Skip to main content
PMC home page
The Journal of Physiology logoLink to The Journal of Physiology
. 1994 Jun 15;477(Pt 3):497–502. doi: 10.1113/jphysiol.1994.sp020210

Role of non-quantal acetylcholine release in surplus polarization of mouse diaphragm fibres at the endplate zone.

E E Nikolsky 1, H Zemková 1, V A Voronin 1, F Vyskocil 1
PMCID: PMC1155613  PMID: 7932237

Abstract

1. In mouse diaphragm, with intact cholinesterase (ChE), the mean value of the resting membrane potential was significantly higher (-84.8 +/- 0.3 mV; mean +/- S.E.M.) at the endplate zone than in the extrajunctional area of the muscle fibres (-82.5 +/- 0.3 mV) at 22 degrees C. 2. This hyperpolarization of about 2-3 mV at the endplate zone was abolished within 5 min by 1 x 10(-6) M ouabain, indicating that it might be caused by an electrogenic Na(+)-K+ pump. (+)-Tubocurarine (TC; 1 x 10(-5) M) had no effect on this hyperpolarization after bath application for 10-20 min. 3. Short-term denervation (4 h), a slight increase of Mg2+ in the bath of from 1 to 4 mM and application of a Ca(2+)-free solution for 60 min also led to the disappearance of the surplus polarization. All of these factors are known to eliminate TC-induced hyperpolarization in anti-ChE-treated muscles (H-effect), which is considered to be a correlate of non-quantal acetylcholine (ACh) leakage. 4. The time courses of the decline of the H-effect and surplus polarization after denervation were identical. 5. In short-term denervated muscles with intact ChE, the surplus polarization was restored by 5 x 10(-8) M ACh, which simulates the H-effect in anti-ChE-treated muscles. The presence of 1 x 10(-6) M ouabain either prevented or abolished the effect of the bath-applied ACh.(ABSTRACT TRUNCATED AT 250 WORDS)

