Skip to main content
The Journal of Physiology logoLink to The Journal of Physiology
. 1995 Dec 15;489(Pt 3):637–648. doi: 10.1113/jphysiol.1995.sp021079

Calcium in the nerve terminals of chick ciliary ganglia during facilitation, augmentation and potentiation.

K L Brain 1, M R Bennett 1
PMCID: PMC1156835  PMID: 8788930

Abstract

1. The calyciform nerve terminals of chick ciliary ganglia were loaded with the calcium indicators calcium green 1 or fura-2. These were used to determine the change in calcium concentration in the terminal, [Ca2+]t, following short (10 impulses) and long (600 impulses) trains of high-frequency (30 Hz) stimulation. 2. Following a single impulse or a short train, the elevated [Ca2+]t declined along two exponentials with time constants similar to slow (F2) facilitation (0.52 s) and augmentation (4.0 s). After a long train elevated [Ca2+]t declined eventually along a single exponential with the time constant of post-tetanic potentiation (162 s). [Ca2+]t was not elevated through long-term potentiation. 3. Addition of Ba2+ (0.75 mM) to the extracellular solution slowed only the decline of [Ca2+]t associated with augmentation. The addition of the nitric oxide donor sodium nitroprusside did not affect [Ca2+]t following short or long trains. 4. Removal of extracellular calcium (buffered with EGTA) and the blockade of calcium channels with Cd2+ completely prevented the changes in [Ca2+]t. 5. The soma of ciliary ganglion cells were loaded with calcium green and the postganglionic nerves stimulated with a single impulse or a short train of impulses. Following stimuli, the elevated [Ca2+]t declined along a single exponential with a time constant similar to F2 facilitation with no augmentation component evident. 6. The results are discussed in terms of the hypothesis that each impulse in a train gives an equal increment of residual Ca2+ to a compartment for secretion and that Ca2+ is removed from the compartment by three first-order kinetics processes associated with F2 facilitation, augmentation and post-tetanic potentiation.

