Skip to main content
NCBI home page
British Journal of Pharmacology logoLink to British Journal of Pharmacology
. 1993 Sep;110(1):461–469. doi: 10.1111/j.1476-5381.1993.tb13833.x

The effect of ions and second messengers on long-term potentiation of chemical transmission in avian ciliary ganglia.

T R Scott 1, M R Bennett 1
PMCID: PMC2175975  PMID: 8220908

Abstract

1. The effects of tetanic stimulation of the oculomotor nerve on transmission through the avian ciliary ganglion have been determined by use of the amplitude of the compound action potential recorded in the ciliary nerve, in the presence of hexamethonium (300 microM), as a measure of synaptic efficacy. 2. Tetanic stimulation for 20 s at 30 Hz potentiated the chemical phase of the compound action potential by at least 100% of its control level. This potentiation, reflecting an increase in synaptic efficacy, decayed over two distinct time courses: firstly, a rapid decay with a time constant in the order of minutes, and secondly, a slower decay, representing a smaller potentiation, with a time constant in the order of an hour. The large increase in synaptic efficacy is attributed to post-tetanic potentiation (PTP) whereas the smaller but longer lasting increase is attributed to long-term potentiation (LTP). 3. Higher frequencies of tetanic stimulation gave increased PTP and LTP. 4. In order to test whether the influx of calcium ions into the nerve terminal during the tetanus is likely to be involved in potentiation, facilitation was measured during PTP and LTP. Facilitation was reduced to approximately zero during PTP but recovered to normal values about 15 min into LTP. A requirement for the induction of LTP was shown to be the presence of calcium in the bathing solution. However, blocking synaptic transmission with a high concentration of hexamethonium (3 mM) during the tetanic stimulation did not block the induction of LTP. 5. Application of the muscarinic inhibitor, atropine (2 microM), did not affect the magnitude of PTP or LTP.(ABSTRACT TRUNCATED AT 250 WORDS)