Full text

PDF

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Beam K. G., Caldwell J. H., Campbell D. T. Na channels in skeletal muscle concentrated near the neuromuscular junction. Nature. 1985 Feb 14;313(6003):588–590. doi: 10.1038/313588a0. [DOI] [PubMed] [Google Scholar]
  2. Betz W. J., Caldwell J. H., Kinnamon S. C. Increased sodium conductance in the synaptic region of rat skeletal muscle fibres. J Physiol. 1984 Jul;352:189–202. doi: 10.1113/jphysiol.1984.sp015286. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bray J. J., Forrest J. W., Hubbard J. I. Evidence for the role of non-quantal acetylcholine in the maintenance of the membrane potential of rat skeletal muscle. J Physiol. 1982 May;326:285–296. doi: 10.1113/jphysiol.1982.sp014192. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Dlouhá H., Teisinger J., Vyskocil F. Activation of membrane Na+/K+-ATPase of mouse skeletal muscle by acetylcholine and its inhibition by alpha-bungarotoxin, curare and atropine. Pflugers Arch. 1979 May 15;380(1):101–104. doi: 10.1007/BF00582620. [DOI] [PubMed] [Google Scholar]
  5. Dlouhá H., Teisinger J., Vyskocil F. The effect of vanadate on the electrogenic Na+/K+ pump, intracellular Na+ concentration and electrophysiological characteristics of mouse skeletal muscle fibre. Physiol Bohemoslov. 1981;30(1):1–10. [PubMed] [Google Scholar]
  6. Dolezal V., Tucek S. The synthesis and release of acetylcholine in normal and denervated rat diaphragms during incubation in vitro. J Physiol. 1983 Jan;334:461–474. doi: 10.1113/jphysiol.1983.sp014506. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Dolezal V., Vyskocil F., Tucek S. Decrease of the spontaneous non-quantal release of acetylcholine from the phrenic nerve in botulinum-poisoned rat diaphragm. Pflugers Arch. 1983 Jun 1;397(4):319–322. doi: 10.1007/BF00580268. [DOI] [PubMed] [Google Scholar]
  8. Drachman D. B., Stanley E. F., Pestronk A., Griffin J. W., Price D. L. Neurotrophic regulation of two properties of skeletal muscle by impulse-dependent and spontaneous acetylcholine transmission. J Neurosci. 1982 Feb;2(2):232–243. doi: 10.1523/JNEUROSCI.02-02-00232.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Ecobichon D. J., Israel Y. Characterization of the esterases from electric tissue of Electrophorus by starch-gel electrophoresis. Can J Biochem. 1967 Jul;45(7):1099–1105. doi: 10.1139/o67-127. [DOI] [PubMed] [Google Scholar]
  10. GOLDUP A., LUCKHURST G. R., SWANTON W. T. Gas-liquid chromatography-variations in partition coefficients with carrier gas. Nature. 1962 Jan 27;193:333–334. doi: 10.1038/193333a0. [DOI] [PubMed] [Google Scholar]
  11. Giniatullin R. A., Khamitov G., Khazipov R., Magazanik L. G., Nikolsky E. E., Snetkov V. A., Vyskocil F. Development of desensitization during repetitive end-plate activity and single end-plate currents in frog muscle. J Physiol. 1989 May;412:113–122. doi: 10.1113/jphysiol.1989.sp017606. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Giniatullin R. A., Khazipov R. N., Oranska T. I., Nikolsky E. E., Voronin V. A., Vyskocil F. The effect of non-quantal acetylcholine release on quantal miniature currents at mouse diaphragm. J Physiol. 1993 Jul;466:105–114. [PMC free article] [PubMed] [Google Scholar]
  13. Grinnell A. D., Gundersen C. B., Meriney S. D., Young S. H. Direct measurement of ACh release from exposed frog nerve terminals: constraints on interpretation of non-quantal release. J Physiol. 1989 Dec;419:225–251. doi: 10.1113/jphysiol.1989.sp017871. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Haimovich B., Schotland D. L., Fieles W. E., Barchi R. L. Localization of sodium channel subtypes in adult rat skeletal muscle using channel-specific monoclonal antibodies. J Neurosci. 1987 Sep;7(9):2957–2966. doi: 10.1523/JNEUROSCI.07-09-02957.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Katz B., Miledi R. Does the motor nerve impulse evoke 'non-quantal' transmitter release? Proc R Soc Lond B Biol Sci. 1981 May 7;212(1186):131–137. doi: 10.1098/rspb.1981.0029. [DOI] [PubMed] [Google Scholar]
  16. Katz B., Miledi R. Transmitter leakage from motor nerve endings. Proc R Soc Lond B Biol Sci. 1977 Feb 11;196(1122):59–72. doi: 10.1098/rspb.1977.0029. [DOI] [PubMed] [Google Scholar]
  17. LILEY A. W. An investigation of spontaneous activity at the neuromuscular junction of the rat. J Physiol. 1956 Jun 28;132(3):650–666. doi: 10.1113/jphysiol.1956.sp005555. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Linden D. C., Newton M. W., Grinnell A. D., Jenden D. J. Rapid decline in acetylcholine release and content of rat extensor digitorum longus muscle after denervation. Exp Neurol. 1983 Sep;81(3):613–626. doi: 10.1016/0014-4886(83)90330-8. [DOI] [PubMed] [Google Scholar]
