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The structural basis for electrotonic coupling in the avian ciliary ganglion. A study with thin sectioning and freeze-fracturing

  • Published:
Journal of Neurocytology

Summary

Each ‘ciliary’ neurone in the ciliary ganglion of adult birds receives its innervation from a single myelinated fibre of the oculomotor nerve by means of a dual mode of synaptic action, electrical and chemical. The preganglionic fibre branches repeatedly around the postganglionic axon but the extracellular compartment is large. The preterminal fibres, most of which are unmyelinated, end with large boutons on the axon hillock, a few on short dendrites and on the portion of the perikaryon of the ciliary neurone from which the axon emerges. This synaptic apparatus is enveloped by a glial sheath, mainly consisting of satellite cell bodies and loose myelin lamellae. The nonsynaptic portion of the ciliary perikaryon is covered by a sheath consisting mainly of compact myelin. The ciliary neurone has an initial axon segment like that of C.N.S. neurones.

The area of each neurone apposed to boutons measures about 16 ooo μm2. Approximately 9% is specialized for chemical transmission and 0.17% for electrical transmission. Each neurone has about 280 000 gap junctional particles. Assuming that each particle represents one channel, the electrical resistance provided by these junctions is estimated to be of the order of 100 k Ω. The electrical coupling between the preganglionic fibre and the ciliary neurone may therefore be of resistive nature.

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References

  • Akert, K., Pfenninger, K. andSandri, C. (1967) Crest synapses with junctional bodies in the subfornical organ.Brain Research 5, 118–21.

    Google Scholar 

  • Bennett, M. V. L. (1972) A comparison of electrically and chemically mediated transmission. InStructure and Function of Synapses (edited byPappas, G. D. andPurpura, D. P.), pp. 221–56. New York: Raven Press.

    Google Scholar 

  • Bennett, M. V. L. (1973) Permeability and structure of electrotonic junctions and intercellular movements of tracers. InIntracellular Staining in Neurobiology (edited byKater, S. B. andNicholson, C.) pp. 115–34. New York: Springer-Verlag.

    Google Scholar 

  • Brightman, M. W. andReese, T. S. (1969) Junctions between intimately apposed cell membranes in the vertebrate brain.Journal of Cell Biology 40, 648–77.

    Google Scholar 

  • Cantino, D. andMugnaini, E. (1974) Adrenergic innervation of the parasympathetic ciliary ganglion in the chick.Science 185, 279–81.

    Google Scholar 

  • Carpenter, F. W. (1911) The ciliary ganglion of birds.Folia Neurobiologica (Leipzig) 5, 738–54.

    Google Scholar 

  • De Lorenzo, A. J. D. (1960) The fine structure of synapses in the ciliary ganglion of the chick.Journal of Biophysical and Biochemical Cytology 7, 31–6.

    Google Scholar 

  • De Lorenzo, A. J. D. (1966) Electron microscopy: tight junctions in synapses of the ciliary ganglion.Science 152, 76–8.

    Google Scholar 

  • Graham, R. C. andKarnovsky, M. J. (1966) The early stages of absorption of injected horseradish peroxidase in the proximal tubules of mouse kidney: ultrastructural cytochemistry by a new technique.Journal of Histochemistry and Cytochemistry 14, 291–302.

    Google Scholar 

  • Hámori, J. andDyachkova, L. N. (1964) Electron microscope studies on developmental differentiation of ciliary ganglion synapses in the chick.Acta Biologica Academiae Scientiarum Hungaricae 15, 213–30.

    Google Scholar 

  • Hess, A. (1965) Developmental changes in the structure of the synapse on the myelinated cell bodies of the chicken ciliar ganglion.Journal of Cell Biology 25, 1–19.

    Google Scholar 

  • Hess, A., Pilar, G. andWeakly, J. N. (1969) Correlation between transmission and structure in avian ciliary ganglion synapses.Journal of Physiology (London) 202, 339–54.

    Google Scholar 

  • Karnovsky, M. J. (1971) Use of ferrocyanide-reduced osmium tetroxide in electron microscopy. InAbstracts of Papers, Eleventh Annual Meeting, p. 146. New Orleans: American Society for Cell Biology.

    Google Scholar 

  • Koenig, H. L. (1967) Quelques particularites ultrastructurales des zones synaptiques dans le ganglion ciliare du poulet.Bulletin de l'Association des Anatomists (Paris) 52, 711–19.

    Google Scholar 

  • Kuno, M., Turkanis, S. A. andWeakly, J. N., (1971) Correlation between nerve terminal size and transmitter release at the junction of the frog.Journal of Physiology (London) 213, 545–56.

    Google Scholar 

  • Landmesser, L. andPilar, G. (1970) Selective reinnervation of two cell populations in the adult pigeon ciliary ganglion.Journal of Physiology (London) 211, 203–16.

    Google Scholar 

  • Landmesser, L. andPilar, G. (1972) The onset and development of transmission in the chick ciliary ganglion.Journal of Physiology (London) 222, 691–713.

    Google Scholar 

  • Landmesser, L. andPilar, G. (1974) Synaptic transmission and cell death during normal ganglionic development.Journal of Physiology (London) 241, 737–49.

    Google Scholar 

  • Lenhossek, Von M. (1911) Das Ganglion Ciliare der Vögel.Archiv für Mikroskopische Anatomie 76, 745–69.

    Google Scholar 

  • Martin, A. R. andPilar, G. (1963a) Dual mode of synaptic transmission in the ayian ciliary ganglion.Journal of Physiology (London) 168, 443–63.

    Google Scholar 

  • Martin, A. R. andPilar, G. (1963b) Transmission through the ciliary ganglion of the chick.Journal of Physiology (London) 168, 464–75.

