Skip to main content
Log in

Calcium Transients and Transmitter Secretion in Different Parts of Frog Nerve Endings in Different Conditions of Calcium Ion Influx

  • Published:
Neuroscience and Behavioral Physiology Aims and scope Submit manuscript

Experiments on frog neuromuscular preparations were performed to study the characteristics of the calcium response and the quantum secretion of acetylcholine in different pats of extended nerve terminals in different conditions of calcium influx. A calcium-sensitive fluorescent dye was used to analyze Ca2+ influx (Ca2+ transients) into the proximal and distal parts of nerve endings in conditions of increased K+ ion content, in response to blockers of N- and L-type calcium channels, and on blockade of calcium-activated potassium channels. These studies showed that at a uniform distribution density of voltage-gated calcium channels along nerve endings, the proximal-to-distal decrement in calcium transients and quantum secretion intensity persisted in conditions of additional opening of voltage-gated calcium channels by potassium depolarization, on “thinning” of these channels using specific blockers, but changed on blockade of calcium-activated potassium channels.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. N. Burnashev and A. Rozov, “Presynaptic Ca2+ dynamics, Ca2+ buffers and synaptic efficacy,” Cell Calcium, 37, No. 5, 489–495 (2005).

    Article  CAS  PubMed  Google Scholar 

  2. J. G. Borst and B. Sakmann, “Calcium influx and transmitter release in a fast CNS synapse,” Nature, 383, No. 6599, 431–434 (1996).

    Article  CAS  PubMed  Google Scholar 

  3. B. Yazejian, D. A. DiGregorio, J. L. Vergara, et al., “Direct measurements of presynaptic calcium and calcium-activated potassium currents regulating neurotransmitter release at cultured Xenopus nerve-muscle synapses,” J. Neurosci., 17, No. 9, 2990–3001 (1997).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. R. Y. Tsien, “Fluorescence ratio imaging of dynamic intracellular signals,” Acta Physiol. Scand., 582, Suppl., 6 (1989).

  5. M. R. Bennett and N. A. Lavidis, “Quantal secretion at release sites of nerve terminals in toad (Bufomarinus) muscle during formation of topographical maps,” J. Physiol., 401, 567–579 (1988).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. B. M. Nudell and A. D. Grinnell, “Inverse relationship between transmitter release and terminal length in synapses on frog muscle fibers of uniform input resistance,” J. Neurosci., 2, No. 2, 216–224 (1982).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. A. Mallart, “Presynaptic currents in frog motor endings,” Pflügers Arch., 400, No. 1, 8–13 (1984).

    Article  CAS  PubMed  Google Scholar 

  8. B. Katz and R. Miledi, “The effect of local blockage of motor nerve terminals,” J. Physiol., 199, No. 3, 729–741 (1968).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. M. Braun and R. F. Schmidt, “Potential changes recorded from the frog motor nerve terminal during its activation,” Pflügers Arch. Gesamte Physiol. Menschen Tiere, 287, No. 1, 56–80 (1966).

    Article  CAS  PubMed  Google Scholar 

  10. A. L. Zefirov and I. A. Khalilov, “Analysis of electrical activity in different parts of amphibian nerve endings. Physiology of mediators. The peripheral synapse,” in: Abstr. 5th All-Union Symp., Kazan, June 1984, pp. 97–99.

  11. M. R. Bennett and N. A. Lavidis, “Variation in quantal secretion at different release sites along developing and mature motor terminal branches,” Brain Res., 281, No. 1, 1–9 (1982).

    Article  Google Scholar 

  12. A. J. D’Alonzo and A. D. Grinnell, “Profiles of evoked release along the length of frog motor nerve terminals,” J. Physiol., 359, 235–258 (1985).

    Article  PubMed  PubMed Central  Google Scholar 

  13. M. R. Bennett, P. Jones, and N. A. Lavidis, “The probability of quantal secretion along visualized terminal branches at amphibian (Bufomarinus) neuromuscular synapses,” J. Physiol., 379, 257–274 (1986).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. E. Bukcharaeva, D. Samigullin, E. E. Nikolsky, and F. Vyskocil, “Cyclic AMP synchronizes evoked quantal release at frog neuromuscular junctions,” Physiol. Res., 49, No. 4, 475–479 (2000).

    CAS  PubMed  Google Scholar 

  15. D. F. Davey and M. R. Bennett, “Variation in the size of synaptic contacts along developing and mature motor terminal branches,” Brain Res., 281, No. 1, 11–22 (1982).

    Article  CAS  PubMed  Google Scholar 

  16. M. R. Bennett, N. A. Lavidis, and F. M. Armson, “Changes in the dimensions of release sites along terminal branches at amphibian neuromuscular synapses,” J. Neurocytol., 16, No. 2, 221–237 (1987).

    Article  CAS  PubMed  Google Scholar 

  17. E. Khaziev, A. Golovyahina, E. Bukharaeva, et al., “Action of ATP on Ca2+-transient in different parts of the frog motor nerve ending,” BioNanoScience (2017), doi: https://doi.org/10.1007/s12668-016-0350-6.