  19. Lupa M. T., Krzemien D. M., Schaller K. L., Caldwell J. H. Aggregation of sodium channels during development and maturation of the neuromuscular junction. J Neurosci. 1993 Mar;13(3):1326–1336. doi: 10.1523/JNEUROSCI.13-03-01326.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. MULLINS L. J., NODA K. THE INFLUENCE OF SODIUM-FREE SOLUTIONS ON THE MEMBRANE POTENTIAL OF FROG MUSCLE FIBERS. J Gen Physiol. 1963 Sep;47:117–132. doi: 10.1085/jgp.47.1.117. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Martin A. R., Levinson S. R. Contribution of the Na(+)-K+ pump to membrane potential in familial periodic paralysis. Muscle Nerve. 1985 Jun;8(5):359–362. doi: 10.1002/mus.880080503. [DOI] [PubMed] [Google Scholar]
  22. 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]
  23. Nikolsky E. E., Voronin V. A., Oranska T. I., Vyskocil F. The dependence of non-quantal acetylcholine release on the choline-uptake system in the mouse diaphragm. Pflugers Arch. 1991 Mar;418(1-2):74–78. doi: 10.1007/BF00370454. [DOI] [PubMed] [Google Scholar]
  24. Pinsker H., Kandel E. R. Synaptic activation of an electrogenic sodium pump. Science. 1969 Feb 28;163(3870):931–935. doi: 10.1126/science.163.3870.931. [DOI] [PubMed] [Google Scholar]
  25. Skou J. C. The Na,K-pump. Methods Enzymol. 1988;156:1–25. doi: 10.1016/0076-6879(88)56004-4. [DOI] [PubMed] [Google Scholar]
  26. Sun Y. A., Poo M. M. Non-quantal release of acetylcholine at a developing neuromuscular synapse in culture. J Neurosci. 1985 Mar;5(3):634–642. doi: 10.1523/JNEUROSCI.05-03-00634.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Tauc L. Non vesicular release of neurotransmitter. Physiol Rev. 1982 Jul;62(3):857–893. doi: 10.1152/physrev.1982.62.3.857. [DOI] [PubMed] [Google Scholar]
  28. Taylor P. The cholinesterases. J Biol Chem. 1991 Mar 5;266(7):4025–4028. [PubMed] [Google Scholar]
  29. Thesleff S. Different kinds of acetylcholine release from the motor nerve. Int Rev Neurobiol. 1986;28:59–88. doi: 10.1016/s0074-7742(08)60106-3. [DOI] [PubMed] [Google Scholar]
  30. Thesleff S., Vyskocil F., Ward M. R. The action potential in end-plate and extrajunctional regions of rat skeletal muscle. Acta Physiol Scand. 1974 Jun;91(2):196–202. doi: 10.1111/j.1748-1716.1974.tb05676.x. [DOI] [PubMed] [Google Scholar]
  31. Thomas R. C. Electrogenic sodium pump in nerve and muscle cells. Physiol Rev. 1972 Jul;52(3):563–594. doi: 10.1152/physrev.1972.52.3.563. [DOI] [PubMed] [Google Scholar]
  32. Tucek S. The synthesis of acetylcholine in skeletal muscles of the rat. J Physiol. 1982 Jan;322:53–69. doi: 10.1113/jphysiol.1982.sp014022. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Vizi E. S., Vyskocil F. Changes in total and quantal release of acetylcholine in the mouse diaphragm during activation and inhibition of membrane ATPase. J Physiol. 1979 Jan;286:1–14. doi: 10.1113/jphysiol.1979.sp012603. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Vyskocil F., Gutmann E. Electrophysiological and contractile properties of the levator ani muscle after castration and testosterone administration. Pflugers Arch. 1977 Mar 11;368(1-2):105–109. doi: 10.1007/BF01063461. [DOI] [PubMed] [Google Scholar]
  35. Vyskocil F., Illés P. Electrophysiological examination of transmitter release in non-quantal form in the mouse diaphragm and the activity of membrane ATP-ase. Physiol Bohemoslov. 1978;27(5):449–455. [PubMed] [Google Scholar]
  36. Vyskocil F., Illés P. Non-quantal release of transmitter at mouse neuromuscular junction and its dependence on the activity of Na+-K+ ATP-ase. Pflugers Arch. 1977 Sep 16;370(3):295–297. doi: 10.1007/BF00585542. [DOI] [PubMed] [Google Scholar]
  37. Vyskocil F., Nikolsky E., Edwards C. An analysis of the mechanisms underlying the non-quantal release of acetylcholine at the mouse neuromuscular junction. Neuroscience. 1983 Jun;9(2):429–435. doi: 10.1016/0306-4522(83)90305-6. [DOI] [PubMed] [Google Scholar]
  38. Vyskocil F., Vrbová G. Non-quantal release of acetylcholine affects polyneuronal innervation on developing rat muscle fibres. Eur J Neurosci. 1993 Dec 1;5(12):1677–1683. doi: 10.1111/j.1460-9568.1993.tb00235.x. [DOI] [PubMed] [Google Scholar]
  39. Zemková H., Vyskocil F., Edwards C. The effects of nerve terminal activity on non-quantal release of acetylcholine at the mouse neuromuscular junction. J Physiol. 1990 Apr;423:631–640. doi: 10.1113/jphysiol.1990.sp018044. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Zemková H., Vyskocil F. Effect of Mg2+ on non-quantal acetylcholine release at the mouse neuromuscular junction. Neurosci Lett. 1989 Sep 11;103(3):293–297. doi: 10.1016/0304-3940(89)90115-8. [DOI] [PubMed] [Google Scholar]

Articles from The Journal of Physiology are provided here courtesy of The Physiological Society

RESOURCES