Full text

PDF
638

Images in this article

Selected References

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

  1. Adler E. M., Augustine G. J., Duffy S. N., Charlton M. P. Alien intracellular calcium chelators attenuate neurotransmitter release at the squid giant synapse. J Neurosci. 1991 Jun;11(6):1496–1507. doi: 10.1523/JNEUROSCI.11-06-01496.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bain A. I., Quastel D. M. Multiplicative and additive Ca(2+)-dependent components of facilitation at mouse endplates. J Physiol. 1992 Sep;455:383–405. doi: 10.1113/jphysiol.1992.sp019307. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Barzilai A., Spanier R., Rahamimoff H. Isolation, purification, and reconstitution of the Na+ gradient-dependent Ca2+ transporter (Na+-Ca2+ exchanger) from brain synaptic plasma membranes. Proc Natl Acad Sci U S A. 1984 Oct;81(20):6521–6525. doi: 10.1073/pnas.81.20.6521. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bennett M. R. Nitric oxide release and long term potentiation at synapses in autonomic ganglia. Gen Pharmacol. 1994 Dec;25(8):1541–1551. doi: 10.1016/0306-3623(94)90353-0. [DOI] [PubMed] [Google Scholar]
  5. Blundon J. A., Wright S. N., Brodwick M. S., Bittner G. D. Residual free calcium is not responsible for facilitation of neurotransmitter release. Proc Natl Acad Sci U S A. 1993 Oct 15;90(20):9388–9392. doi: 10.1073/pnas.90.20.9388. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. 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]
  7. 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]
  8. 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]
  9. 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]
  10. Grynkiewicz G., Poenie M., Tsien R. Y. A new generation of Ca2+ indicators with greatly improved fluorescence properties. J Biol Chem. 1985 Mar 25;260(6):3440–3450. [PubMed] [Google Scholar]
  11. Hernández-Cruz A., Sala F., Adams P. R. Subcellular calcium transients visualized by confocal microscopy in a voltage-clamped vertebrate neuron. Science. 1990 Feb 16;247(4944):858–862. doi: 10.1126/science.2154851. [DOI] [PubMed] [Google Scholar]
  12. Kamiya H., Zucker R. S. Residual Ca2+ and short-term synaptic plasticity. Nature. 1994 Oct 13;371(6498):603–606. doi: 10.1038/371603a0. [DOI] [PubMed] [Google Scholar]
  13. 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]
  14. Landò L., Zucker R. S. Ca2+ cooperativity in neurosecretion measured using photolabile Ca2+ chelators. J Neurophysiol. 1994 Aug;72(2):825–830. doi: 10.1152/jn.1994.72.2.825. [DOI] [PubMed] [Google Scholar]
  15. Larkum M. E., Warren D. A., Bennett M. R. Calcium concentration changes in the calyciform nerve terminal of the avian ciliary ganglion after tetanic stimulation. J Auton Nerv Syst. 1994 Mar;46(3):175–188. doi: 10.1016/0165-1838(94)90035-3. [DOI] [PubMed] [Google Scholar]
  16. Lin Y. Q., Bennett M. R. Nitric oxide modulation of quantal secretion in chick ciliary ganglia. J Physiol. 1994 Dec 1;481(Pt 2):385–394. doi: 10.1113/jphysiol.1994.sp020447. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Llinás R., Gruner J. A., Sugimori M., McGuinness T. L., Greengard P. Regulation by synapsin I and Ca(2+)-calmodulin-dependent protein kinase II of the transmitter release in squid giant synapse. J Physiol. 1991 May;436:257–282. doi: 10.1113/jphysiol.1991.sp018549. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. 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]
  19. 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]
  20. Magleby K. L., Zengel J. E. Augmentation: A process that acts to increase transmitter release at the frog neuromuscular junction. J Physiol. 1976 May;257(2):449–470. doi: 10.1113/jphysiol.1976.sp011378. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Mallart A., Martin A. R. An analysis of facilitation of transmitter release at the neuromuscular junction of the frog. J Physiol. 1967 Dec;193(3):679–694. doi: 10.1113/jphysiol.1967.sp008388. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. 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]
  23. Monck J. R., Fernandez J. M. The exocytotic fusion pore and neurotransmitter release. Neuron. 1994 Apr;12(4):707–716. doi: 10.1016/0896-6273(94)90325-5. [DOI] [PubMed] [Google Scholar]
  24. Mulkey R. M., Zucker R. S. Posttetanic potentiation at the crayfish neuromuscular junction is dependent on both intracellular calcium and sodium ion accumulation. J Neurosci. 1992 Nov;12(11):4327–4336. doi: 10.1523/JNEUROSCI.12-11-04327.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Nichol K. A., Chan N., Davey D. F., Bennett M. R. Location of nitric oxide synthase in the developing avian ciliary ganglion. J Auton Nerv Syst. 1995 Feb 9;51(2):91–102. doi: 10.1016/0165-1838(94)00116-2. [DOI] [PubMed] [Google Scholar]
  26. Peng Y. Y., Zucker R. S. Release of LHRH is linearly related to the time integral of presynaptic Ca2+ elevation above a threshold level in bullfrog sympathetic ganglia. Neuron. 1993 Mar;10(3):465–473. doi: 10.1016/0896-6273(93)90334-n. [DOI] [PubMed] [Google Scholar]
  27. Poage R. E., Zengel J. E. Kinetic and pharmacological examination of stimulation-induced increases in synaptic efficacy in the chick ciliary ganglion. Synapse. 1993 May;14(1):81–89. doi: 10.1002/syn.890140111. [DOI] [PubMed] [Google Scholar]
  28. Regehr W. G., Delaney K. R., Tank D. W. The role of presynaptic calcium in short-term enhancement at the hippocampal mossy fiber synapse. J Neurosci. 1994 Feb;14(2):523–537. doi: 10.1523/JNEUROSCI.14-02-00523.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Regehr W. G., Tank D. W. The maintenance of LTP at hippocampal mossy fiber synapses is independent of sustained presynaptic calcium. Neuron. 1991 Sep;7(3):451–459. doi: 10.1016/0896-6273(91)90297-d. [DOI] [PubMed] [Google Scholar]
  30. Scott T. R., Bennett M. R. The effect of ions and second messengers on long-term potentiation of chemical transmission in avian ciliary ganglia. Br J Pharmacol. 1993 Sep;110(1):461–469. doi: 10.1111/j.1476-5381.1993.tb13833.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. 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]
  32. 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]
  33. Wu L. G., Saggau P. Presynaptic calcium is increased during normal synaptic transmission and paired-pulse facilitation, but not in long-term potentiation in area CA1 of hippocampus. J Neurosci. 1994 Feb;14(2):645–654. doi: 10.1523/JNEUROSCI.14-02-00645.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Yawo H., Chuhma N. Preferential inhibition of omega-conotoxin-sensitive presynaptic Ca2+ channels by adenosine autoreceptors. Nature. 1993 Sep 16;365(6443):256–258. doi: 10.1038/365256a0. [DOI] [PubMed] [Google Scholar]
  35. 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]
  36. Zengel J. E., Magleby K. L. Changes in miniature endplate potential frequency during repetitive nerve stimulation in the presence of Ca2+, Ba2+, and Sr2+ at the frog neuromuscular junction. J Gen Physiol. 1981 May;77(5):503–529. doi: 10.1085/jgp.77.5.503. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. 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]
  38. 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 The Journal of Physiology are provided here courtesy of The Physiological Society

RESOURCES