Summary
The post-embryonic development of the rectifying Giant Fibre-Motor Giant (GF-MoG) synapse and the Giant Fibre-Segmental Giant (GF-SG) synapse has been investigated using electron-microscopy. In adults, the MoG and SG neurons make contact with the GFs by sending narrow ‘finger-like’ processes through the glial and connective tissue sheath surrounding each GF. The junctional region is characterized by closely apposed membranes (approximately 4 nm separation) traversed by regularly spaced connections, and large (60–80 nm) spherical vesicles in the presynaptic fibre.
In newly hatched crayfish junctional contact is made over extensive areas of flat membrane apposition, due to the absence of a thick connective sheath around the giant fibres. Initially the junctional region is dominated by contacts which are morphologically indistinguishable from chemical synapses, i.e.
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The apposed membranes are separated by a cleft of approximately 20–30 nm (an order of magnitude larger than the cleft distance at electrotonic synapses).
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There is pre- and post-synaptic thickening of the junctional membranes with a dense cytoplasmic material.
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Small (25–40nm) pleomorphic vesicles are found on the presynaptic side of the junction, commonly in association with a dense presynaptic bar.
Regions of junctional contact displaying the adult electrotonic-type morphology first appear at approximately one week post-hatching. At this age they are limited in distribution and occupy a central position in the area of contact surrounded by a broad ‘chemical-like’ annulus. During subsequent development these sites with electrotonic-type morphology grow in relative size, so that the ‘chemical-like’ sites become compressed towards the edges of the regions of contact. The adult type of morphology, in which the ‘chemical-like’ regions are vestigial, is achieved approximately two months after hatching.
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References
Bennett, M. V. L. (1972) A comparison of electrically and chemically mediated transmission. InStructure and Function of Synapses (edited byPappas, G. D. &Purpura, D. P.), pp. 222–56. New York: Raven Press.
Bennett, M. V. L., Pappas, G. D., Gimenez, M. &Nakajima, Y. (1967) Physiology and ultrastructure of electrotonic junctions. IV. Medullary electromotor nuclei in gymnotid fish,Journal of Neurophysiology 30, 236–300.
Casper, D. L. D., Goodenough, D. A., Makowski, L. &Phillips, D. M. (1977) Gap junction structures. I. Correlated electron microscopy and X-ray diffraction,Journal of Cell Biology 74, 605–28.
Faber, D. S., Kaars, C. &Zottoli, S. J. (1980) Dual transmission at morphologically mixed synapses: evidence from postsynaptic cobalt injections.Neuroscience 5, 433–40.
Furshpan, E. J. &Potter, D. D. (1959) Transmission at the giant motor synapse of the crayfish,Journal of Physiology 145, 289–325.
Hall, D. H., Spray, D. C. &Bennett, M. V. L. (1983) Gap junctions and septate-like junctions between neurons of the opisthobranch molluscNavanax inermis.Journal of Neurocytology 12, 831–46.
Hall, D. H., Gilat, E. &Bennett, M. V. L. (1985) Ultrastructure of the rectifying electrotonic synapses between giant fibres and pectoral fin adductor motor neurons in the hatchetfish.Journal of Neurocytology 14, 825–34.
Hama, K. (1961) Some observations on the fine structure of the giant fibres of the crayfishes (Cambarus virilus andCambarus clarkii) with special reference to the submicroscopic rganization of the synapses.Anatomical Record 141, 275–94.
Hanna, R. B., Keeter, J. S. &Pappas, G. D. (1978) The fine structure of a rectifying electronic synapse,Journal of Cell Biology 79, 764–73.
Heitler, W. J., Cobb, J. L. S. &Fraser, K. (1985) Ultrastructure of the segmental giant neuron of crayfish,Journal of Neurocytology 14, 921–41.
Heitler, W. J. &Darrig, S. (1986) The segmental giant neuron of the signal crayfish,Pacifastacus leniusculus, and its interactions with abdominal fast flexor and swimmeret motor-neurons,Journal of Experimental Biology 121, 55–75.
Jaslove, S. W. &Brink, P. R. (1986) The mechanism of rectification at the electrotonic motor giant synapse of the crayfish.Nature 323, 63–5.
Killmann, F. &Gras, H. (1988) Chemical and electrotonic synapses on the collaterals of the lateral giant fibres in the earthworm,Lumbricus terrestris L.(Annelida, Oligochaeta) Zoologischer Anzeiger 221 [Supplement] 157–82.
Killmann, F. &Schurmann, F. W. (1985) Both electrical and chemical transmission between the ‘lobula giant movement detector’ and the ‘descending contralateral movement detector’ neurons of locusts are supported by electron microscopy,Journal of Neurocytology 14, 637–52.
