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AII amacrine cells in the rabbit retina possess AMPA-, NMDA-, GABA-, and glycine-activated currents

Published online by Cambridge University Press:  23 June 2004

CHENGWEN ZHOU  and
RAMON F. DACHEUX
CHENGWEN ZHOU
Affiliation:
Department of Ophthalmology, University of Alabama at Birmingham, Birmingham
RAMON F. DACHEUX
Affiliation:
Department of Ophthalmology, University of Alabama at Birmingham, Birmingham
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Abstract

Physiological properties of ligand-activated currents were characterized for morphologically identified AII amacrine cells in the rabbit retina by using whole-cell recordings in a superfused retina slice preparation. The AII amacrine cells were identified based on their distinct narrow-field, bistratified morphology. In the present study, the whole-cell recordings from AII amacrine cells synaptically isolated from presynaptic influences demonstrated the presence of glutamate AMPA (α-amino-3-hydroxy-5-methyl-4-isoxazole-propionic acid) receptors, but no kainate receptors. The presence of only AMPA receptors on rabbit AII amacrine cells is in contrast to an earlier study on rabbit AII amacrine cells by Bloomfield and Xin (2000), but consistent with previous studies on rat AII amacrine cells. In addition, NMDA (N-methyl-D-aspartate) -activated currents blocked by the NMDA antagonist D-AP7 (D-2-amino-7-phosphonoheptanoic acid) were found on the AII amacrine cells. These most likely extrasynaptic NMDA-activated currents were attenuated by the presence of Co2+ interacting with Mg2+ and Ca2+ as they competed for divalent cation-binding sites within the NMDA channel. AII amacrine cells also possessed GABA (γ-aminobutyric acid) -activated currents that were unaffected by the GABAC receptor antagonist TPMPA (1,2,5,6-tetrahydropyridine-4-yl methylphosphinic), but were completely blocked by the GABAA antagonist bicuculline. This indicates that the major inhibitory inputs were mediated by only GABAA receptors located directly on the AII amacrine cells. Furthermore, although the AII amacrine cells were glycinergic amacrine cells, they also possessed glycine-activated currents that may be mediated by autoreceptors.

Keywords

Rabbit retina AII amacrine cellsAMPA-activated currentsNMDA-activated currentsGABA-activated currentsGlycine-activated currents
Type
Research Article
Information
Visual Neuroscience , Volume 21 , Issue 2 , March 2004 , pp. 181 - 188
Copyright
2004 Cambridge University Press

