Summary
Freeze-fracture replicas and ultrathin sections were used to characterize the gap junctions on the somata and large dendrites of frog motoneurons found earlier by Sonnhof et al. (1977). In freeze-fracture replicas one of the specific features of these relatively frequent gap junctions is the presence of circular regions of non-junctional membrane (“fenestrae”) within areas of typical gap junction appearance displaying P-face particles or E-face pits. Such “fenestrated” gap junctions are mostly associated with membrane specializations indicative of the active zone of a chemical synapse (including vesicle attachment sites in non anaesthetized animals) to constitute mixed synapses. These findings could be verified in ultrathin sections, which revealed that the vesicles of the chemical component of the mixed synapses were spherical and agranular. Our results suggest that the mixed synapses are predominantly axo-somatic and axo-dendritic.
The existence of dendro-dendritic gap junctions in the ventral horn region as described by Sotelo and Taxi (1970) was verified in ultrathin sections; they were rare, solely electrotonic in character, and probably represent the morphological basis for the VR-EPSP (Katz and Miledi, 1963; Kubota and Brookhart, 1963), i.e. electrotonic coupling between motoneurons of different spinal segments (Washizu, 1960).
Electrotonic coupling can also be demonstrated between motoneurons and afferent fibers of the dorsal root and the lateral column. Electrotonic potentials recorded within motoneurons during electrical stimulation of dorsal root or lateral column precede the chemical postsynaptic potentials; after Mn2+ blockade of chemical synaptic transmission, the electrotonic component persists. Some fibers of these afferent pathways are therefore assumed to act monosynaptically on the motoneuron via mixed axo-somatic and axo-dendritic synapses.
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References
Baylor, D.A., Nicholls, J.G.: Chemical and electrical synaptic connexions between cutaneous mechanoreceptor neurones in the central nervous system of the leech. J. Physiol. (Lond.) 203, 591–609 (1969)
Bennett, M.V.L.: Flexibility and rigidity in electrotonically coupled systems. In: Synaptic transmission and neuronal interaction (M.V.L. Bennett, ed.), pp. 153–178. New York: Raven Press 1974
Bennett, M.V.L., Pappas, G.D., Aljure, E., Nakajima, Y.: Physiology and ultrastructure of electrotonic junctions. II. Spinal and medullary electromotor nuclei in mormyrid fish. J. Neurophysiol. 30, 180–208 (1967a)
Bennett, M.V.L., Pappas, G.D., Giménez, M., Nakajima, Y.: Physiology and ultrastructure of electrotonic junctions. IV. Medullary electromotor nuclei in gymnotid fish. J. Neurophysiol. 30, 236–300 (1967b)
Branton, D., Bullivant, S., Gilula, N.B., Karnovsky, M.J., Moor, H., Mühlethaler, K., Northcote, D.H., Packer, L., Satir, B., Satir, P., Speth, V., Staehlin, L.A., Steere, R.L., Weinstein, R.S.: Freeze-etching nomenclature. Science 190, 54–56 (1975)
Brightman, M.W., Reese, T.S.: Junctions between intimately apposed cell membranes in the vertebrate brain. J. Cell Biol. 40, 648–677 (1969)
Cantino, D., Mugnaini, E.: The structural basis for electrotonic coupling in the avian ciliary ganglion. A study with thin sectioning and freeze-fracturing. J. Neurocytol. 4, 505–536 (1975)
Charlton, B.T., Gray, E.G.: Electron microscopy of specialized synaptic contacts suggesting electrical transmission in frog spinal cord. J. Physiol. (Lond.) 179, 2P-4P (1965)
Charlton, B.T., Gray, E.G.: Comparative electron microscopy of synapses in the vertebrate spinal cord. J. Cell Sci. 1, 67–80 (1966)
Ecker, A., Wiedersheim, R., Gaupp, E.: Anatomie des Frosches, Zweite Abteilung. 2. Auflage, Braunschweig: Vieweg 1899
Fadiga, E., Brookhart, J.M.: Monosynaptic activation of different portions of the motor neuron membrane. Amer. J. Physiol. (Lond.) 198, 693–703 (1960)
Forssmann, W.G., Ito, S., Weihe, E., Aoki, A., Dym, M., Fawcett, D.W.: An improved perfusion fixation method for the testis. Anat. Rec. 188, 307–314 (1977)
Glitsch, S.: Verdampfung von Platin aus Kohletiegeln zur elektronenmikroskopischen Schrägbedampfung. Naturwissenschaften 56, 559 (1969)
Gray, E.G.: Round and flat synaptic vesicles in the fish central nervous system. Symp. Int. Soc. Cell Biol. 8, 211–227 (1969)
Grinnell, A.D.: A study of the interaction between motoneurons in the frog spinal cord. J. Physiol. (Lond.) 182, 612–648 (1966)
Ito, S.: Thin section staining with uranyl-acetate in aqueous-acetone solution. Pers. communication, 1975
Karnovsky, M.J.: Use of ferrocyanide-reduced osmium tetroxide in electron microscopy. J. Cell Biol. 51, ASCB abstracts, 146 (1971)
Katz, B., Miledi, R.: A study of spontaneous miniature potentials in spinal motoneurons. J. Physiol. (Lond.) 168, 389–422 (1963)