Full text

PDF
461

Selected References

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

  1. Briggs C. A., Brown T. H., McAfee D. A. Neurophysiology and pharmacology of long-term potentiation in the rat sympathetic ganglion. J Physiol. 1985 Feb;359:503–521. doi: 10.1113/jphysiol.1985.sp015599. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Briggs C. A., McAfee D. A. Long-term potentiation at nicotinic synapses in the rat superior cervical ganglion. J Physiol. 1988 Oct;404:129–144. doi: 10.1113/jphysiol.1988.sp017282. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Brown T. H., McAfee D. A. Long-term synaptic potentiation in the superior cervical ganglion. Science. 1982 Mar 12;215(4538):1411–1413. doi: 10.1126/science.6278593. [DOI] [PubMed] [Google Scholar]
  4. Bär P. R., Wiegant F., Lopes da Silva F. H., Gispen W. H. Tetanic stimulation affects the metabolism of phosphoinositides in hippocampal slices. Brain Res. 1984 Nov 12;321(2):381–385. doi: 10.1016/0006-8993(84)90198-7. [DOI] [PubMed] [Google Scholar]
  5. Delaney K. R., Zucker R. S., Tank D. W. Calcium in motor nerve terminals associated with posttetanic potentiation. J Neurosci. 1989 Oct;9(10):3558–3567. doi: 10.1523/JNEUROSCI.09-10-03558.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Dunant Y., Dolivo M. Plasticity of synaptic functions in the exised sympathetic ganglion of the rat. Brain Res. 1968 Aug 26;10(2):271–273. doi: 10.1016/0006-8993(68)90134-0. [DOI] [PubMed] [Google Scholar]
  7. Erulkar S. D., Rahamimoff R. The role of calcium ions in tetanic and post-tetanic increase of miniature end-plate potential frequency. J Physiol. 1978 May;278:501–511. doi: 10.1113/jphysiol.1978.sp012320. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Fujii J. T. Repetitive firing properties in subpopulations of the chick Edinger Westphal nucleus. J Comp Neurol. 1992 Feb 15;316(3):279–286. doi: 10.1002/cne.903160303. [DOI] [PubMed] [Google Scholar]
  9. Hess A. Developmental changes in the structure of the synapse on the myelinated cell bodies of the chicken ciliary ganglion. J Cell Biol. 1965 Jun;25(3 Suppl):1–19. doi: 10.1083/jcb.25.3.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Hess A., Pilar G., Weakly J. N. Correlation between transmission and structure in avian ciliary ganglion synapses. J Physiol. 1969 Jun;202(2):339–354. doi: 10.1113/jphysiol.1969.sp008815. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Koyano K., Kuba K., Minota S. Long-term potentiation of transmitter release induced by repetitive presynaptic activities in bull-frog sympathetic ganglia. J Physiol. 1985 Feb;359:219–233. doi: 10.1113/jphysiol.1985.sp015582. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Kuba K., Kumamoto E. Long-term potentiations in vertebrate synapses: a variety of cascades with common subprocesses. Prog Neurobiol. 1990;34(3):197–269. doi: 10.1016/0301-0082(90)90012-6. [DOI] [PubMed] [Google Scholar]
  13. MARTIN A. R., PILAR G. AN ANALYSIS OF ELECTRICAL COUPLING AT SYNAPSES IN THE AVIAN CILIARY GANGLION. J Physiol. 1964 Jun;171:454–475. doi: 10.1113/jphysiol.1964.sp007390. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. MARTIN A. R., PILAR G. DUAL MODE OF SYNAPTIC TRANSMISSION IN THE AVIAN CILIARY GANGLION. J Physiol. 1963 Sep;168:443–463. doi: 10.1113/jphysiol.1963.sp007202. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. MARTIN A. R., PILAR G. PRESYNAPTIC AND POST-SYNAPTIC EVENTS DURING POST-TETANIC POTENTIATION AND FACILITATION IN THE AVIAN CILIARY GANGLION. J Physiol. 1964 Dec;175:17–30. doi: 10.1113/jphysiol.1964.sp007500. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. MARTIN A. R., PILAR G. QUANTAL COMPONENTS OF THE SYNAPTIC POTENTIAL IN THE CILIARY GANGLION OF THE CHICK. J Physiol. 1964 Dec;175:1–16. doi: 10.1113/jphysiol.1964.sp007499. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Magleby K. L., Zengel J. E. A quantitative description of tetanic and post-tetanic potentiation of transmitter release at the frog neuromuscular junction. J Physiol. 1975 Feb;245(1):183–208. doi: 10.1113/jphysiol.1975.sp010840. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Marwitt R., Pilar G., Weakly J. N. Characterization of two ganglion cell populations in avian ciliary ganglia. Brain Res. 1971 Jan 22;25(2):317–334. doi: 10.1016/0006-8993(71)90441-0. [DOI] [PubMed] [Google Scholar]
  19. Minota S., Kumamoto E., Kitakoga O., Kuba K. Long-term potentiation induced by a sustained rise in the intraterminal Ca2+ in bull-frog sympathetic ganglia. J Physiol. 1991 Apr;435:421–438. doi: 10.1113/jphysiol.1991.sp018517. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Racine R. J., Milgram N. W. Short-term potentiation phenomena in the rat limbic forebrain. Brain Res. 1983 Feb 7;260(2):201–216. doi: 10.1016/0006-8993(83)90675-3. [DOI] [PubMed] [Google Scholar]
  21. Rahamimoff R., Lev-Tov A., Meiri H. Primary and secondary regulation of quantal transmitter release: calcium and sodium. J Exp Biol. 1980 Dec;89:5–18. doi: 10.1242/jeb.89.1.5. [DOI] [PubMed] [Google Scholar]
  22. Rose B., Loewenstein W. R. Permeability of cell junction depends on local cytoplasmic calcium activity. Nature. 1975 Mar 20;254(5497):250–252. doi: 10.1038/254250a0. [DOI] [PubMed] [Google Scholar]
  23. Sobue K., Kanda K., Adachi J., Kakiuchi S. Calmodulin-binding proteins that interact with actin filaments in a Ca2+-dependent flip-flop manner: survey in brain and secretory tissues. Proc Natl Acad Sci U S A. 1983 Nov;80(22):6868–6871. doi: 10.1073/pnas.80.22.6868. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Stanley E. F. Single calcium channels on a cholinergic presynaptic nerve terminal. Neuron. 1991 Oct;7(4):585–591. doi: 10.1016/0896-6273(91)90371-6. [DOI] [PubMed] [Google Scholar]
  25. Swandulla D., Hans M., Zipser K., Augustine G. J. Role of residual calcium in synaptic depression and posttetanic potentiation: fast and slow calcium signaling in nerve terminals. Neuron. 1991 Dec;7(6):915–926. doi: 10.1016/0896-6273(91)90337-y. [DOI] [PubMed] [Google Scholar]
  26. Tamaoki T., Nomoto H., Takahashi I., Kato Y., Morimoto M., Tomita F. Staurosporine, a potent inhibitor of phospholipid/Ca++dependent protein kinase. Biochem Biophys Res Commun. 1986 Mar 13;135(2):397–402. doi: 10.1016/0006-291x(86)90008-2. [DOI] [PubMed] [Google Scholar]
  27. Tanabe N., Kijima H. Ca(2+)-dependent and -independent components of transmitter release at the frog neuromuscular junction. J Physiol. 1992 Sep;455:271–289. doi: 10.1113/jphysiol.1992.sp019301. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Waziri R., Kandel E. R., Frazier W. T. Organization of inhibition in abdominal ganglion of Aplysia. II. Posttetanic potentiation, heterosynaptic depression, and increments in frequency of inhibitory postsynaptic potentials. J Neurophysiol. 1969 Jul;32(4):509–519. doi: 10.1152/jn.1969.32.4.509. [DOI] [PubMed] [Google Scholar]
  29. Zalutsky R. A., Nicoll R. A. Comparison of two forms of long-term potentiation in single hippocampal neurons. Science. 1990 Jun 29;248(4963):1619–1624. doi: 10.1126/science.2114039. [DOI] [PubMed] [Google Scholar]
  30. Zengel J. E., Magleby K. L. Augmentation and facilitation of transmitter release. A quantitative description at the frog neuromuscular junction. J Gen Physiol. 1982 Oct;80(4):583–611. doi: 10.1085/jgp.80.4.583. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Zengel J. E., Magleby K. L., Horn J. P., McAfee D. A., Yarowsky P. J. Facilitation, augmentation, and potentiation of synaptic transmission at the superior cervical ganglion of the rabbit. J Gen Physiol. 1980 Aug;76(2):213–231. doi: 10.1085/jgp.76.2.213. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Zucker R. S. Short-term synaptic plasticity. Annu Rev Neurosci. 1989;12:13–31. doi: 10.1146/annurev.ne.12.030189.000305. [DOI] [PubMed] [Google Scholar]

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

RESOURCES