Skip to main content
NCBI home page
British Journal of Pharmacology logoLink to British Journal of Pharmacology
. 1995 Jun;115(3):441–450. doi: 10.1111/j.1476-5381.1995.tb16353.x

The effect of opiates on the terminal nerve impulse and quantal secretion from visualized amphibian nerve terminals.

N A Lavidis 1
PMCID: PMC1908413  PMID: 7582455

Abstract

1. Secretion of transmitter from amphibian motor nerve terminal release sites is intermittent, spatially non-uniform and varies considerably throughout the year and during development. The role of opioid receptors in modulating transmitter secretion from amphibian motor nerve terminals is evaluated in this study. 2. Dynorphin-A (24 microM) and morphine (500 microM) did not significantly change the shape of the nerve impulse or the consistency with which it was observed, but decreased evoked quantal secretion by more than 50%. These effects of dynorphin-A and morphine were largely reversed by naloxone (50 microM). 3. Dynorphin-A and morphine did not significantly change either the amplitude or the frequency of spontaneous quantal secretions. 4. There was a uniform decrease in evoked quantal secretion from release sites along terminal branches, irrespective of the quantal content value before drug treatment, indicating no difference in the susceptibility of proximal vs distal release sites to opiates. 5. Increasing the extracellular calcium concentration (0.3 to 0.4 mM) or trains of conditioning-test impulses (25 to 100 Hz) resulted in smaller dynorphin-A or morphine-induced decreases in evoked quantal secretion. 6. The decrease in evoked quantal secretion occurs as a result of a uniform decrease in the probability of quantal secretion from release sites without any affect on the propagation of the nerve terminal impulse. Low probability release sites become effectively silent.