Kensler, R.W., Brink, P., Dewey, M.M.: Nexus of frog ventricle. J. Cell Biol. 73, 768–781 (1977)
Kubota, K., Brookhart, J.M.: Recurrent facilitation of frog motoneurons. J. Neurophysiol. 26, 877–893 (1963)
Luft, J.H.: Embedding media — old and new. In: Advanced techniques in biological electron microscopy (J.K. Koehler, ed.), pp. 1–34. Berlin-Heidelberg-New York: Springer 1973
Magherini, P.C., Precht, W., Schwindt, P.C.: Evidence for electrotonic coupling between frog motoneurons in the in situ spinal cord. J. Neurophysiol. 39, 474–484 (1976)
Meszler, R.M., Pappas, G.D., Bennett, M.V.L.: Morphological demonstration of electrotonic coupling of neurons by way of presynaptic fibers. Brain Res. 36, 412–415 (1972)
Nicholls, J.G., Purves, D.: Monosynaptic chemical and electrical connexions between sensory and motor cells in the central nervous system of the leech. J. Physiol. (Lond.) 209, 647–667 (1970)
Pappas, G.D., Waxman, S.G., Bennett, M.V.L.: Morphology of spinal electromotor neurons and presynaptic coupling in the gymnotid Sternarchus albifrons. J. Neurocytol. 4, 469–478 (1975)
Peters, A., Palay, S.L., Webster, H.de F.: The fine structure of the nervous system: The neurons and supporting cells. Philadelphia-London-Toronto: W.B. Saunders Company 1976
Reynolds, E.S.: The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J. Cell Biol. 17, 208–212 (1963)
Robertson, J.D., Bodenheimer, T.S., Stage, D.E.: The ultrastructure of Mauthner cell synapses and nodes in goldfish brains. J. Cell Biol. 19, 159–199 (1963)
Sandri, C., Akert, K., Livingston, R.B., Moor, H.: Particle aggregations at specialized sites in freezeetched postsynaptic membranes. Brain Res. 41, 1–16 (1972)
Sandri, C., Buren, J.M. van, Akert, K.: Membrane morphology of the vertebrate nervous system. A study with freeze-etch technique. In: Progress in Brain Research, Vol. 46. Amsterdam-Oxford-New York: Elsevier Scientific Publishing Company 1977
Sonnhof, U., Grafe, P., Krumnikl, J., Lindner, M., Schindler, Lucia: Inhibitory postsynaptic actions of taurine, GABA and other amino acids on motoneurons of the isolated frog spinal cord. Brain Res. 100, 327–341 (1975)
Sonnhof, U., Richter, D.W., Taugner, R.: Electrotonic coupling between frog spinal motoneurons. An electrophysiological and morphological study. Brain Res. 138, 197–215 (1977)
Sotelo, C.: Morphological correlates of electrotonic coupling between neurons in mammalian nervous system. In: Golgi Centennial Symposium. Proceedings (M. Santini, ed.), pp. 355–365. New York: Raven Press 1975
Sotelo, C., Grofová, I.: Ultrastructural features of the spinal cord. In: Frog neurobiology. A handbook (R. Llinás, W. Precht, eds.), pp. 707–727. Berlin-Heidelberg-New York: Springer 1976
Sotelo, C., Llinás, R.: Specialized membrane junctions between neurons in the vertebrate cerebellar cortex. J. Cell Biol. 53, 271–289 (1972)
Sotelo, C., Palay, S.L.: Synapses avec des contacts étroits (tight junctions) dans le noyau vestibulaire latéral du rat. J. Microscopie 6, 83a (1967)
Sotelo, C., Palay, S.L.: The fine structure of the lateral vestibular nucleus in the rat. II. Synaptic organization. Brain Res. 18, 93–115 (1970)
Sotelo, C., Taxi, J.: Ultrastructural aspects of electrotonic junctions in the spinal cord of the frog. Brain Res. 17, 137–141 (1970)
Stensaas, L.J., Stensaas, S.S.: Light and electron microscopy of motoneurons and neuropile in the amphibian spinal cord. Brain Res. 31, 67–84 (1971)
Székely, G.: The morphology of motoneurons and dorsal root fibers in the frog's spinal cord. Brain Res. 103, 275–290 (1976)
Székely, G., Czéh, G.: Organization of locomotion. In: Frog neurobiology. A handbook (R. Llinás, W. Precht, eds.), pp. 756–792. Berlin-Heidelberg-New York: Springer 1976
Takahashi, K., Hama, K.: Some observations on the fine structure of the synaptic area in the ciliary ganglion of the chick. Z. Zellforsch. 67, 174–184 (1965)
Voss, Chr., Taugner, R.: In prepration
Washizu, Y.: Single spinal motoneurons excitable from two different antidromic pathways. Jap. J. Physiol. 10, 121–131 (1960)
Werman, R., Carlen, P.L.: Unusual bahavior of the I a EPSP in cat spinal motoneurons. Brain Res. 112, 395–401 (1976)
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Supported by the Deutsche Forschungsgemeinschaft
We thank Mrs. B. Brühl and cand. med. P. Zahn for technical assistance and Mrs. M. Wybraniec for preparing the manuscript
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Taugner, R., Sonnhof, U., Richter, D.W. et al. Mixed (chemical and electrical) synapses on frog spinal motoneurons. Cell Tissue Res. 193, 41–59 (1978). https://doi.org/10.1007/BF00221600
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DOI: https://doi.org/10.1007/BF00221600