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References

REFERENCES

Ault, R., Evans, R.H., Francis, A.A., Oakes, D.J., & Watkins, J.C. (1980). Selective depression of excitatory amino acid induced depolarizations by magnesium in isolated spinal cord preparations. Journal of Physiology (London) 307, 413–428.CrossRefGoogle Scholar
Bekkers, J.M. & Stevens, C.F. (1989). NMDA and non-NMDA receptors are co-localized at individual excitatory synapses in cultured rat hippocampus. Nature 341, 230–233.CrossRefGoogle Scholar
Bloomfield, S.A. & Xin, D.Y. (2000). Surround inhibition of mammalian AII amacrine cells is generated in the proximal retina. Journal of Physiology (London) 523, 771–783.CrossRefGoogle Scholar
Bloomfield, S.A. & Dacheux, R.F. (2001). Rod vision: Pathways and processing in the mammalian retina. Progress in Retinal and Eye Research 20, 351–384.CrossRefGoogle Scholar
Boos, R., Schneider, H., & Wässle, H. (1993). Voltage- and transmitter-gated currents of AII-amacrine cells in slice preparation of the rat retina. Journal of Neuroscience 13, 2874–2888.Google Scholar
Crunelli, V., Forda, S., & Kelly, J.S. (1984). The reversal potential of excitatory amino acid action on granule cells of the rat dentate gyrus. Journal of Physiology (London) 351, 327–342.CrossRefGoogle Scholar
Dacheux, R.F. & Miller, R.F. (1976). Photoreceptor-bipolar cell transmission in the perfused mudpuppy eyecup. Science 191, 963–964.CrossRefGoogle Scholar
Dacheux, R.F. & Raviola, E. (1986). The rod pathway in the rabbit retina: A depolarizing bipolar and amacrine cell. Journal of Neuroscience 6, 331–345.Google Scholar
Dacheux, R.F., Frumkes, T.E., & Miller, R.F. (1979). Pathways and polarities of synaptic interactions in the inner retina of the mudpuppy: Synaptic blocking studies. Brain Research 161, 1–12.Google Scholar
Euler, T. & Wässle, H. (1998). Different contributions of GABAA and GABAC receptors to rod and cone bipolar cells in a rat retinal slice preparation. Journal of Neurophysiology 79, 1384–1395.Google Scholar
Famiglietti, E.V. & Kolb, H. (1975). A bistratified amacrine cell and synaptic circuitry in the inner plexiform layer of the retina. Brain Research 84, 293–300.CrossRefGoogle Scholar
Fletcher, E. & Wässle, H. (1999). Indoleamine-accumulating amacrine cells are presynaptic to rod bipolar cells through GABAC receptors. Journal of Comparative Neurology 413, 155–167.3.0.CO;2-6>CrossRefGoogle Scholar
Fletcher, E., Koulen, P., & Wässle, H. (1998). GABAA and GABAC receptors on mammalian rod bipolar cells. Journal of Comparative Neurology 39, 351–365.3.0.CO;2-1>CrossRefGoogle Scholar
Fletcher, E., Hack, I., Brandstätter, J.H., & Wässle, H. (2000). Synaptic localization of NMDA receptor subunits in the rat retina. Journal of Comparative Neurology 420, 98–112.3.0.CO;2-U>CrossRefGoogle Scholar
Ghosh, K.K., Haverkamp, S., & Wässle, H. (2001). Glutamate receptors in the rod pathway of the mammalian retina. Journal of Neuroscience 21, 8636–8647.Google Scholar
Gillette, M.A. & Dacheux, R.F. (1995). GABA- and glycine-activated currents in the rod bipolar cell of the rabbit. Journal of Neurophysiology 74, 856–875.Google Scholar
Grünert, U. & Wässle, H. (1993). Immunocytochemical localization of glycine receptors in the mammalian retina. Journal of Comparative Neurology 335, 523–537.CrossRefGoogle Scholar
Hartveit, E. & Veruki, M.L. (1997). AII amacrine cells express functional NMDA receptors. NeuroReport 8, 1219–1223.CrossRefGoogle Scholar
Kneussel, M., Haverkamp, S., Fuhrmann, J.C., Wang, H., Wässle, H., Olsen, R.W., & Betz, H. (2000). The γ-aminobutyric acid type A receptor (GABAAR)-associated protein GABARAP interacts with gephyrin but is not involved in receptor anchoring at the synapse. Proceedings of the National Academy of Sciences of the U.S.A. 97, 8594–8599.CrossRefGoogle Scholar
Kneussel, M., Brandstätter, J.H., Gasnier, B., Feng, G., Sanes, J.R., & Betz, H. (2001). Gephyrin-independent clustering of postsynaptic GABAA receptor subtypes. Molecular and Cellular Neuroscience 17, 973–982.CrossRefGoogle Scholar
Li, W., Trexler, B., & Massey, S.C. (2002). Glutamate receptors at rod bipolar ribbon synapses in the rabbit retina. Journal of Comparative Neurology 448, 230–248.CrossRefGoogle Scholar
MacNeil, M.A., Heussey, J.K., Dacheux, R.F., Raviola, E., & Masland, R. (1999). The shapes of and numbers of amacrine cell: Matching of photofilled with Golgi-stained cells in the rabbit retina and comparison with other mammalian species. Journal of Comparative Neurology 413, 305–326.3.0.CO;2-E>CrossRefGoogle Scholar
McBain, C. & Dingledine, R. (1992). Dual-component miniature excitatory synaptic currents in rat hippocampal CA3 pyramidal neurons. Journal of Neurophysiology 68, 16–27.Google Scholar
Mørkve, S.H., Veruki, M.L., & Hartveit, E. (2002). Functional characteristics of non-NMDA-type ionotropic glutamate receptor channels in AII amacrine cells in rat retina. Journal of Physiology (London) 542, 147–165.CrossRefGoogle Scholar
Nelson, R. (1982). AII amacrine cells quicken time course of rod signals in the cat retina. Journal of Neurophysiology 47, 928–947.Google Scholar
Nelson, R. & Kolb, H. (1985). A17: A broad-field amacrine cell in the rod system of the cat retina. Journal of Neurophysiology 54, 592–614.Google Scholar
Pourcho, R.G. (1980). Uptake of (3H) glycine and (3H) GABA by amacrine cells in the cat retina. Brain Research 198, 333–346.CrossRefGoogle Scholar
Qin, P. & Pourcho, R.G. (1999a). Localization of AMPA-selective glutamate receptor subunits in the cat retina: A light- and electron-microscopic study. Visual Neuroscience 16, 169–177.Google Scholar
Qin, P. & Pourcho, R.G. (1999b). AMPA-selective glutamate receptor subunits GluR2 and GluR4 in the cat retina: An immunocytochemical study. Visual Neuroscience 16, 1105–1114.Google Scholar
Raviola, E. & Dacheux, R.F. (1987). Excitatory dyad synapse in rabbit retina. Proceedings of the National Academy of Sciences of the U.S.A. 84, 7324–7328.CrossRefGoogle Scholar
Strettoi, E., Dacheux, R.F., & Raviola, E. (1990). Synaptic connections rod bipolar cells in the inner plexiform layer of the rabbit retina. Journal of Comparative Neurology 295, 449–466.CrossRefGoogle Scholar
Strettoi, E., Raviola, E., & Dacheux, R.F. (1992). Synaptic connections of the narrow-field, bistratified rod amacrine cell (AII) in the rabbit retina. Journal of Comparative Neurology 325, 152–168.CrossRefGoogle Scholar
Triller, A., Cluzeaud, F., & Korn, H. (1987). Gamma-aminobutyric acid-containing terminals can be apposed to glycine receptors at central synapses. Journal of Cell Biology, 104, 947–956.CrossRefGoogle Scholar
Veruki, M.L., Mørkve, S.H., & Hartveit, E. (2003). Functional properties of spontaneous EPSCs and non-NMDA receptors in rod amacrine (AII) cells in the rat retina. Journal of Physiology (London) 549, 759–774.CrossRefGoogle Scholar
Völgyi, B., Xin, D., & Bloomfield, S. (2002). Feedback inhibition in the inner plexiform layer underlies the surround-mediated responses of AII amacrine cells in the mammalian retina. Journal of Physiology (USA) 539, 603–614.CrossRefGoogle Scholar
Wässle, H., Koulen, P., Brandstätter, J.H., Fletcher, E.L., & Becker, C.-M. (1998). Glycine and GABA receptors in the mammalian retina. Vision Research 38, 1411–1430.CrossRefGoogle Scholar
Yazulla, S. & Studholme, K.M. (1991). Glycinergic interplexiform cells make synaptic contact with amacrine cells bodies in goldfish retina. Journal of Comparative Neurology 310, 1–10.Google Scholar