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The fine structure of freeze-fractured presynaptic membranes

  • Published:
Journal of Neurocytology

Summary

Electron micrographs of presynaptic membrane faces were obtained from replicas of aldehyde-fixed, freeze-fractured neuropil of mammalian and avian C.N.S. There is strong evidence that the presynaptic membrane is split and that the exposed membrane faces represent the inner and outer membrane leaflet respectively. Presynaptic sites on the inner face appear as patches adhering to postsynaptic elements and include a distinctly indented area. They bear clusters of membrane particles and a varying number of small protuberances. The latter apparently occur in presynaptic membranes exclusively and form hexagonal patterns corresponding to the ‘presynaptic vesicular grid’. Evidence is presented that the protuberances are temporary attachment sites of transmitter vesicles to the presynaptic membrane. These contacts may be identical with the sites of transmitter release.

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References

  • Akert, K., Moor, H. andPfenninger, K. (1971) Synaptic fine structure. InAdvances in Cytopharmacology (edited byClementi, F. andCeccarelli, B.) Vol. 1, pp. 273–90. New York: Raven Press.

    Google Scholar 

  • Akert, K., Moor, H., Pfenninger, K. andSandri, C. (1969) Contribution of new impregnation methods and freeze-etching to the problems of synaptic fine structure.Progress in Brain Research 31, 223–40.

    Google Scholar 

  • Akert, K. andPfenninger, K. (1969) Synaptic fine structure and neural dynamics. InCellular Dynamics of the Neuron (edited byBarondes, S. H.). ISCB Symposium Paris, Vol. 8, pp. 245–60. New York: Academic Press.

    Google Scholar 

  • Akert, K., Pfenninger, K., Sandri, C. andMoor, H. (1972) Freeze-etching and cytochemistry of vesicles and membrane complexes in synapses of the C.N.S. InStructure and Function of Synapses (edited byPappas, G. D. andPurpura, D. P.), pp. 67–86. New York: Raven Press.

    Google Scholar 

  • Akert, K. andSandri, C. (1970) Identification of the active synaptic region by means of histochemical and freeze-etching techniques. InExcitatory Synaptic Mechanisms (edited byAndersen, P. andJansen, J. K. S.), pp. 27–41. Oslo: Universitetsforlaget.

    Google Scholar 

  • Bennett, M. V. L., Nakajima, Y. andPappas, G. D. (1967) Physiology and ultrastructure of electrotonic junctions. III. Giant electromotor neurons ofMalapterurus electricus.Journal of Neurophysiology 30, 209–35.

    Google Scholar 

  • Bloom, F. E., Iversen, L. L. andSchmitt, F. O. (Editors) (1970) Macromolecules in synaptic function.Neurosciences Research Program Bulletin 8, 325–455.

    Google Scholar 

  • Branton, D. (1966) Fracture faces of frozen membranes.Proceedings of the National Academy of Science U.S. 55, 1048–56.

    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 

  • Clark, A. W. andBranton, D. (1968). Fracture faces in frozen outer segments from the guinea pig retina.Zeitschrift für Zellforschung und Mikroskopische Anatomie 91, 586–603.

    Google Scholar 

  • Couteaux, R. andPécot-Dechavassine, M. (1970a) L'ouverture des vésicules synaptiques au niveau des ‘zones actives’.Microscopic Electronique, Vol.III, pp. 709–10. Paris: Société Française de Microscopie Electronique.

    Google Scholar 

  • Couteaux, R. andPécot-Dechavassine, M. (1970b) Vésicules synaptiques et poches au niveau des ‘zones actives’ de la jonction neuromusculaire.Comptes Rendues de l'Académie des Sciences Paris 271, 2346–9.

    Google Scholar 

  • Gall, J. G. (1967) The light microscope as an optical diffractometer.Journal of Cell Science 2, 163–8.

    Google Scholar 

  • Goodenough, D. A. andRevel, J. P. (1970) A fine structural analysis of intercellular junctions in the mouse liver.Journal of Cell Biology 45, 272–90.

    Google Scholar 

  • Gray, E. G. (1959) Axo-somatic and axo-dendritic synapses of the cerebral cortex: An electron microscope study.Journal of Anatomy (London) 93, 420–33.

    Google Scholar 

  • Gray, E. G. (1966) Problems of interpreting the fine structure of vertebrate and invertebrate synapses.International Review of Genetics and Experimental Zoology 2, 139–70.

    Google Scholar 

  • Katz, B. (1969) The release of neural transmitter substances. The Sherrington Lectures X. Liverpool: University Press.

    Google Scholar 

  • Loewenstein, W. R. (1966) Permeability of membrane junctions.Annals of the New York Academy of Sciences 137, 441–72.

