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N-type and L-type calcium channels mediate glycinergic synaptic inputs to retinal ganglion cells of tiger salamanders

Published online by Cambridge University Press:  01 July 2004

MARK C. BIEDA
Affiliation:
Department of Ophthalmology, University of California, San Francisco Current address of Mark C. Bieda: Santa Fe Institute, 1399 Hyde Park Rd., Santa Fe, NM 87501, USA
DAVID R. COPENHAGEN
Affiliation:
Department of Ophthalmology, University of California, San Francisco

Abstract

Synaptically localized calcium channels shape the timecourse of synaptic release, are a prominent site for neuromodulation, and have been implicated in genetic disease. In retina, it is well established that L-type calcium channels play a major role in mediating release of glutamate from the photoreceptors and bipolar cells. However, little is known about which calcium channels are coupled to synaptic exocytosis of glycine, which is primarily released by amacrine cells. A recent report indicates that glycine release from spiking AII amacrine cells relies exclusively upon L-type calcium channels. To identify calcium channel types controlling neurotransmitter release from the population of glycinergic neurons that drive retinal ganglion cells, we recorded electrical and potassium evoked inhibitory synaptic currents (IPSCs) from these postsynaptic neurons in retinal slices from tiger salamanders. The L-channel antagonist nifedipine strongly inhibited release and FPL64176, an L-channel agonist, greatly enhanced it, indicating a significant role for L-channels. ω-Conotoxin MVIIC, an N/P/Q-channel antagonist, strongly inhibited release, indicating an important role for non-L channels. While the P/Q-channel blocker ω-Aga IVA produced only small effects, the N-channel blocker ω-conotoxin GVIA strongly inhibited release. Hence, N-type and L-type calcium channels appear to play major roles, overall, in mediating synaptic release of glycine onto retinal ganglion cells.