Full text

PDF
441

Selected References

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

  1. Balnave R. J., Gage P. W. Facilitation of transmitter secretion from toad motor nerve terminals during brief trains of action potentials. J Physiol. 1977 Apr;266(2):435–451. doi: 10.1113/jphysiol.1977.sp011776. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bennet M. R., Lavidis N. A. Variation in quantal secretion at different release sites along developing and mature motor terminal branches. Brain Res. 1982 Sep;281(1):1–9. doi: 10.1016/0165-3806(82)90107-9. [DOI] [PubMed] [Google Scholar]
  3. Bennett M. R., Florin T. A statistical analysis of the release of acetylcholine at newly formed synapses in striated muscle. J Physiol. 1974 Apr;238(1):93–107. doi: 10.1113/jphysiol.1974.sp010512. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bennett M. R., Jones P., Lavidis N. A. The probability of quantal secretion along visualized terminal branches at amphibian (Bufo marinus) neuromuscular synapses. J Physiol. 1986 Oct;379:257–274. doi: 10.1113/jphysiol.1986.sp016252. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bennett M. R., Karunanithi S., Lavidis N. A. Probabilistic secretion of quanta from nerve terminals in toad (Bufo marinus) muscle modulated by adenosine. J Physiol. 1991 Feb;433:421–434. doi: 10.1113/jphysiol.1991.sp018435. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Bennett M. R., Lavidis N. A. An electrophysiological analysis of the effects of morphine on the calcium dependence of neuromuscular transmission in the mouse vas deferens. Br J Pharmacol. 1980 Jun;69(2):185–191. doi: 10.1111/j.1476-5381.1980.tb07889.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Bennett M. R., Lavidis N. A., Armson F. M. Changes in the dimensions of release sites along terminal branches at amphibian neuromuscular synapses. J Neurocytol. 1987 Apr;16(2):221–237. doi: 10.1007/BF01795306. [DOI] [PubMed] [Google Scholar]
  8. Bennett M. R., Lavidis N. A., Lavidis-Armson F. The probability of quantal secretion at release sites of different length in toad (Bufo marinus) muscle. J Physiol. 1989 Nov;418:235–249. doi: 10.1113/jphysiol.1989.sp017837. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Bennett M. R., Lavidis N. A. Probabilistic secretion of quanta from the release sites of nerve terminals in amphibian muscle modulated by seasonal changes. Neurosci Lett. 1991 Dec 16;134(1):79–82. doi: 10.1016/0304-3940(91)90513-s. [DOI] [PubMed] [Google Scholar]
  10. Bennett M. R., Lavidis N. A. Quantal secretion at release sites of nerve terminals in toad (Bufo marinus) muscle during formation of topographical maps. J Physiol. 1988 Jul;401:567–579. doi: 10.1113/jphysiol.1988.sp017180. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Bennett M. R., Lavidis N. A. The effect of calcium ions on the secretion of quanta evoked by an impulse at nerve terminal release sites. J Gen Physiol. 1979 Oct;74(4):429–456. doi: 10.1085/jgp.74.4.429. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Bennett M. R., Lavidis N. A. The probability of quantal secretion at release sites in different calcium concentrations in toad (Bufo marinus) muscle. J Physiol. 1989 Nov;418:219–233. doi: 10.1113/jphysiol.1989.sp017836. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Bixby J. L., Spitzer N. C. Enkephalin reduces quantal content at the frog neuromuscular junction. Nature. 1983 Feb 3;301(5899):431–432. doi: 10.1038/301431a0. [DOI] [PubMed] [Google Scholar]
  14. Bornstein J. C., Fields H. L. Morphine presynaptically inhibits a ganglionic cholinergic synapse. Neurosci Lett. 1979 Nov;15(1):77–82. doi: 10.1016/0304-3940(79)91532-5. [DOI] [PubMed] [Google Scholar]
  15. Brigant J. L., Mallart A. Presynaptic currents in mouse motor endings. J Physiol. 1982 Dec;333:619–636. doi: 10.1113/jphysiol.1982.sp014472. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Brock J. A., Cunnane T. C. Electrical activity at the sympathetic neuroeffector junction in the guinea-pig vas deferens. J Physiol. 1988 May;399:607–632. doi: 10.1113/jphysiol.1988.sp017099. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Cherubini E., North R. A. Mu and kappa opioids inhibit transmitter release by different mechanisms. Proc Natl Acad Sci U S A. 1985 Mar;82(6):1860–1863. doi: 10.1073/pnas.82.6.1860. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Cone R. I., Goldstein A. A dynorphin-like opioid in the central nervous system of an amphibian. Proc Natl Acad Sci U S A. 1982 May;79(10):3345–3349. doi: 10.1073/pnas.79.10.3345. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. D'Alonzo A. J., Grinnell A. D. Profiles of evoked release along the length of frog motor nerve terminals. J Physiol. 1985 Feb;359:235–258. doi: 10.1113/jphysiol.1985.sp015583. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. 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]
  21. Dodge F. A., Jr, Rahamimoff R. Co-operative action a calcium ions in transmitter release at the neuromuscular junction. J Physiol. 1967 Nov;193(2):419–432. doi: 10.1113/jphysiol.1967.sp008367. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Einstein R., Lavidis N. A. The dependence of excitatory junction potential amplitude on the external calcium concentration in mouse vas deferens during narcotic withdrawal. Br J Pharmacol. 1984 Dec;83(4):863–870. doi: 10.1111/j.1476-5381.1984.tb16525.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. 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]
