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. 1988 Jun;400:335–348. doi: 10.1113/jphysiol.1988.sp017123

Analysis of quantal acetylcholine noise at end-plates of frog muscle during rapid transmitter secretion.

P C Molenaar 1, B S Oen 1
PMCID: PMC1191810  PMID: 3262154

Abstract

1. Using the theory of noise analysis an attempt was made to measure frequency and amplitude of miniature end-plate potentials (MEPPs) under conditions of vigorous transmitter release. Frog sartorius muscles were incubated in a depolarizing (32 mM-K+) medium which lacked Ca2+ to prevent transmitter release. Subsequently, when the membrane potential had become stable at about -40 mV, end-plates were superfused with 4 mM-Ca2+-containing medium for 1 min periods with 5 min intervals between the superfusions. 2. Most junctions ('fast' type) responded to Ca2+ with a relatively large, noisy depolarization (5.8-14.5 mV) which subsided rapidly during subsequent challenges with Ca2+. Other junctions ('slow' type) responded with only 1-1.6 mV depolarizations which were rather well sustained during the consecutive Ca2+ applications. 3. From the variance, E2, and the depolarization, V, caused by Ca2+ the frequency n and amplitude factor q of the MEPPs were calculated. Values of n were 3-4 x 10(4) and 0.1-1 x 10(4) s-1 in the fast- and slow-type junctions, respectively. The mean value of q was 0.16 mV; it remained more or less constant in the fast-type junctions, but tended to decline in the slow-type junctions. 4. As expected, cholinesterase inhibitors potentiated V and E2 as well as individual MEPPs. However, no advantage could be taken from this finding, since these drugs caused burst-like peaks superimposed on the voltage signal, precluding application of noise analysis. 5. The results strongly suggest that, at least in the fast-type junctions, K+ caused an extremely rapid depletion of the store of transmitter quanta, whose mean size did not change appreciably in the course of the experiment. However, in the slow-type junctions during prolonged incubation, it cannot be excluded that the gradual decline of q was due to the release of newly formed, unripe quanta.

