Summary
The formation of synapses between sensory cells and the terminals of afferent axons has been examined in the embryonic chick labyrinth. Neurites initially cross the otocyst basal lamina and ramify among the undifferentiated epithelial cells by stage 25 of Hamburger and Hamilton. At the same time granular vesicles, with diameters averaging 130 nm, appear in the basal cytoplasm of a few of the epithelial cells. These vesicles often exist in groups at sites of contact with neuntes. By stages 27–28, non membrane-bound densities are frequently found in association with groups of granular vesicles at the plasma membrane. Smaller, clear synaptic vesicles are also a prominent component of these arrangements in presumptive hair cells. Presynaptic ribbons opposite postsynaptic densites are identifiable at about stage 28, and their number increases during subsequent embryonic stages. Specialized appositions, including adherent, postsynaptic and possibly gap junctional contacts, join epithelial cells and nerve terminals throughout this period. The distribution of these junctions is variable, and is not necessarily correlated with the sites of formation of presynaptic ribbons. By stage 32, well-developed chemical synapses consisting of presynaptic ribbons with vesicle halos and postsynaptic densities are common features of hair cell-afferent nerve terminal contact regions. In addition, possible sites of gap junctional contact between adjacent intra-epithelial nerve endings found at stage 32 presage those found in the cristae and maculae of pre-hatch (stage 45) embryos and adults.
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References
Bunge, M. B. (1973) Fine structure of nerve fibers and growth cones of isolated sympathetic neurons in culture.Journal of Cell Biology 56, 713–35.
Burnstock, G. &Costa, M. (1975)Adrenergic Neurons; Their Organization, Function and Development in the Peripheral Nervous System. New York: Wiley.
Chan-Palay, V. (1978) The paratrigeminal nucleus. II. Identification and inter-relations of catecholamine axons, indoleamine axons and substance P immunoreactive cells in the neuropil.Journal of Neurocytology 7, 419–42.
Dixon, J. S. &Cronly-Dillon, J. R. (1972) The fine structure of the developing retina inXenopus laevis.Journal of Embryology and Experimental Morphology 28, 659–66.
Dixon, J. S. &Cronly-Dillon, J. R. (1974) Intercellular gap junctions in pigment epithelium cells during retinal specification inXenopus laevis.Nature 251, 505.
Favre, D. &Sans, A. (1979) Embryonic and postnatal development of afferent innervation in cat vestibular receptors.Acta Otolaryngologica 87, 97–107.
Fink, D. J. &Morest, D. K. (1977) Formation of synaptic endings by colossal fibers in the vestibular epithelium of the chick embryo.Neuroscience 2, 229–52.
Flock, A. (1974) The ultrastructure of lateral line sense organs in the juvenile salamander.Ambystoma mexicanum. Cell and Tissue Research152, 283–92.
Foelix, R. F. &Oppenheim, R. W. (1973) Synaptogenesis in the avian embryo: Ultrastructure and possible behavioral correlates. InStudies on the Development of Behavior and the Nervous System (edited byGottlieb, G.), Vol. 1, pp. 103–139. New York: Academic Press.
Friedmann, I. &Bird, E. S. (1967) Electron microscopic studies of the isolated fowl embryo otocyst in tissue culture.Journal of Ultrastructure Research 20, 356–65.
Fujisawa, H., Morioka, H., Watanabe, K. &Nakamura, H. (1976) A decay of gap junctions in association with cell differentiation of neural retina in chick embryonic development.Journal of Cell Science 22, 585–96.
Ginzberg, R. D. &Gilula, N. B. (1979a) Modulation of cell junctions during differentiation of the chicken otocyst sensory epithelium.Developmental Biology 68, 110–29.
Ginzberg, R. D. &Gilula, N. B. (1979b) Development of ribbon synapses in the chick otocyst.Anatomical Record 193, 548–9 (abstract).
Hamburger, V. &Hamilton, H. L. (1951) A series of normal stages in the development of the chick embryo.Journal of Morphology 88, 49–92.
Hamilton, D. W. (1968) The calyceal synapse of type I vestibular hair cells.Journal of Ultrastructure Research 23, 98–114.
Hayes, B. P. (1976) The distribution of intercellular gap junctions in the developing retina and pigment epithelium ofXenopus laevis.Anatomy and Embryology 150, 99–111.
Hinojosa, R. &Robertson, J. D. (1967) Ultrastructure of the spoon type synaptic endings in the nucleus vestibularis tangentialis of the chick.Journal of Cell Biology 34, 421–30.
Hirokawa, N. (1977) Disappearance of afferent and efferent nerve terminals in the inner ear of the chick embryo after chronic treatment with β-bungarotoxin.Journal of Cell Biology 73, 27–46.
Hirokawa, N. (1978) Synaptogenesis in the basilar papilla of the chick.Journal of Neurocytology 7, 283–300.
Jones, D. G. &Revell, E. (1970a) The postnatal development of the synapse: A morphological approach utilizing synaptosomes. I. General features.Zeitschrift für Zellforschung und mikroskopische Anatomie 111, 179–94.
Jones, D. G. &Revell, E. (1970b) The postnatal development of the synapse: A morphological approach utilizing synaptosomes. II. Paramembranous densities.Zeitschrift für Zellforschung und mikroskopische Anatomie 111, 195–208.
Jørgensen, J. M. &Flock, A. (1976) Non-innervated sense organs of the lateral line: development in regenerating tail of the salamanderAmbystoma mexicanum.Journal of Neurocytology 5, 33–41.
Kelly, A. M. &Zacks, S. I. (1969) The fine structure of motor endplate morphogenesis.Journal of Cell Biology 42, 154–69.
