Hostname: page-component-7479d7b7d-767nl Total loading time: 0 Render date: 2024-07-08T12:29:08.706Z Has data issue: false hasContentIssue false
  • English
  • Français

Two neuropharmacological types of rabbit ON-alpha ganglion cells express GABAC receptors

Published online by Cambridge University Press:  18 November 2003

THOMAS C. ROTOLO  and
RAMON F. DACHEUX
THOMAS C. ROTOLO
Affiliation:
Department of Ophthalmology, University of Alabama at Birmingham, Birmingham
RAMON F. DACHEUX
Affiliation:
Department of Ophthalmology, University of Alabama at Birmingham, Birmingham
Get access Rights & Permissions [Opens in a new window]

Abstract

The major inhibitory neurotransmitters GABA and glycine provide the bulk of input to large-field ganglion cells in the retina. Whole-cell patch-clamp recordings were used to characterize the glycine- and GABA-activated currents for morphologically identified ON-α ganglion cells in the rabbit retina. Cells identified as ON-α cells by light evoked currents were intracellularly stained and examined by light microscopy which revealed dendritic stratification in the vitreal half of the inner plexiform layer and confirmed their physiological identity. All Ca2+-mediated synaptic influences were abolished with Co2+, revealing two types of ON-α cell characterized by their different inhibitory current profiles. One group exhibited larger glycine- than GABA-activated currents, while the other group had larger GABA- than glycine-activated currents. Both cell types demonstrated strychnine-sensitive glycine-activated currents and bicuculline-sensitive GABAA-activated currents. Surprisingly, both cell types expressed functional GABAC receptors demonstrated by their sensitivity to TPMPA. In addition, the cells with larger glycine-activated currents also possessed GABAB receptors, whereas those with larger GABA-activated currents did not. Immunocytochemical experiments confirmed the presence of glycine, GABAA, and GABAC receptor subunits on all physiologically identified ON-α ganglion cells in this study. In addition, the GABAB receptor immunolabeled puncta were present on the cells with larger glycine-activated currents, but not on the cells with the larger GABA-activated currents. In conclusion, the presence of different functional GABA and glycine receptors determined physiologically correlated well with the specific GABA and glycine receptor immunolabeling for two neuropharmacological types of rabbit ON-α ganglion cells.

