Skip to main content
SpringerLink
Log in

Local vesicle populations in rat superior cervical ganglia and the vesicle hypothesis

  • Published:
Journal of Neurocytology

Summary

The ‘local vesicle population’ (LVP), namely the population of synaptic vesicles lying in a zone 0.25 μm wide adjacent to the presynaptic membrane, has been measured at synapses of rat superior cervical ganglia fixed for electron microscopy following experiments performed during a 60 min periodin vitro. The mean LVP of 78 synapses in three unstimulated control ganglia was 122.0 ± s.e. 5·9 vesicles μm-2. Ganglia fixed 1 min after 3 min 10 Hz tetani of the preganglionic nerve had a significantly (P<0.001) higher mean LVP (158.0 ± s.e. 5·0). Replacement of the Ca2+ of the bathing medium by Mg2+ for the final 30 min did not affect the mean LVP of unstimulated ganglia but prevented the increase following preganglionic stimulation. When a bathing medium with Mg2+ replaced by Ca2+, or when a drug such as caffeine, morphine or adrenaline was present for the final 30 min of the experimental period, preganglionic nerve stimulation reduced the mean LVP below the mean value in paired unstimulated ganglia.

The findings are discussed in the light of recent ideas of transmitter physiology and it is concluded that they are compatible with the concept that synaptic vesicles contain, or are associated with, the synaptic transmitter.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Bailey, N. T. J. (1959)Statistical Methods in Biology. London: English University Press.

    Google Scholar 

  • Betz, W. J. (1970) Depression of transmitter release at the neuromuscular junction of thefrog.Journal of Physiology (London) 206, 629–44.

    Google Scholar 

  • Bianchi, C. P. (1968) Pharmacological action in excitation contraction coupling in striated muscle.Federation Proceedings 27, 126–31.

    PubMed  Google Scholar 

  • Birks, R. I. (1971) Effects of stimulation on synaptic vesicles in sympathetic ganglia as shown by fixation in the presence of Mg2+.Journal of Physiology (London) 216, 26–27P.

    Google Scholar 

  • Birks, R. I. andMacintosh, F. C. (1961) Acetylcholine metabolism of a sympathetic ganglion.Canadian Journal of Biochemistry and Physiology 39, 787–827.

    Google Scholar 

  • Christ, D. D. andNishi, S. (1971a). Effects of adrenaline on nerve terminals in the superior cervical ganglion of the rabbit.British Journal of Pharmacology 41, 331–38.

    PubMed  Google Scholar 

  • Christ, D. D. andNishi, S. (1971b) Site of adrenaline blockade in the superior cervical ganglion of therabbit.Journal of Physiology (London) 213, 107–18.

    Google Scholar 

  • Christensen, B. N. andMartin, A. R. (1970) Estimates of the probability of transmitter release at the mammalian neuromuscular junction.Journal of Physiology (London) 210, 933–46.

    Google Scholar 

  • Collier, B. andKatz, H. S. (1971) The synthesis, turnover and release of surplus acetylcholine in a sympathetic ganglion.Journal of Physiology (London) 214, 537–52.

    Google Scholar 

  • Crossland, J. andSlater, P. (1968) The effects of some drugs on the ‘free’ and ‘bound’ acetylcholine of rat brain.British Journal of Pharmacology and Chemotherapy 33, 42–47.

    Google Scholar 

  • Curtis, D. R. andEccles, J. C. (1960) Synaptic action during and after repetitive stimulation.Journal of Physiology (London) 150, 374–98.

    Google Scholar 

  • Elfvin, L. G. (1963) Ultrastructure of the superior cervical ganglion of the cat. II. The structure of the preganglionic end fibres and the synapses as studied by serial sections.Journal of Ultrastructure Research 8, 441–76.

    Google Scholar 

  • Grynszpan-Winograd, O. (1971) Morphological aspects of exocytosis in the adrenal medulla.Philosophical Transactions of the Royal Society, Series B 261, 291–92.

    Google Scholar 

  • Harvey, A. M. andMacintosh, F. C. (1960) Calcium and synaptic transmission in a sympathetic ganglion.Journal of Physiology (London) 97, 408–16.

    Google Scholar 

  • Hoffmann, W. W. (1969) Caffeine effects on transmitter depletion and mobilisation at motor nerve terminals.American Journal of Physiology 216, 621–29.

    PubMed  Google Scholar 

  • Hubbard, J. I. (1961) The effect of calcium and magnesium on the spontaneous release of transmitter from mammalian motor nerve terminals.Journal of Physiology (London) 159, 507–17.

    Google Scholar 

  • Hubbard, J. I. (1963) Repetitive stimulation at the mammalian neuromuscular junction and the mobilisation of transmitter.Journal of Physiology (London) 169, 640–62.