Klinke, R. &Evans, E. F. (1977) Evidence that catecholamines are not the afferent transmitter in the cochlea.Experimental Brain Research 28, 315–24.
Klinke, R. &Oertel, W. (1977a) Evidence that 5-HT is not the afferent transmitter in the cochlea.Experimental Brain Research 30, 141–3.
Klinke, R. &Oertel, W. (1977b) Amino acids — putative afferent transmitter in the cochlea.Experimental Brain Research 30, 145–8.
Knowlton, V. Y. (1967) Correlation of the development of membranous and bony labyrinths, acoustic ganglia, nerves, and brain centers in the chick embryo.Journal of Morphology 121, 179–207.
Lawrence, T. S., Beers, W. H. &Gilula, N. B. (1978) Transmission of hormonal stimulation by cell-to-cell communication.Nature 272, 501–6.
Lentz, T. L. (1967) Fine structure of nerves in the regenerating limb of the newtTriturus.American Journal of Anatomy 121, 647–69.
LoPresti, V., Macagno, E. R. &Levinthal, C. (1974) Structure and development of neuronal connections in isogenic organisms: transient gap junctions between growing optic axons and lamina neuroblasts.Proceedings of the National Academy of Science (U.S.A.) 71, 1098–102.
McLaughlin, B. J. (1976) A fine structural and E-PTA study of photoreceptor synaptogenesis in the chick retina.Journal of Comparative Neurology 170, 347–64.
Meier, S. (1978a) Development of the embryonic chick otic placode. I. Light microscopic analysis.Anatomical Record 191, 447–58.
Meier, S. (1978b) Development of the embryonic chick otic placode. II. Electron microscopic analysis.Anatomical Record 191, 459–78.
Monaghan, P. (1975) Ultrastructural and pharmacological studies on the afferent synapse of lateral-line sensory cells of the African clawed toad,Xenopus laevis.Cell and Tissue Research 163, 239–47.
Ochi, J. (1967) Elektronenmikroskopische Untersuchung des Bulbus Olfactorius der Ratte Während der Entwicklung.Zeitschrift für Zellforschung und mikroskopische Anatomie 76, 339–48.
Orr, M. F. (1968) Histogenesis of sensory epithelium in reaggregates of dissociated embrycmic chick otocysts.Developmental Biology 17, 39–54.
Overton, J. (1977) Formation of junctions and cell sorting in aggregates of chick and mouse cells.Developmental Biology 55, 103–16.
Pannese, E., Luciano, L., Iurato, S. &Reale, E. (1977) Intercellular junctions and other membrane specializations in developing spinal ganglia; a freeze-fracture study.Journal of Ultrastructure Research 60, 169–80.
Sotelo, C. &Korn, H. (1978) Morphological correlates of electrical and other interactions through low-resistance pathways between neurons of the vertebrate central nervous system.International Review of Cytology 55, 67–107.
Steinbach, A. B. &Bennett, M. V. L. (1971) Effects of divalent ions and drugs on synaptic transmission in phasic electroreceptors in a mormyrid fish.Journal of General Physiology 58, 580–98.
Takasaka, T. &Smith, C. A. (1971) The structure and innervation of the pigeon's basilar papilla.Journal of Ultrastructure Research 35, 20–65.
Thornhill, R. A. (1972a) The development of the labyrinth of the lamprey (Lampetra fluviatilis Linn. 1758).Proceedings of the Royal Society of London, Series B 181, 175–98.
Thornhill, R. A. (1972b) The effect of catecholamine precursors and related drugs on the morphology of the synaptic bars in the vestibular epithelia of the frog,Rana temporaria.Comparative and General Pharmacology 3, 89–97.
Tweedle, C. D. (1977) Ultrastructure of lateral line organs in aneurogenic amphibian larvae (Ambystama).Cell and Tissue Research 185, 191–7.
Tweedle, C. D. (1978) Ultrastructure of Merkel cell development in aneurogenic and control amphibian larvae (Ambystoma).Neuroscience 3, 481–6.
Van Buren, J, M., Akert, K. &Sandri, C. (1977) Neuritic growth cone and ependymal gap junctions in the feline subfomical organ during early development.Cell and Tissue Research 181, 27–36.
Van De Water, T. R. (1976) Effects of removal of the statoacoustic ganglion complex upon the growing otocyst.Annals of Otology, Rhinology and Laryngology, Suppl.33, 1–32.
Van De Water, T. R., WersÄll, J., Anniko, M. &Nordeman, H. (1978) Development of the sensory receptor cells in the utricular macula.Otolaryngology 86, 297–304.
Vázquez-Nin, G. H. &Sotelo, J. R. (1968) Electron microscope study of the developing nerve terminals in the acoustic organs of the chick embryo.Zeitschrift für Zellforschung und mikroskopische Anatomie 92, 325–38.
Wersäll, J., Gleisner, L. &Lundquist, P.-G. (1966) Ultrastructure of the vestibular end organs. InMyotactic, Kinesthetic and Vestibular Mechanisms (edited byde Reuck, A. V. S. andKnight, J.), pp. 105–120. Boston: Little, Brown and Co.
Westrum, L. E. (1975) Electron microscopy of synaptic structures in olfactory cortex of early postnatal rats.Journal of Neurocytology 4, 713–32.
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Ginzberg, R.D., Gilula, N.B. Synaptogene sis in the vestibular sensory epithelium of the chick embryo. J Neurocytol 9, 405–424 (1980). https://doi.org/10.1007/BF01181545
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DOI: https://doi.org/10.1007/BF01181545