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Selected References

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  1. Bevan S. Sub-miniature end-plate potentials at untreated frog neuromuscular junctions. J Physiol. 1976 Jun;258(1):145–155. doi: 10.1113/jphysiol.1976.sp011411. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Ceccarelli B., Grohovaz F., Hurlbut W. P. Freeze-fracture studies of frog neuromuscular junctions during intense release of neurotransmitter. II. Effects of electrical stimulation and high potassium. J Cell Biol. 1979 Apr;81(1):178–192. doi: 10.1083/jcb.81.1.178. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Ceccarelli B., Hurlbut W. P., Mauro A. Turnover of transmitter and synaptic vesicles at the frog neuromuscular junction. J Cell Biol. 1973 May;57(2):499–524. doi: 10.1083/jcb.57.2.499. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Ceccarelli B., Hurlbut W. P. The effects of prolonged repetitive stimulation in hemicholinium on the frog neuromuscular junction. J Physiol. 1975 May;247(1):163–188. doi: 10.1113/jphysiol.1975.sp010926. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Cooke J. D., Quastel D. M. Transmitter release by mammalian motor nerve terminals in response to focal polarization. J Physiol. 1973 Jan;228(2):377–405. doi: 10.1113/jphysiol.1973.sp010092. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Couteaux R., Pécot-Dechavassine M. Données ultrastructurales et cytochimiques sur le mécanisme de libération de l'acetylcholine dans la transmission synaptique. Arch Ital Biol. 1973 Dec;111(3-4):231–262. [PubMed] [Google Scholar]
  7. Couteaux R., Pécot-Dechavassine M. Les zones spécialisées des membranes présynaptiques. C R Acad Sci Hebd Seances Acad Sci D. 1974 Jan 7;278(2):291–293. [PubMed] [Google Scholar]
  8. DEL CASTILLO J., KATZ B. Biophysical aspects of neuro-muscular transmission. Prog Biophys Biophys Chem. 1956;6:121–170. [PubMed] [Google Scholar]
  9. DEL CASTILLO J., KATZ B. Localization of active spots within the neuromuscular junction of the frog. J Physiol. 1956 Jun 28;132(3):630–649. doi: 10.1113/jphysiol.1956.sp005554. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. DEL CASTILLO J., KATZ B. Quantal components of the end-plate potential. J Physiol. 1954 Jun 28;124(3):560–573. doi: 10.1113/jphysiol.1954.sp005129. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. FATT P., KATZ B. Spontaneous subthreshold activity at motor nerve endings. J Physiol. 1952 May;117(1):109–128. [PMC free article] [PubMed] [Google Scholar]
  12. Fesce R., Segal J. R., Hurlbut W. P. Fluctuation analysis of nonideal shot noise. Application to the neuromuscular junction. J Gen Physiol. 1986 Jul;88(1):25–57. doi: 10.1085/jgp.88.1.25. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Gage P. W. Generation of end-plate potentials. Physiol Rev. 1976 Jan;56(1):177–247. doi: 10.1152/physrev.1976.56.1.177. [DOI] [PubMed] [Google Scholar]
  14. Hartzell H. C., Kuffler S. W., Yoshikami D. Post-synaptic potentiation: interaction between quanta of acetylcholine at the skeletal neuromuscular synapse. J Physiol. 1975 Oct;251(2):427–463. doi: 10.1113/jphysiol.1975.sp011102. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Heuser J. E. Proceedings: A possible origin of the 'giant' spontaneous potentials that occur after prolonged transmitter release at frog neuromuscular junctions. J Physiol. 1974 Jun;239(2):106P–108P. doi: 10.1113/jphysiol.1974.sp010593. [DOI] [PubMed] [Google Scholar]
  16. Heuser J. E., Reese T. S. Evidence for recycling of synaptic vesicle membrane during transmitter release at the frog neuromuscular junction. J Cell Biol. 1973 May;57(2):315–344. doi: 10.1083/jcb.57.2.315. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Heuser J., Miledi R. Effects of lanthanum ions on function and structure of frog neuromuscular junctions. Proc R Soc Lond B Biol Sci. 1971 Dec 14;179(1056):247–260. doi: 10.1098/rspb.1971.0096. [DOI] [PubMed] [Google Scholar]
  18. Katz B., Miledi R. Estimates of quantal content during 'chemical potentiation' of transmitter release. Proc R Soc Lond B Biol Sci. 1979 Aug 31;205(1160):369–378. doi: 10.1098/rspb.1979.0070. [DOI] [PubMed] [Google Scholar]
  19. Katz B., Miledi R. The statistical nature of the acetycholine potential and its molecular components. J Physiol. 1972 Aug;224(3):665–699. doi: 10.1113/jphysiol.1972.sp009918. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Kriebel M. E., Florey E. Effect of lanthanum ions on the amplitude distributions of miniature endplate potentials and on synaptic vesicles in frog neuromuscular junctions. Neuroscience. 1983 Jul;9(3):535–547. doi: 10.1016/0306-4522(83)90172-0. [DOI] [PubMed] [Google Scholar]
  21. Magleby K. L., Stevens C. F. The effect of voltage on the time course of end-plate currents. J Physiol. 1972 May;223(1):151–171. doi: 10.1113/jphysiol.1972.sp009839. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. McLachlan E. M., Martin A. R. Non-linear summation of end-plate potentials in the frog and mouse. J Physiol. 1981 Feb;311:307–324. doi: 10.1113/jphysiol.1981.sp013586. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Miledi R., Molenaar P. C., Polak R. L. An analysis of acetylcholine in frog muscle by mass fragmentography. Proc R Soc Lond B Biol Sci. 1977 Jun 15;197(1128):285–297. doi: 10.1098/rspb.1977.0071. [DOI] [PubMed] [Google Scholar]
  24. Miledi R., Molenaar P. C., Polak R. L. Electrophysiological and chemical determination of acetylcholine release at the frog neuromuscular junction. J Physiol. 1983 Jan;334:245–254. doi: 10.1113/jphysiol.1983.sp014492. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Miledi R., Molenaar P. C., Polak R. L. Free and bound acetylcholine in frog muscle. J Physiol. 1982 Dec;333:189–199. doi: 10.1113/jphysiol.1982.sp014448. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Molenaar P. C., Oen B. S., Polak R. L. Effect of chloride ions on giant miniature end-plate potentials at the frog neuromuscular junction. J Physiol. 1987 Feb;383:143–152. doi: 10.1113/jphysiol.1987.sp016401. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Molenaar P. C., Polak R. L. Potassium propionate causes preferential loss of 'bound' acetylcholine in frog muscle. Neurosci Lett. 1983 Dec 30;43(2-3):209–213. doi: 10.1016/0304-3940(83)90189-1. [DOI] [PubMed] [Google Scholar]
  28. Polak R. L., Molenaar P. C. A method for determination of acetylcholine by slow pyrolysis combined with mass fragmentography on a packed capillary column. J Neurochem. 1979 Feb;32(2):407–412. doi: 10.1111/j.1471-4159.1979.tb00364.x. [DOI] [PubMed] [Google Scholar]
  29. Polak R. L., Molenaar P. C. Pitfalls in determination of acetylcholine from brain by pyrolysis-gas chromatography/mass spectrometry. J Neurochem. 1974 Dec;23(6):1295–1297. doi: 10.1111/j.1471-4159.1974.tb12230.x. [DOI] [PubMed] [Google Scholar]
  30. Segal J. R., Ceccarelli B., Fesce R., Hurlbut W. P. Miniature endplate potential frequency and amplitude determined by an extension of Campbell's theorem. Biophys J. 1985 Feb;47(2 Pt 1):183–202. doi: 10.1016/s0006-3495(85)83891-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. TAKEUCHI N. Some properties of conductance changes at the end-plate membrane during the action of acetylcholine. J Physiol. 1963 Jun;167:128–140. doi: 10.1113/jphysiol.1963.sp007136. [DOI] [PMC free article] [PubMed] [Google Scholar]

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