  24. FRANKENHAEUSER B., HODGKIN A. L. The action of calcium on the electrical properties of squid axons. J Physiol. 1957 Jul 11;137(2):218–244. doi: 10.1113/jphysiol.1957.sp005808. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Frederickson R. C., Pinsky C. Morphine impairs acetylcholine release but facilitates acetylcholine action at a skeletal neuromuscular junction. Nat New Biol. 1971 May 19;231(20):93–94. doi: 10.1038/newbio231093a0. [DOI] [PubMed] [Google Scholar]
  26. Ginsborg B. L., Hirst G. D. The effect of adenosine on the release of the transmitter from the phrenic nerve of the rat. J Physiol. 1972 Aug;224(3):629–645. doi: 10.1113/jphysiol.1972.sp009916. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Gross R. A., Macdonald R. L. Dynorphin A selectively reduces a large transient (N-type) calcium current of mouse dorsal root ganglion neurons in cell culture. Proc Natl Acad Sci U S A. 1987 Aug;84(15):5469–5473. doi: 10.1073/pnas.84.15.5469. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Haynes L. W., Smith M. E. Selective inhibition of 'motor endplate-specific' acetylcholinesterase by beta-endorphin and related peptides. Neuroscience. 1982 Apr;7(4):1007–1013. doi: 10.1016/0306-4522(82)90057-4. [DOI] [PubMed] [Google Scholar]
  29. Hirai K., Katayama Y. Methionine enkephalin presynaptically facilitates and inhibits bullfrog sympathetic ganglionic transmission. Brain Res. 1988 May 17;448(2):299–307. doi: 10.1016/0006-8993(88)91267-x. [DOI] [PubMed] [Google Scholar]
  30. Illes P., Meier C., Starke K. Non-competitive interaction between normorphine and calcium on the release of noradrenaline. Brain Res. 1982 Nov 11;251(1):192–195. doi: 10.1016/0006-8993(82)91292-6. [DOI] [PubMed] [Google Scholar]
  31. Illes P., Zieglgänsberger W., Herz A. Calcium reverses the inhibitory action of morphine on neuroeffector transmission in the mouse vas deferens. Brain Res. 1980 Jun 9;191(2):511–522. doi: 10.1016/0006-8993(80)91299-8. [DOI] [PubMed] [Google Scholar]
  32. JENKINSON D. H. The nature of the antagonism between calcium and magnesium ions at the neuromuscular junction. J Physiol. 1957 Oct 30;138(3):434–444. doi: 10.1113/jphysiol.1957.sp005860. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. 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]
  34. Macdonald R. L., Werz M. A. Dynorphin A decreases voltage-dependent calcium conductance of mouse dorsal root ganglion neurones. J Physiol. 1986 Aug;377:237–249. doi: 10.1113/jphysiol.1986.sp016184. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Milner J. D., North R. A., Vitek L. V. Interactions among the effects of normorphine, calcium and magnesium on transmitter release in the mouse vas deferens. Br J Pharmacol. 1982 May;76(1):45–49. doi: 10.1111/j.1476-5381.1982.tb09189.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Montecucchi P. C., de Castiglione R., Piani S., Gozzini L., Erspamer V. Amino acid composition and sequence of dermorphin, a novel opiate-like peptide from the skin of Phyllomedusa sauvagei. Int J Pept Protein Res. 1981 Mar;17(3):275–283. doi: 10.1111/j.1399-3011.1981.tb01993.x. [DOI] [PubMed] [Google Scholar]
  37. Morita K., North R. A. Opiate activation of potassium conductance in myenteric neurons: inhibition by calcium ion. Brain Res. 1982 Jun 17;242(1):145–150. doi: 10.1016/0006-8993(82)90504-2. [DOI] [PubMed] [Google Scholar]
  38. North R. A., Williams J. T. Opiate activation of potassium conductance inhibits calcium action potentials in rat locus coeruleus neurones. Br J Pharmacol. 1983 Oct;80(2):225–228. doi: 10.1111/j.1476-5381.1983.tb10023.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. North R. A., Williams J. T., Surprenant A., Christie M. J. Mu and delta receptors belong to a family of receptors that are coupled to potassium channels. Proc Natl Acad Sci U S A. 1987 Aug;84(15):5487–5491. doi: 10.1073/pnas.84.15.5487. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Pepper C. M., Henderson G. Opiates and opioid peptides hyperpolarize locus coeruleus neurons in vitro. Science. 1980 Jul 18;209(4454):394–395. doi: 10.1126/science.7384811. [DOI] [PubMed] [Google Scholar]
  41. Silinsky E. M. On the association between transmitter secretion and the release of adenine nucleotides from mammalian motor nerve terminals. J Physiol. 1975 May;247(1):145–162. doi: 10.1113/jphysiol.1975.sp010925. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Suzuki T., Oka J., Fukuda H. In vitro studies of the effects of naloxone on the root potentials in the frog spinal cord: enkephalin-like effect on the recurrent presynaptic inhibition. Comp Biochem Physiol C. 1987;87(1):221–225. doi: 10.1016/0742-8413(87)90207-6. [DOI] [PubMed] [Google Scholar]
  43. Werz M. A., Macdonald R. L. Dynorphin and neoendorphin peptides decrease dorsal root ganglion neuron calcium-dependent action potential duration. J Pharmacol Exp Ther. 1985 Jul;234(1):49–56. [PubMed] [Google Scholar]
  44. Werz M. A., Macdonald R. L. Opioid peptides with differential affinity for mu and delta receptors decrease sensory neuron calcium-dependent action potentials. J Pharmacol Exp Ther. 1983 Nov;227(2):394–402. [PubMed] [Google Scholar]
  45. Yoshikami D., Okun L. M. Staining of living presynaptic nerve terminals with selective fluorescent dyes. Nature. 1984 Jul 5;310(5972):53–56. doi: 10.1038/310053a0. [DOI] [PubMed] [Google Scholar]
  46. Zucker R. S., Fogelson A. L. Relationship between transmitter release and presynaptic calcium influx when calcium enters through discrete channels. Proc Natl Acad Sci U S A. 1986 May;83(9):3032–3036. doi: 10.1073/pnas.83.9.3032. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from British Journal of Pharmacology are provided here courtesy of The British Pharmacological Society

RESOURCES