Kramer, A. P., Krasne, F. B. &Wine, J. J. (1981) Interneurons between giant axons and motoneurons in crayfish escape circuitry,Journal of Neurophysiology 45, 550–73.
Krasne, F. &Stirling, C. A. (1972) Synapses of crayfish abdominal ganglia with special attention to afferent and efferent connections of the lateral giant fibres.Zeitschrift fur Zellforschung und mikroskopische Anatomie 127, 526–44.
Lopresti, V., Macagno, F. 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 Sciences (USA) 71, 1098–1102.
Martin, A. R. &Pilar, G. (1963) Dual mode of synaptic transmission in the avian ciliary ganglion.Journal of Physiology 168, 443–63.
Mittenthal, J. E. &Wine, J. J. (1973) Connectivity patterns of crayfish giant interneurons: visulation of synaptic regions with cobalt dye.Science 179, 182–4.
Pappas, G. D. (1975) The fine structure of electrotonic synapses. InGolgi Centennial Symposium: Perspectives in Neurobiology (edited bySantini, M.), pp. 339–44. New York: Raven Press.
Peracchia, C. (1973) Low resistance junctions in crayfish. I. Two arrays of globules in junctional membranes.Journal of Cell Biology 57, 54–65.
Peracchia, C. &Dulhunty, A. F. (1976) Low resistance junctions in crayfish. Structural changes with functional uncoupling.Journal of Cell Biology 70, 419–39.
Peracchia, C. &Mittler, R. S. (1972) Fixation by means of glutaraldehyde-hydrogen peroxide reaction products.Journal of Cell Biology 53, 234–8.
Peters, A., Palay, S. L. &Webster, H. de F. (1970)The fine structure of the nervous system: the cells and their processes. New York: Harper & Row.
Ringham, G. L. (1975) Localization and electrical characteristics of a giant synapse in the spinal cord of the lamprey.Journal of Physiology 251, 395–407.
Robertson, J. D. (1961) Ultrastructure of excitable membranes and the crayfish median-giant synapse.Annals of the New York Academy of Sciences 94, 339–89.
Roberts, A., Krasne, F. B., Hagiwara, G., Wine, J. J. &Kramer, A. P. (1982) Segmental giant: evidence for a driver neuron interposed between command and motor neurons in the crayfish escape system,Journal of Neurophysiology 47, 761–81.
Sotelo, C. (1975) Morphological correlates of electrotonic coupling between neurons in mammalian nervous system. InGolgi Centennial Symposium: Perspectives in Neurobiology (edited bySantini, M.), pp. 355–65. New York: Raven Press.
Sotelo, C. &Korn, H. (1978) Morphological correlates of electrical coupling and other interactions through low resistance pathways between neurons of the vertebrate central nervous system.International Review of Cytology 55, 67–107.
Steinberg, M. S., Shida, H., Giudice, G. J., Shida, M., Patel, N. H. &Blaschuk, O. W. (1986) On the molecular organization, diversity and functions of desmosomal proteins. Infunctional Complexes of Epithelial Cells. (Ciba Foundation Symposium 125), pp. 3–25. Chichester: Wiley.
Stirling, C. A. (1972) The ultrastructure of giant fibre and serial synapses in crayfish.Zeitschrift für Zellforschung and mikroskopische Anatomie 131, 31–45.
Strausfeld, N. &Bassemir, U. K. (1983) Cobalt-coupled neurons of a giant fibre system of diptera.Journal of Neurocytology 12, 971–91.
Taugner, R., Sonnhof, U., Richter, D. W. &Schiller, A. (1978) Mixed (chemical and electrical) synapses on frog spinal motoneurons.Cell & Tissue Research 193, 41–59.
Wine, J. J. &Krasne, F. B. (1982) The cellular organization of the crayfish escape behaviour. InThe biology of the Crustacea, Vol. III, Neural Integration (edited byAtwood, H. &Sandeman, D.), Chap. 15. New York: Academic Press, 241–92.
Zampighi, G., Ramon, F. &Duran, W. (1978) Fine structure of the electrotonic synapse of the lateral giant axons in a crayfish (Procambarus clarkii).Tissue & Cell 10, 413–26.
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Leitch, B., Cobb, J.L.S., Heitler, W.J. et al. Post-embryonic development of rectifying electrical synapses in the crayfish: ultrastructure. J Neurocytol 18, 749–761 (1989). https://doi.org/10.1007/BF01187228
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DOI: https://doi.org/10.1007/BF01187228