    Google Scholar 

  • Hubbard, J. I., Jones, S. F. andLandau, E. M. (1968) On the mechanisms by which calcium and magnesium affect the spontaneous release of transmitter from mammalian motor nerve terminals.Journal of Physiology (London) 194, 355–80.

    Google Scholar 

  • Hubbard, J. I. andKwanbunbumpen, S. (1968) Evidence for the vesicle hypothesis.Journal of Physiology (London) 194 407–20.

    Google Scholar 

  • Hutter, O. F. andKostial, K. (1954) The effect of magnesium and calcium ions on the release of acetylcholine.Journal of Physiology (London) 124, 234–41.

    Google Scholar 

  • Jones, S. F. andKwanbunbumpen, S. (1970) The effects of nerve stimulation and hemicholinium on synaptic vesicles at the mammalian neuromuscular junction.Journal of Physiology (London) 207, 31–50.

    Google Scholar 

  • Krnjevic, K. andMiledi, R. (1958) Some effects produced by adrenaline upon neuromuscular propagation in rats.Journal of Physiology (London) 141, 291–304.

    Google Scholar 

  • Larrabee, M. G. andBronk, D. W. C. (1947) Prolonged facilitation of synaptic excitation in sympathetic ganglion.Journal of Neurophysiology 10, 139–54.

    Google Scholar 

  • Liley, A. W. andNorth, K. A. K. (1953) An electrical investigation of effects of repetitive stimulation on mammalian neuromuscular junction.Journal of Neurophysiology 16, 509–27.

    PubMed  Google Scholar 

  • Mcewen, L. M. (1956) The effect on the isolated rabbit heart of vagal stimulation and its modification by cocaine, hexamethonium and ouabain.Journal of Physiology (London) 131, 678–89.

    Google Scholar 

  • Martin, A. R. andPilar, G. (1964) Presynaptic and postsynaptic events during post-tetanic potentiation and facilitation in the avian ciliary ganglion.Journal of Physiology (London) 175, 17–30.

    Google Scholar 

  • Mather, K. (1965)Statistical Analysis in Biology, 5th Edn. London: Methuen.

    Google Scholar 

  • Nagasawa, J., Douglas, W. W. andSchultz, R. A. (1970) Ultrastructural evidence of secretion by exocytosis and of ‘synaptic vesicle’ formation in posterior pituitary glands.Nature (London) 227, 407–9.

    Google Scholar 

  • Párducz, Á., Fehér, O. andJoó, F. (1971) Effects of stimulation and of hemicholinium (HC-3) on the fine structure of nerve endings in the superior cervical ganglion of the cat.Brain Research 34, 61–72.

    PubMed  Google Scholar 

  • Perri, V., Sacchi, O., Raviola, E. andRaviola, G. (1972) Evaluation of the number and distribution of synaptic vesicles at cholinergic nerve-endings after sustained stimulation.Brain Research 39, 526–29.

    PubMed  Google Scholar 

  • Pysh, J. J. andWiley, R. G. (1972) Morphological alterations in electrically stimulated superior cervical ganglia of the cat.Science 176, 191–93.

    PubMed  Google Scholar 

  • Quilliam, J. P. andTamarind, D. L. (1969) Experimental modification of synaptic vesicle populations in synapses of the rat superior cervical ganglion.Fourth International Congress on Pharmacology (Basel), Abstracts p. 146.

  • Quilliam, J. P. andTamarind, D. L. (1970) The vesicle population of rat ganglionic synapses and the effects of some drugs.British Journal of Pharmacology 39, 244P.

    Google Scholar 

  • Reynolds, E. S. (1963) The use of lead citrate at high pH as an electron-opaque stain in electron microscopy.Journal of Cell Biology 17, 208–12.

    PubMed  Google Scholar 

  • Rosenthal, J. (1969) Post-tetanic potentiation at the neuromuscular junction of the frog.Journal of Physiology (London) 203, 121–33.

    Google Scholar 

  • Tamarind, D. L. andQuilliam, J. P. (1971) Synaptic organization and other ultrastructural features of the superior cervical ganglion of the rat, kitten and rabbit.Micron 2, 204–34.

    Google Scholar 

  • Whittaker, V. P. (1970) The vesicle hypothesis. InExcitatory Synaptic Mechanisms (edited byAnderson, P. andJansen, J. S.) pp. 67–76. Oslo, Bergen, Tronsö: Oslo University Press.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Pharmacology, St Bartholomew's Hospital Medical College, Charterhouse Square, EC1, London

    J. P. Quilliam & D. L. Tamarind

Authors
  1. J. P. Quilliam
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. D. L. Tamarind
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Quilliam, J.P., Tamarind, D.L. Local vesicle populations in rat superior cervical ganglia and the vesicle hypothesis. J Neurocytol 2, 59–75 (1973). https://doi.org/10.1007/BF01099208

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01099208

Keywords

Search

Navigation