Keywords

Alpha-ganglion cellsGABA receptorsGlycine receptorsWhole-cell patch-clamp recordingsConfocal microscopyImmunocytochemistry
Type
Research Article
Information
Visual Neuroscience , Volume 20 , Issue 4 , July 2003 , pp. 373 - 384
Copyright
2003 Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Albrecht, B.E., Breitenbach, U., Stuhmer, T., Harvey, R.J., & Darlison, M.G. (1997). In situ hybridization and reverse transcription-polymerase chain reaction studies on the expression of the GABAC receptor ρ1- and ρ2-subunit genes in avian and rat brain. European Journal of Neuroscience 9, 2414–2422.Google Scholar
Bai, S.-H. & Slaughter, M.M. (1989). Effects of baclofen on transient neurons in the mudpuppy retina: Electrogenic and network actions. Journal of Neurophysiology 61, 382–390.Google Scholar
Bindokas, V.P. & Ishida, A.T. (1991). (−)-baclofen and gamma-aminobutyric acid inhibit calcium currents in isolated retinal ganglion cells. Proceedings of the National Academy of Sciences of the U.S.A. 88, 10759–10763.Google Scholar
Bloomfield, S.A. & Miller, R.F. (1986). A functional organization of ON and OFF pathways in the rabbit retina. Journal of Neuroscience 6, 1–13.Google Scholar
Boue-Grabot, E., Roudbaraki, M., Bascles, L., Tramu, G., Bloch, B., & Garret, M. (1998). Expression of GABA receptor ρ subunits in rat brain. Journal of Neurochemistry 70, 899–907.Google Scholar
Cohen, E.D., Zhou, Z.J., & Fain, G.L. (1994). Ligand-gated currents of alpha and beta ganglion cells in the cat retinal slice. Journal of Neurophysiology 72, 1260–1269.Google Scholar
Enz, R. & Cutting, G.R. (1999). GABAC receptor ρ subunits are heterogeneously expressed in the human CNS and form homo- and heterooligomers with distinct physical properties. European Journal of Neuroscience 11, 41–50.Google Scholar
Enz, R., Brandstätter, J.H., Hartveit, E., Wässle, H., & Bormann, J. (1995). Expression of GABA receptor ρ1 and ρ2 subunits in the retina and brain of the rat. European Journal of Neuroscience 7, 1495–1501.Google Scholar
Enz, R., Brandstätter, J.H., Wässle, H., & Bormann, J. (1996). Immunocytochemical localization of the GABAC receptor ρ subunits in the mammalian retina. Journal of Neuroscience 16, 4479–4490.Google Scholar
Famiglietti, E.V., Kaneko, A., & Tachibana, M. (1977). Neuronal architecture of ON and OFF pathways to ganglion cells in carp retina. Science 198, 1267–1269.Google Scholar
Flores-Herr, N., Protti, D.A., & Wässle, H. (2001). Synaptic currents generating the inhibitory surround of ganglion cells in the mammalian retina. Journal of Neuroscience 21, 4852–4863.Google Scholar
Freed, M.A. & Sterling, P. (1988). The ON-alpha ganglion cell of the cat retina and its presynaptic cell types. Journal of Neuroscience 8, 2303–2320.Google Scholar
Greferath, U., Müller, F., Wässle, H., Shivers, B., & Seeburg, P. (1993). Localization of GABAA receptors in the rat retina. Visual Neuroscience 10, 551–561.Google Scholar
Greferath, U., Grünert, U., Fritschy, J.M., Stephenson, A., Möhler, H., & Wässle, H. (1995). GABAA receptor subunits have differential distributions in the rat retina: In situ hybridization and immunohistochemistry. Journal of Comparative Neurology 353, 553–571.Google Scholar
Greka, A., Koolen, J.A., Lipton, S.A., & Zhang, D. (1998). Cloning and characterization of mouse GABAC receptor subunits. Neuroreport 9, 229–232.Google Scholar
Greka, A., Lipton, S.A., & Zhang, D. (2000). Expression of GABAC receptor ρ1 and ρ2 subunits during development of the mouse retina. European Journal of Neuroscience 12, 3575–3582.Google Scholar
Grünert, U. & Wässle, H. (1993). Immunocytochemical localization of glycine receptors in the mammalian retina. Journal of Comparative Neurology 335, 523–537.Google Scholar
Grünert, U., Greferath, U., Boycott, B.B., & Wässle, H. (1993). Parasol (P alpha) ganglion-cells of the primate fovea: Immunocytochemical staining with antibodies against GABAA-receptors. Vision Research 33, 1–14.Google Scholar
Hu, E.H., Dacheux, R.F., & Bloomfield, S.A. (2000). A flattened retina-eyecup preparation suitable for electrophysiological studies of neurons visualized with trans-scleral infrared illumination. Journal of Neuroscience Methods 103, 209–216.Google Scholar
Ichinose, T. & Lukasiewicz, P.D. (2002). GABA transporters regulate inhibition in the retina by limiting GABAC receptor activation. Journal of Neuroscience 22, 3285–3292.Google Scholar
Ige, A.O., Bolam, J.P., Billinton, A., White, J.H., Marshall, F.H., & Emson, P.C. (2000). Cellular and sub-cellular localization of GABAB1 and GABAB2 receptor proteins in the rat cerebellum. Molecular Brain Research 83, 72–80.Google Scholar
Ishida, A.T. & Cohen, B.N. (1988). GABA-activated whole-cell currents in isolated retinal ganglion cells. Journal of Neurophysiology 60, 381–396.Google Scholar
Jacoby, R., Stafford, D., Kouyama, N., & Marshak, D. (1996). Synaptic inputs to ON parasol ganglion cells in the primate retina. Journal of Neuroscience 16, 8041–8056.Google Scholar
Kolb, H. & Nelson, R. (1993). OFF-alpha and OFF-beta ganglion cells in cat retina: II. Neural circuitry as revealed by electron microscopy of HRP stains. Journal of Comparative Neurology 329, 85–110.Google Scholar
Koulen, P., Sassoè-Pognetto, M., Grünert, U., & Wässle, H. (1996). Selective clustering of GABAA and glycine receptors in the mammalian retina. Journal of Neuroscience 16, 2127–2140.Google Scholar