    Google Scholar 

  • Markham, R., Frey, S. andHills, G. (1963) Methods for the enhancement of image detail and accentuation of structure in electron microscopy.Virology 20, 88–102.

    Google Scholar 

  • Moor, H. andMühlethaler, K. (1963) Fine structure in frozen-etched yeast cells.Journal of Cell Biology 17, 609–28.

    Google Scholar 

  • Moor, H., Pfenninger, K. andAkert, K. (1969) Synaptic vesicles in electron micrographs of freeze-etched nerve terminals.Science 164, 1405–07.

    Google Scholar 

  • Nickel, E. andGrieshaber, E. (1969) Elektronenmikroskopische Darstellung der Muskelkapillaren im Gefrierätzbild.Zeitschrift für Zellforschung und Mikroskopische Anatomie 95, 445–61.

    Google Scholar 

  • Nickel, E. andPotter, L. T. (1970) Synaptic vesicles in freeze-etched electric tissue of Torpedo.Brain Research 23, 95–100.

    Google Scholar 

  • Palade, G. E. andBruns, R. R. (1968) Structural modulations of plasmalemmal vesicles.Journal of Cell Biology 37, 633–49.

    Google Scholar 

  • Payton, B. W., Bennett, M. V. L. andPappas, G. D. (1969) Permeability and structure of junctional membranes at an electrotonic synapse.Science 166, 1641–3.

    Google Scholar 

  • Pfenninger, K. (1971a) The cytochemistry of synaptic densities. I. An analysis of the bismuth iodide impregnation method.Journal of Ultrastructure Research 34, 103–22.

    Google Scholar 

  • Pfenninger, K. (1971b) The cytochemistry of synaptic densities. II. Proteinaceous components and mechanism of synaptic connectivity.Journal of Ultrastructure Research 35, 451–75.

    Google Scholar 

  • Pfenninger, K. (1971c) Freeze-etching of presynaptic membranes: ‘Synaptopores’ as a morphological basis of transmitter release? Inaugural-Dissertation. Zürich University.

  • Pfenninger, K., Akert, K., Moor, H. andSandri, C. (1971a) Das Gefrierätzbild der präsynaptischen Membran.Acta Anatomica 79, 148 (Abstract).

    Google Scholar 

  • Pfenninger, K., Akert, K., Moor, H. andSandri, C. (1971b) Freeze-fracturing of presynaptic membranes in the central nervous system.Philosophical Transactions of the Royal Society of London B 261, 387–8.

    Google Scholar 

  • Pfenninger, K., Akert, K. andSandri, C. (1970) Structural organization of the synaptic cleft: Polyionic binding between pre- and postsynaptic membranes.Microscopie Electronique Vol.III pp. 715–16. Paris: Société Française de Microscopie Electronique.

    Google Scholar 

  • Pfenninger, K., Akert, K., Sandri, C. andMoor, H. (1971) Ultrastructure of transmitter release.Experientia 27, 11.

    Google Scholar 

  • Pfenninger, K., Sandri, C., Akert, K. andEugster, C. H. (1969) Contribution to the problem of structural organization of the presynaptic area.Brain Research 12, 10–18.

    Google Scholar 

  • Pinto da Silva, P. andBranton, D. (1970) Membrane splitting in freeze-etching.Journal of Cell Biology 45, 598–605.

    Google Scholar 

  • Robertson, J. D. (1963) The occurrence of a subunit pattern in the unit membranes of club endings in Mauthner cell synapses in goldfish brains.Journal of Cell Biology 19, 201–21.

    Google Scholar 

  • Spycher, M. A. (1970) Intercellular adhesions. An electron microscope study on freeze-etched rat hepatocytes.Zeitschrift für Zellforschung und Mikroskopische Anatomie III, 64–74.

    Google Scholar 

  • Spycher, M. A. (1971) Personal communication.

  • Tillack, T. W. andMarchesi, V. T. (1970) Demonstration of the outer surface of freeze-etched red blood cell membranes.Journal of Cell Biology 45, 649–53.

    Google Scholar 

  • Van Der Loos, H. (1963) Fine structure of synapses in the cerebral cortex.Zeitschrift für Zellforschung und Mikroskopische Anatomie 60, 815–25.

    Google Scholar 

  • Wehrli, E., Mühlethaler, K. andMoor, H. (1970) Membrane structure as seen with a double replica method for freeze-fracturing.Experimental Cell Research 59, 336–9.

    Google Scholar 

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Pfenninger, K., Akert, K., Moor, H. et al. The fine structure of freeze-fractured presynaptic membranes. J Neurocytol 1, 129–149 (1972). https://doi.org/10.1007/BF01099180

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  • DOI: https://doi.org/10.1007/BF01099180

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