Abstract
1. Presynaptic nerve terminals of ciliary ganglia of the chick embryo were identified by the accumulation of dextran-tetramethylrhodamine applied to the cut end of the oculomotor nerve. Ca2+ currents were then recorded from the identified nerve terminals. 2. Whole-cell recordings were carried out simultaneously from a presynaptic terminal and its postsynaptic cell. The generation of presynaptic Ca2+ currents induced a postsynaptic response with a short delay. Electrical coupling was present in eight of fifteen pairs. The coupling ratio did not exceed 5%. 3. High-threshold Ba2+ currents were observed in presynaptic terminals without any evidence for the presence of low-threshold Ca2+ channels. The Ba2+ current was completely blocked by 50 microM Cd2+. 4. The presynaptic Ca2+ current induced by a long depolarizing pulse showed inactivation, but this inactivation was diminished when Ca2+ was replaced with Ba2+. 5. The presynaptic Ba2+ current was insensitive to dihydropyridines (DHPs). omega-Conotoxin GVIA (omega CgTX) suppressed a large fraction of the Ba2+ current irreversibly. About 10% of the Ba2+ current was resistant to both DHPs and omega CgTX. 6. The omega CgTX-sensitive component was not sensitive to changes in the holding potential between -120 and -50 mV. The omega CgTX-resistant component tended to be inactivated at depolarized holding potentials. 7. In some perisynaptic Schwann cells, small Ca2+ currents were observed. These Ca2+ currents increased monotonically with depolarization. 8. Only high-threshold Ca2+ channel currents were observed in postsynaptic ciliary cells. Exposure to 50 microM Cd2+ completely abolished the Ca2+ current. 9. About 25% of the Ba2+ currents were blocked by nifedipine (10 microM) in ciliary cells. The nifedipine-resistant component was partly blocked by omega CdTX (10 microM) leaving a small component (about 20%) which was resistant to both nifedipine and omega CgTX. 10. In ciliary cells, the fraction of Ba2+ currents blocked by omega CgTX was not affected by the presence or absence of nifedipine. Similarly, nifedipine blocked the Ba2+ currents to the same extent whether omega CgTX was present or not. The Ba2+ currents potentiated by Bay K 8644 were eliminated by nifedipine. 11. It is concluded that the presynaptic terminal of chick ciliary ganglion did not possess DHP-sensitive Ca2+ channels in contrast with the postsynaptic cell. Two subpopulations of presynaptic Ca2+ channels were distinguishable by their sensitivity to omega CgTX and membrane potential.
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- Aosaki T., Kasai H. Characterization of two kinds of high-voltage-activated Ca-channel currents in chick sensory neurons. Differential sensitivity to dihydropyridines and omega-conotoxin GVIA. Pflugers Arch. 1989 Jun;414(2):150–156. doi: 10.1007/BF00580957. [DOI] [PubMed] [Google Scholar]
- Artalejo C. R., Perlman R. L., Fox A. P. Omega-conotoxin GVIA blocks a Ca2+ current in bovine chromaffin cells that is not of the "classic" N type. Neuron. 1992 Jan;8(1):85–95. doi: 10.1016/0896-6273(92)90110-y. [DOI] [PubMed] [Google Scholar]
- Augustine G. J., Charlton M. P., Smith S. J. Calcium action in synaptic transmitter release. Annu Rev Neurosci. 1987;10:633–693. doi: 10.1146/annurev.ne.10.030187.003221. [DOI] [PubMed] [Google Scholar]
- Augustine G. J., Eckert R. Divalent cations differentially support transmitter release at the squid giant synapse. J Physiol. 1984 Jan;346:257–271. doi: 10.1113/jphysiol.1984.sp015020. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Cantino D., Mugnaini E. The structural basis for electrotonic coupling in the avian ciliary ganglion. A study with thin sectioning and freeze-fracturing. J Neurocytol. 1975 Oct;4(5):505–536. doi: 10.1007/BF01351535. [DOI] [PubMed] [Google Scholar]