    Google Scholar 

  • Martin, A. R. andPilar, G. (1964) An analysis of electrical coupling at synapses in the avian ciliary ganglion.Journal of Physiology (London) 171, 454–75.

    Google Scholar 

  • Marwitt, R., Pilar, G. andWeakly, J. N. (1971) Characterization of two ganglion cell populations in avian ciliary ganglia.Brain Research 25, 317–34.

    Google Scholar 

  • Mcnutt, S. N. andWeinstein, R. S. (1973) Membrane ultrastructure at mammalian intercellular junctions.Progress in Biophysics and Molecular Biology 26, 45–101.

    Google Scholar 

  • Milhaud, M. andPappas, G. D. (1966) Postsynaptic bodies in the habenula and interpeduncular nuclei of the cat.Journal of Cell Biology 30, 437–41.

    Google Scholar 

  • Mugnaini, E., Atluri, R. L. andHour, J. C. (1974) Fine structure of granular layer in turtle cerebellum with emphasis on large glomeruli.Journal of Neurophysiology 37, 1–29.

    Google Scholar 

  • Palay, S. L. Sotelo, C., Peters, A. andOrkand, P. M. (1968) The axon hillock and the initial axonsegment.Journal of Cell Biology 38, 193–201.

    Google Scholar 

  • Palkovits, M., Magyar, P. andSzentágothai, J. (1971) Quantitative histological analysis of the cerebellar cortex in the cat. I. Number and arrangement in space of the Purkinje cells.Brain Research 32, 1–13.

    Google Scholar 

  • Pappas, G. D. andWaxman, S. G. (1972) Synaptic fine structure-morphological correlates of chemical and electrotonic transmission. InStructure and Function of Synapses (edited byPappas, G. D. andPurpura, D. P.), pp. 1–43. New York: Raven Press.

    Google Scholar 

  • Peracchia, C. (1973a) Low resistance junctions in crayfish. I. Two arrays of globules in junctional membranes.Journal of Cell Biology 57. 54–66.

    Google Scholar 

  • Peracchia, C. (1973b) Low resistance junctions in crayfish. II. Structural details and further evidence for intracellular channels by freeze-fracture and negative staining.Journal of Cell Biology 57, 66–76.

    Google Scholar 

  • Peters, A., Palay, S. L. andWebster, H. DE F. (1970)The Fine Structure of the Nervous System, p. 56. New York: Harper and Row.

    Google Scholar 

  • Rosenbluth, J. (1962) The fine structure of acoustic ganglia in the rat.Journal of Cell Biology 12, 329–59.

    Google Scholar 

  • Rosenbluth, J. andPalay, S. L. (1961) The fine structure of nerve cell bodies and their myelin sheaths in the eighth nerve ganglion of the goldfish.Journal of Biophysical and Biochemical Cytology 9, 853–77.

    Google Scholar 

  • Seto, H. (1931) Anatomisch-histologische Studien über das Ganglion ciliare der Vogel nebst seinen ein- und austretenden Nerven. I Mit, Bei den erwachsenen Hühnern.Journal of Oriental Medicine 15, 123.

    Google Scholar 

  • Sotelo, C. (1971) General features of the synaptic organization in the central nervous system. InChemistry and Brain Development (edited byPaoletti, R. andDavison, A. N.), pp. 239–80. New York: Plenum Press.

    Google Scholar 

  • Sotelo, C. andLlinas, R. (1972) Specialized membrane junctions between neurons in the vertebrate cerebellar cortex.Journal of Cell Biology 53, 271–89.

    Google Scholar 

  • Sotelo, C. andPalay, S. L. (1970) The fine structure of the lateral vestibular nucleus in the rat. II. Synaptic organization.Brain Research 18, 93–115.

    Google Scholar 

  • Staehelin, L. A. (1974) Structure and function of intercellular junctions.International Review of Cytology 39, 191–283.

    Google Scholar 

  • Szentágothai, J. (1964) The structure of the autonomie interneuronal synapse.Acta Neurovegetativa 26, 338–59.

    Google Scholar 

  • Takahashi, K. (1967) Special somatic spine synapses in the ciliary ganglion of the chick.Zeitschrift für Zellforschung 83, 70.

    Google Scholar 

  • Takahashi, K. andHama, K. (1965) Some observations on the fine structure of the synaptic area in the ciliary ganglion of the chick.Zeitschrift für Zellforschung 67, 174–84.

    Google Scholar 

  • Taxi, J. (1965) Contribution a l'etude des connexions des neurones moteurs du système nerveux autonome.Annales des Sciences Naturelles 7, 413–674.

    Google Scholar 

  • Terzuolo, C. A. (1951) Richerche sul ganglio ciliare degli Uccelli. Connessioni e mutamenti in relazione all'eta' e dopo recisione delie fibre pregangliari.Zeitschrift für Zellforschung 36, 255–67.

    Google Scholar 

  • Vaughan, P. C. andPilar, G. Smooth muscle cells of the choroidal coat of the pigeon eye and their cholinergic innervation (submitted for publication).

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Author notes

  1. Dario Cantino

    Present address: Istituto di Anatomia Umana Normale, Università' di Torino, Italy

Authors and Affiliations

  1. Laboratory of Neuromorphology, Department of Biobehavioral Sciences, The University of Connecticut, 06268, Storrs, Connecticut, USA

    Dario Cantino & Enrico Mugnaini

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  1. Dario Cantino
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  2. Enrico Mugnaini
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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). https://doi.org/10.1007/BF01351535

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  • DOI: https://doi.org/10.1007/BF01351535

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