Type
Research Article
Copyright
2004 Cambridge University Press

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References

REFERENCES

Barnes, S. & Werblin, F. (1986). Gated currents generate single spike activity in amacrine cells of the tiger salamander retina. Proceedings of the National Academy of Sciences of the U.S.A. 83, 15091512.CrossRefGoogle Scholar
Bieda, M.C. & Copenhagen, D.R. (1999). Sodium action potentials are not required for light-evoked release of GABA or glycine from retinal amacrine cells. Journal of Neurophysiology 81, 30923095.Google Scholar
Bieda, M.C. & Copenhagen, D.R. (2000). Inhibition is not required for the production of transient spiking responses from retinal ganglion cells. Visual Neuroscience 17, 243254.Google Scholar
Burgess, D.L. & Noebels, J.L. (1999). Voltage-dependent calcium channel mutations in neurological disease. Annals of the New York Academy of Sciences 868, 199212.CrossRefGoogle Scholar
Cook, P.B., Lukasiewicz, P.D., & McReynolds, J.S. (1998). Action potentials are required for the lateral transmission of glycinergic transient inhibition in the amphibian retina. Journal of Neuroscience 18, 23012308.Google Scholar
Dowling, J.E. (1987). The Retina: An Approachable Part of the Brain. Cambridge, Massachusetts: Harvard University Press.
Doze, V.A., Cohen, G.A., & Madison, D.V. (1995). Calcium channel involvement in GABAB receptor-mediated inhibition of GABA release in area CA1 of the rat hippocampus. Journal of Neurophysiology 74, 4353.Google Scholar
Dunlap, K., Luebke, J.I., & Turner, T.J. (1995). Exocytotic Ca2+ channels in mammalian central neurons. Trends in Neuroscience 18, 8998.CrossRefGoogle Scholar
Gleason, E., Borges, S., & Wilson, M. (1994). Control of transmitter release from retinal amacrine cells by Ca2+ influx and efflux. Neuron 13, 11091117.CrossRefGoogle Scholar
Habermann, C.J., O'Brien, B.J., Wassle, H., & Protti, D.A. (2003). AII amacrine cells express L-type calcium channels at their output synapses. Journal of Neuroscience 23, 69046913.Google Scholar
Kamphuis, W. & Hendriksen, H. (1998). Expression patterns of voltage-dependent calcium channel alpha 1 subunits (alpha 1A-alpha 1E) mRNA in rat retina. Brain Research Molecular Brain Research 55, 209220.CrossRefGoogle Scholar
Koizumi, A., Watanabe, I., & Kaneko, A. (2001). Persistent Na+ current and Ca2+ current boost graded depolarization of rat retinal amacrine cells in culture. Journal of Neurophysiology 86, 10061016.Google Scholar
Maguire, G. (1999). Spatial heterogeneity and function of voltage- and ligand-gated ion channels in retinal amacrine neurons. Proceedings of the Royal Society B (London) 266, 987992.CrossRefGoogle Scholar
Mennerick, S. & Matthews, G. (1996). Ultrafast exocytosis elicited by calcium current in synaptic terminals of retinal bipolar neurons. Neuron 17, 12411249.CrossRefGoogle Scholar
Mermelstein, P.G., Bito, H., Deisseroth, K., & Tsien, R.W. (2000). Critical dependence of cAMP response element-binding protein phosphorylation on L-type calcium channels supports a selective response to EPSPs in preference to action potentials. Journal of Neuroscience 20, 266273.Google Scholar
Pan, Z.-H. (2000). Differential expression of high- and two types of low-voltage-activated calcium currents in rod and cone bipolar cells of the rat retina. Journal of Neurophysiology 83, 513527.Google Scholar
Pan, Z.-H., Hu, H.-J., Perring, P., & Andrade, R. (2001). T-Type Ca2+ channels mediate neurotransmitter release in retinal bipolar cells. Neuron 32, 8998.CrossRefGoogle Scholar
Schmitz, Y. & Witkovsky, P. (1997). Dependence of photoreceptor glutamate release on a dihydropyridine-sensitive calcium channel. Neuroscience 78, 12091216.CrossRefGoogle Scholar
Strom, T.M., Nyakatura, G., Apfelstedt-Sylla, E., Hellebrand, H., Lorenz, B., Weber, B.H., Wutz, K., Gutwillinger, N., Reuther, K., Drescher, B., Sauer, C., Zrenner, E., Meitinger, T., Rosenthal, A., & Meindl, A. (1998). An L-type calcium-channel gene mutated in incomplete X-linked congenital stationary night blindness. Nature Genetics 19, 260263.Google Scholar
Tachibana, M., Okada, T., Arimura, T., Kobayashi, K., & Piccolino, M. (1993). Dihydropyridine-sensitive calcium current mediates neurotransmitter release from bipolar cells of the goldfish retina. Journal of Neuroscience 13, 28982909.Google Scholar
Takahashi, T. & Momiyama, A. (1993). Different types of calcium channels mediate central synaptic transmission. Nature 366, 156158.CrossRefGoogle Scholar
Taschenberger, H. & Grantyn, R. (1995). Several types of Ca2+ channels mediate glutamatergic synaptic responses to activation of single Thy-1-immunolabeled rat retinal ganglion neurons. Journal of Neuroscience 15, 22402254.Google Scholar
Vigh, J., Solessio, E., Morgans, C.W., & Lasater, E.M. (2003). Ionic mechanisms mediating oscillatory membrane potentials in wide-field retinal amacrine cells. Journal of Neurophysiology 90, 431443.CrossRefGoogle Scholar
von Gersdorff, H. & Matthews, G. (1996). Calcium-dependent inactivation of calcium current in synaptic terminals of retinal bipolar neurons. Journal of Neuroscience 16, 115122.Google Scholar
von Gersdorff, H., Sakaba, T., Berglund, K., & Tachibana, M. (1998). Submillisecond kinetics of glutamate release from a sensory synapse. Neuron 21, 11771188.CrossRefGoogle Scholar
Wheeler, D.B., Randall, A., & Tsien, R.W. (1994). Roles of N-type and Q-type Ca2+ channels in supporting hippocampal synaptic transmission. Science 264, 107111.CrossRefGoogle Scholar
Wilkinson, M.F. & Barnes, S. (1996). The dihydropyridine-sensitive calcium channel subtype in cone photoreceptors. Journal of General Physiology 107, 621630.CrossRefGoogle Scholar
Wu, L.G. & Saggau, P. (1997). Presynaptic inhibition of elicited neurotransmitter release. Trends in Neuroscience 20, 204212.CrossRefGoogle Scholar
Wu, L.G., Borst, J.G., & Sakmann, B. (1998). R-type Ca2+ currents evoke transmitter release at a rat central synapse. Proceedings of the National Academy of Sciences of the U.S.A. 95, 47204725.CrossRefGoogle Scholar
Zamponi, G.W., Bourinet, E., & Snutch, T.P. (1996). Nickel block of a family of neuronal calcium channels: Subtype- and subunit-dependent action at multiple sites. Journal of Membrane Biology 151, 7790.CrossRefGoogle Scholar