Koulen, P., Brandstätter, J.H., Enz, R., Bormann, J., & Wässle, H. (1998a). Synaptic clustering of GABAC receptor ρ-subunits in the rat retina. European Journal of Neuroscience 10, 115–127.Google Scholar
Koulen, P., Malitschek, B., Kuhn, R., Bettler, B., Wässle, H., & Brandstätter, J.H. (1998b). Presynaptic and postsynaptic localization of GABAB receptors in neurons of the rat retina. European Journal of Neuroscience 10, 1446–1456.Google Scholar
Lasater, E.M. & Liu, Y. (2001). Properties of turtle retinal ganglion cell GABA receptors. Progress in Brain Research 131, 319–331.Google Scholar
Lin, B., Martin, P.R., Solomon, S.G., & Grünert, U. (2000). Distribution of glycine receptor subunits on primate retinal ganglion cells: A quantitative analysis. European Journal of Neuroscience 12, 4155–4170.Google Scholar
Macri, J., Martin, P.R., & Grünert, U. (2000). Distribution of the alpha1 subunit of the GABAA receptor on midget and parasol ganglion cells in the retina of the common marmoset Callithrix jacchus. Visual Neuroscience 17, 437–448.Google Scholar
Muller, J.F. & Dacheux, R.F. (1997). Alpha ganglion cells of the rabbit retina lose antagonistic surround responses under dark adaptation. Visual Neuroscience 14, 395–401.Google Scholar
Nelson, R., Famiglietti, E.V., & Kolb, H. (1978). Intracellular staining reveals different levels of stratification for on- and off-center ganglion cells in cat retina. Journal of Neurophysiology 41, 472–483.Google Scholar
Newberry, N.R. & Nicoll, R.A. (1984). Baclofen directly hyperpolarizes hippocampal cells. Nature 308, 163–174.Google Scholar
Ogurusu, T., Eguchi, G., & Shingai, R. (1997). Localization of gamma-aminobutyric acid (GABA) receptor ρ3 subunit in rat retina. Neuroreport 8, 925–927.Google Scholar
Ogurusu, T., Yanagi, K., Watanabe, M., Fukaya, M., & Shingai, R. (1999). Localization of GABA receptor ρ2 and ρ3 subunits in rat brain and functional expression of homooligomeric ρ3 receptors and heterooligomeric ρ2 ρ3 receptors. Receptors & Channels 6, 463–475.Google Scholar
Peichl, L., Buhl, E.H., & Boycott, B.B. (1987). Alpha ganglion cells in the rabbit retina. Journal of Comparative Neurology 263, 25–41.Google Scholar
Peters, B.N. & Masland, R.H. (1996). Responses to light of starburst amacrine cells. Journal of Neurophysiology 75, 469–480.Google Scholar
Pourcho, R.G. & Goebel, D.J. (1985). A combined Golgi and autoradiographic study of 3H glycine-accumulating amacrine cells in the cat retina. Journal of Comparative Neurology 233, 473–480.Google Scholar
Pourcho, R.G. & Owczarzak, M.T. (1991). Connectivity of glycine immunoreactive amacrine cells in the cat retina. Journal of Comparative Neurology 307, 549–561.Google Scholar
Qian, H. & Dowling, J.E. (1994). Pharmacology of novel GABA receptors found on rod horizontal cells of the white perch retina. Journal of Neuroscience 14, 4299–4307.Google Scholar
Qian, H., Dowling, J.E., & Ripps, H. (1998). Molecular and pharmacological properties of GABA-rho subunits from white perch retina. Journal of Neurobiology 37, 305–320.Google Scholar
Ragozzino, D., Woodward, R.M., Murata, Y., Eusebi, F., Overman, L.E., & Miledi, R. (1996). Design and in vitro pharmacology of a selective γ-aminobutyric acidC receptor antagonist. Molecular Pharmacology 50, 1024–1030.Google Scholar
Rotolo, T.C. & Dacheux, R.F. (2003). Evidence for glycine, GABAA, and GABAB receptors on rabbit OFF-alpha ganglion cells. Visual Neuroscience (in press).Google Scholar
Shen, W. & Slaughter, M.M. (1999). Metabotropic GABA receptors facilitate L-type and inhibit N-type calcium channels in single salamander retinal neurons. Journal of Physiology 516, 711–718.Google Scholar
Shingai, R., Yanagi, K., Fukushima, T., Sakata, K., & Ogurusu, T. (1996). Functional expression of GABA ρ3 receptors in Xenopus oocytes. Neuroscience Research 26, 387–390.Google Scholar
Slaughter, M.M. & Bai, S.-H. (1989). Differential effects of baclofen on sustained and transient cells in the mudpuppy retina. Journal of Neurophysiology 61, 374–381.Google Scholar
Ueno, S., Bracamontes, J., Zorumski, C., Weiss, D.S., & Steinbach, J.H. (1997). Bicuculline and gabazine are allosteric inhibitors of channel opening of the GABAA receptor. Journal of Neuroscience 17, 625–634.Google Scholar
Wässle, H. & Chun, M.H. (1988). Dopaminergic and indolamine-accumulating amacrine cells express GABA-like immunoreactivity in the cat retina. Journal of Neuroscience 8, 3383–3394.Google Scholar
Wässle, H., Peichl, L., & Boycott, B.B. (1981). Morphology and topography of on- and off-alpha cells in the cat retina. Proceedings of the Royal Society B (London), 212, 157–175.Google 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.Google Scholar
Xin, D. & Bloomfield, S.A. (1997). Tracer coupling pattern of amacrine and ganglion cells in the rabbit retina. Journal of Comparative Neurology 383, 512–528.Google Scholar
Yeh, H.H, Grigorenko, E.V., & Veruki, M.L. (1996). Correlation between a bicuculline-resistant response to GABA and GABAA receptor ρ1 subunit expression in single rat retinal bipolar cells. Visual Neuroscience 13, 283–292.Google Scholar
Zhang, J. & Slaughter, M.M. (1995). Preferential suppression of the ON pathway by GABAC receptors in the amphibian retina. Journal of Neurophysiology 74, 1583–1592.Google Scholar
Zhang, D., Pan, Z-H., Awobuluyi, M., & Lipton, S.A. (2001). Structure and function of GABAC receptors: A comparison of native versus recombinant receptors. Trends in Pharmacological Sciences 22, 121–132.Google Scholar