitro. Z. Zellforsch. 108, 93–104 (1970)
Grainger, F., James, D. W., Tresman, R. L.: An electron-microscope study of the early outgrowth from chick spinal cord in vitro. Z. Zellforsch. 90, 53–67 (1968)
Guillery, R. W., Sobkowicz, H. M., Scott, G. L.: Relationships between glial and neuronal elements in the development of long term cultures of spinal cord in the fetal mouse. J. comp. Neurol. 140, 1–34 (1970)
Hayes, B. P., Roberts, A.: Synaptic junction development in the spinal cord of an amphibian embryo: an electron microscope study. Z. Zellforsch. 137, 251–269 (1973)
Hughes, A. F. W.: Development of the primary sensory system in Xenopus laevis (Daudin). J. Anat. (Lond.) 91, 323–338 (1957)
Hughes, A. F. W.: Studies in embryonic and larval development in Amphibia. II. The spinal motor-root. J. Embryol. exp. Morph. 7, 128–145 (1959)
James, D. W., Tresman, R. L.: Synaptic profiles in the outgrowth from chick spinal cord in vitro. Z. Zellforsch. 101, 598–606 (1969)
Kappers, C. U. A., Huber, G. C., Crosby, E. C.: The comparative anatomy of the nervous system of vertebrates including man. New York: The Macmillan Co. (1936)
Lopresti, V., Macagno, E. R., Levinthal, C.: Structure and development of neuronal connections in isogenic organisms: Cellular interactions in the development of the optic lamina of Daphnia. Proc. nat. Acad. Sci. (Wash.) 70, 433–437 (1973)
Lyser, K. M.: Microtubules and filaments in developing axons and optic stalks. Tissue and Cell 3, 395–404 (1971)
May, M. K., Biscoe, T. J.: Preliminary observations on synaptic development in the foetal rat spinal cord. Brain Res. 53, 181–186 (1973)
Nieuwkoop, P. D., Faber, J.: Normal tables of Xenopus laevis (Daudin). Amsterdam: North Holland Publishing Co. 1956
Oppenheim, R. W., Foelix, R. F.: Synaptogenesis in the chick embryo spinal cord. Nature (Lond.) New Biol. 235, 126–128 (1972)
Peters, A., Palay, S. L., Webster, H. de F.: The fine structure of the nervous system. New York: Hoeber 1970
Sidman, R. L., Rakic, P.: Neuronal migration, with special reference to developing human brain: A. Review. Brain Res. 62, 1–35 (1973)
Skoff, R. P., Hamburger, V.: Fine structure of dendritic and axonal growth cones in embryonic chick spinal cord. J. comp. Neurol. 153, 107–148 (1974)
Spiedel, C. C.: Studies of living nerves. II. Activities of ameboid growth cones, sheath cells and myelin segments, as revealed by prolonged observation of individual nerve fibres in frog tadpoles. Amer. J. Anat. (Lond.) 52, 1–79 (1933)
Stelzner, D. J., Martin, A. H., Scott, G. L.: Early stages of synaptogenesis in the cervical spinal cord of the chick embryo. Z. Zellforsch. 138, 475–488 (1973)
Sumi, S. M.: The extracellular space in the developing rat brain: its variation with changes in the osmolarity of the fixative, method of fixation and maturation. J. Ultrastuct. Res. 29, 398–425 (1969)
Tennyson, V. M.: Fine structure of axon and growth cone of the dorsal root neuroblast of the rabbit embryo. J. Cell Biol. 44, 62–79 (1970)
Vaughn, J. E., Henrikson, C. K., Grieshaber, J. A.: A quantitive study of synapses on motoneurone dendritic growth cones in developing mouse spinal cord. J. Cell Biol. 60, 664–672 (1974)
Yamada, K. M., Spooner, B. S., Wessells, N. K.: Ultrastructure and function of growth cones and axons of cultured nerve cells. J. Cell Biol. 49, 614–635 (1971)
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Hayes, B.P., Roberts, A. The distribution of synapses along the spinal cord of an amphibian embryo: An electron microscope study of junction development. Cell Tissue Res. 153, 227–244 (1974). https://doi.org/10.1007/BF00226611
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DOI: https://doi.org/10.1007/BF00226611