  18. D. V. Samigullin, A. L. Vasin, E. A. Bukharaeva, and E. E. Nikolsky, “Characteristics of calcium transient in different parts of frog nerve terminal in response to nerve impulse,” Dokl. Biol. Sci., 431, No. 1, 83–85 (2010).

    Article  CAS  PubMed  Google Scholar 

  19. L. F. Nurullin, A. R. Mukhitov, A. N. Tsentsevytsky, et al., “Voltagedependent P/Q-type calcium channels at the frog neuromuscular junction,” Physiol. Res., 60, 815–823 (2011).

    Article  CAS  PubMed  Google Scholar 

  20. Y. Y. Peng and R. S. Zucker, “Release of LHRH is linearly related to the time integral of presynaptic Ca2 elevation above a threshold level in bullfrog sympathetic ganglia,” Neuron, 10, No. 3, 465–473 (1993).

    Article  CAS  PubMed  Google Scholar 

  21. E. Neher, “The use of fura-2 for estimating Ca buffers and Ca fluxes,” Neuropharmacology, 34, No. 11, 1423–1442 (1995).

    Article  CAS  PubMed  Google Scholar 

  22. V. Shahrezaei, A. Cao, and K. R. Delaney, “Ca2+ from one or two channels controls fusion of a single vesicle at the frog neuromuscular junction,” J. Neurosci., 26, No. 51, 13,240–13,249 (2006).

    Article  CAS  Google Scholar 

  23. D. V. Samigullin, E. F. Khaziev, N. V. Zhilyakov, et al., “Loading a calcium dye into frog nerve endings through the nerve stump: calcium transient registration in the frog neuromuscular junction,” J. Vis. Exp., (125) e55122 (2017), doi: https://doi.org/10.3791/55122.

    Article  CAS  Google Scholar 

  24. J. Del Castillo and B. Katz, “Quantal components of the end-plate potential,” J. Physiol., 124, 560–573 (1954).

    Article  PubMed Central  Google Scholar 

  25. D. P. Matyushkin, I. A. Shabunova, G. M. Sharovarova, and I. M. Vinogradova, “On potassium functional feedback in neuromuscular junction,” J. Neurosci. Res., 3, 441–450 (1978).

    Article  CAS  PubMed  Google Scholar 

  26. E. Khaziev, D. Samigullin, N. Zhilyakov, et al., “Acetylcholineinduced inhibition of presynaptic calcium signals and transmitter release in the frog neuromuscular junction,” Front. Physiol., 7, 621 (2016), doi: https://doi.org/10.3389/fphys.2016.00621.

  27. A. N. Tsentsevitsky, D. V. Samigullin, L. F. Nurullin, et al., “Presynaptic voltage-dependent calcium channels at the frog neuromuscular junction,” in: Frogs: Genetic Diversity, Neural Development and Ecological Implications, Nova Science Publishers Inc., New York (2014), Chpt. 5, pp. 179–194, ISBN: 978-1-63117-626-5.

  28. R. Roncarati, M. Di Chio, A. Sava, et al., “Presynaptic localization of the small conductance calcium-activated potassium channel SK3 at the neuromuscular junction,” Neuroscience, 104, No. 1, 253–262 (2001).

    Article  CAS  PubMed  Google Scholar 

  29. E. A. Bukcharaeva, K. C. Kim, J. Moravec, et al., “Noradrenaline synchronizes evoked quantal release at frog neuromuscular junctions,” J. Physiol., 517, No. 3, 879–888 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Z. P. Pang and T. C. Südhof, “Cell biology of Ca2+-triggered exocytosis,” Curr. Opin. Cell Biol., 22, No. 4, 496–505 (2010), doi: https://doi.org/10.1016/j.ceb.2010.05.001.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. R. Robitaille, E. M. Adler, and M. P. Charlton, “Strategic location of calcium channels at transmitter release sites of frog neuromuscular synapses,” Neuron, 5, 773–779 (1990).

    Article  CAS  PubMed  Google Scholar 

  32. J. M. Pattillo, B. Yazejian, D. A. DiGregorio, et al., “Contribution of presynaptic calcium-activated potassium currents to transmitter release regulation in cultured Xenopus nerve-muscle synapses,” Neuroscience, 102, 229–240 (2001).

    Article  CAS  PubMed  Google Scholar 

  33. M. Dittrich, A. E.Homan, and S. D.Meriney, “Presynaptic mechanisms controlling calcium-triggered transmitter release at the neuromuscular junction,” Curr. Opin. Physiol., 4, 15–24 (2018), doi: https://doi.org/10.1016/j.cophys.2018.03.004.

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to E. F. Khaziev.

Additional information

Translated from Rossiiskii Fiziologicheskii Zhurnal imeni I. M. Sechenova, Vol. 105, No. 10, pp. 1262–1270, October, 2019.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Khaziev, E.F., Balashova, D.V., Tsentsevitsky, A.N. et al. Calcium Transients and Transmitter Secretion in Different Parts of Frog Nerve Endings in Different Conditions of Calcium Ion Influx. Neurosci Behav Physi 50, 914–919 (2020). https://doi.org/10.1007/s11055-020-00985-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11055-020-00985-0

Keywords

Navigation