- Charlton M. P., Augustine G. J. Classification of presynaptic calcium channels at the squid giant synapse: neither T-, L- nor N-type. Brain Res. 1990 Aug 13;525(1):133–139. doi: 10.1016/0006-8993(90)91328-e. [DOI] [PubMed] [Google Scholar]
- DE LORENZO A. J. The fine structure of synapses in the ciliary ganglion of the chick. J Biophys Biochem Cytol. 1960 Feb;7:31–36. doi: 10.1083/jcb.7.1.31. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Dryer S. E., Dourado M. M., Wisgirda M. E. Properties of Ca2+ currents in acutely dissociated neurons of the chick ciliary ganglion: inhibition by somatostatin-14 and somatostatin-28. Neuroscience. 1991;44(3):663–672. doi: 10.1016/0306-4522(91)90086-4. [DOI] [PubMed] [Google Scholar]
- Eckert R., Chad J. E. Inactivation of Ca channels. Prog Biophys Mol Biol. 1984;44(3):215–267. doi: 10.1016/0079-6107(84)90009-9. [DOI] [PubMed] [Google Scholar]
- Epstein M. L., Davis J. P., Gellman L. E., Lamb J. R., Dahl J. L. Cholinergic neurons of the chicken ciliary ganglion contain somatostatin. Neuroscience. 1988 Jun;25(3):1053–1060. doi: 10.1016/0306-4522(88)90058-9. [DOI] [PubMed] [Google Scholar]
- Fox A. P., Nowycky M. C., Tsien R. W. Kinetic and pharmacological properties distinguishing three types of calcium currents in chick sensory neurones. J Physiol. 1987 Dec;394:149–172. doi: 10.1113/jphysiol.1987.sp016864. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fox A. P., Nowycky M. C., Tsien R. W. Single-channel recordings of three types of calcium channels in chick sensory neurones. J Physiol. 1987 Dec;394:173–200. doi: 10.1113/jphysiol.1987.sp016865. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fujiwara T., Nagakuro C. Three-dimensional structure of the presynaptic nerve ending in the ciliary ganglion of the chick embryo: a scanning electron microscopic study. Neurosci Lett. 1989 Mar 27;98(2):125–128. doi: 10.1016/0304-3940(89)90496-5. [DOI] [PubMed] [Google Scholar]
- Gray D. B., Zelazny D., Manthay N., Pilar G. Endogenous modulation of ACh release by somatostatin and the differential roles of Ca2+ channels. J Neurosci. 1990 Aug;10(8):2687–2698. doi: 10.1523/JNEUROSCI.10-08-02687.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gundersen C. B., Katz B., Miledi R. The antagonism between botulinum toxin and calcium in motor nerve terminals. Proc R Soc Lond B Biol Sci. 1982 Oct 22;216(1204):369–376. doi: 10.1098/rspb.1982.0080. [DOI] [PubMed] [Google Scholar]
- Hamill O. P., Marty A., Neher E., Sakmann B., Sigworth F. J. Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflugers Arch. 1981 Aug;391(2):85–100. doi: 10.1007/BF00656997. [DOI] [PubMed] [Google Scholar]
- Johnson D. A., Pilar G. The release of acetylcholine from post-ganglionic cell bodies in response to depolarization. J Physiol. 1980 Feb;299:605–619. doi: 10.1113/jphysiol.1980.sp013144. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Katz B., Miledi R. The release of acetylcholine from nerve endings by graded electric pulses. Proc R Soc Lond B Biol Sci. 1967 Jan 31;167(1006):23–38. doi: 10.1098/rspb.1967.0011. [DOI] [PubMed] [Google Scholar]
- Keyser D. O., Alger B. E. Arachidonic acid modulates hippocampal calcium current via protein kinase C and oxygen radicals. Neuron. 1990 Oct;5(4):545–553. doi: 10.1016/0896-6273(90)90092-t. [DOI] [PubMed] [Google Scholar]
- Landmesser L., Pilar G. The onset and development of transmission in the chick ciliary ganglion. J Physiol. 1972 May;222(3):691–713. doi: 10.1113/jphysiol.1972.sp009822. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Llinás R., Steinberg I. Z., Walton K. Presynaptic calcium currents in squid giant synapse. Biophys J. 1981 Mar;33(3):289–321. doi: 10.1016/S0006-3495(81)84898-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Llinás R., Sugimori M., Lin J. W., Cherksey B. Blocking and isolation of a calcium channel from neurons in mammals and cephalopods utilizing a toxin fraction (FTX) from funnel-web spider poison. Proc Natl Acad Sci U S A. 1989 Mar;86(5):1689–1693. doi: 10.1073/pnas.86.5.1689. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- 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]
- Martin A. R., Patel V., Faille L., Mallart A. Presynaptic calcium currents recorded from calyciform nerve terminals in the lizard ciliary ganglion. Neurosci Lett. 1989 Oct 23;105(1-2):14–18. doi: 10.1016/0304-3940(89)90004-9. [DOI] [PubMed] [Google Scholar]
- 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]
- McCleskey E. W., Fox A. P., Feldman D. H., Cruz L. J., Olivera B. M., Tsien R. W., Yoshikami D. Omega-conotoxin: direct and persistent blockade of specific types of calcium channels in neurons but not muscle. Proc Natl Acad Sci U S A. 1987 Jun;84(12):4327–4331. doi: 10.1073/pnas.84.12.4327. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mori Y., Friedrich T., Kim M. S., Mikami A., Nakai J., Ruth P., Bosse E., Hofmann F., Flockerzi V., Furuichi T. Primary structure and functional expression from complementary DNA of a brain calcium channel. Nature. 1991 Apr 4;350(6317):398–402. doi: 10.1038/350398a0. [DOI] [PubMed] [Google Scholar]
- Olivera B. M., Gray W. R., Zeikus R., McIntosh J. M., Varga J., Rivier J., de Santos V., Cruz L. J. Peptide neurotoxins from fish-hunting cone snails. Science. 1985 Dec 20;230(4732):1338–1343. doi: 10.1126/science.4071055. [DOI] [PubMed] [Google Scholar]
- Pilar G., Vaughan P. C. Electrophysiological investigations of the pigeon iris neuromuscular junctions. Comp Biochem Physiol. 1969 Apr;29(1):51–72. doi: 10.1016/0010-406x(69)91725-3. [DOI] [PubMed] [Google Scholar]
- Plummer M. R., Logothetis D. E., Hess P. Elementary properties and pharmacological sensitivities of calcium channels in mammalian peripheral neurons. Neuron. 1989 May;2(5):1453–1463. doi: 10.1016/0896-6273(89)90191-8. [DOI] [PubMed] [Google Scholar]
- Regan L. J., Sah D. W., Bean B. P. Ca2+ channels in rat central and peripheral neurons: high-threshold current resistant to dihydropyridine blockers and omega-conotoxin. Neuron. 1991 Feb;6(2):269–280. doi: 10.1016/0896-6273(91)90362-4. [DOI] [PubMed] [Google Scholar]
- Stanley E. F., Atrakchi A. H. Calcium currents recorded from a vertebrate presynaptic nerve terminal are resistant to the dihydropyridine nifedipine. Proc Natl Acad Sci U S A. 1990 Dec;87(24):9683–9687. doi: 10.1073/pnas.87.24.9683. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Stanley E. F. Calcium currents in a vertebrate presynaptic nerve terminal: the chick ciliary ganglion calyx. Brain Res. 1989 Dec 29;505(2):341–345. doi: 10.1016/0006-8993(89)91465-0. [DOI] [PubMed] [Google Scholar]
- Stanley E. F., Goping G. Characterization of a calcium current in a vertebrate cholinergic presynaptic nerve terminal. J Neurosci. 1991 Apr;11(4):985–993. doi: 10.1523/JNEUROSCI.11-04-00985.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Takahashi K., Hama K. Some observations on the fine structure of the synaptic area in the ciliary ganglion of the chick. Z Zellforsch Mikrosk Anat. 1965 Jul 15;67(2):174–184. doi: 10.1007/BF00344467. [DOI] [PubMed] [Google Scholar]
- Yawo H. Voltage-activated calcium currents in presynaptic nerve terminals of the chicken ciliary ganglion. J Physiol. 1990 Sep;428:199–213. doi: 10.1113/jphysiol.1990.sp018207. [DOI] [PMC free article] [PubMed] [Google Scholar]