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The role of GABA in modulating the Xenopus electroretinogram

Published online by Cambridge University Press:  02 June 2009

Arsaell Arnarsson  and
Thor Eysteinsson
Arsaell Arnarsson
Affiliation:
Department of Physiology, University of Iceland, 101 Reykjavik, Iceland
Thor Eysteinsson
Affiliation:
Department of Physiology, University of Iceland, 101 Reykjavik, Iceland
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Abstract

We have recorded the electroretinogram (ERG) from the superfused eyecup of the Xenopus retina in order to assess the effects of the inhibitory neurotransmitter gamma-aminobutyric acid (GABA), and its agonists and antagonists, on individual ERG components. We found that GABA (0.5–10 mM) reduced the amplitudes of both the b- and d-waves of the Xenopus ERG. The GABA uptake blocker nipecotic acid (1 mM) had similar effects on b- and d-waves. GABA at 5 mM and 10 mM also caused an increase in the a-wave. The GABA antagonist picrotoxin (0.1–2 mM) and the GABA/a antagonist bicuculline (0.2 mM) both increased the amplitude of the b- and d-waves of the ERG. The GABA/b agonist baclofen (0.3 mM) reduced the amplitude of the ERG b-wave, enhanced the amplitude of the a-wave, and slightly reduced the amplitude and increased the peak time of the d-wave. The GABA/b antagonists phaclofen and saclofen had no reliable effects on the Xenopus ERG. Glutamate analogs known to affect specific types of retinal neurons were applied to modify the retinal circuitry and then the effects of GABA and its antagonists were examined under these modified conditions. 2-amino-4-phosphonobutyric acid (APB) increased the d-wave, and blocked the b-wave and the effect of GABA on the ERG, but not the antagonist-induced increase in the d-wave. KYN blocked the antagonist-induced increase in the b-wave, while GABA increases the amplitude of the b-wave if the d-wave has been removed by prior superfusion with kynurenic acid (KYN). N-methyl-DL-aspartate (NMDLA), which acts only in the proximal retina, reduced the amplitude of the ERG and blocked the effect of GABA and the antagonist-induced increase in ERG b- and d-waves amplitude. These results suggest that GABAergic mechanisms related to both A and B receptor types can influence the amplitude and light sensitivity of all the components of the Xenopus ERG. Since GABA is found in greatest abundance in the proximal retina, and B type of receptors are present almost exclusively there, the data suggests that most of the effects of GABA agonists and antagonists observed are dependent on proximal retinal mechanisms, and that there are separate mechanisms in the proximal retina related to the b- and the d-waves.

Keywords

XenopusERGGABAGlutamate analogsBaclofen
Type
Research Articles
Information
Visual Neuroscience , Volume 14 , Issue 6 , November 1997 , pp. 1143 - 1152
Copyright
Copyright © Cambridge University Press 1997

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References

Arkin, M.S. & Miller, R.F. (1987). Subtle action of 2-amino-4-phosphonobutyriate (APB) on the Off pathway in the mudpuppy retina. Brain Research 426, 142–148.Google Scholar
Attwell, D., Mobbs, P., Tessier-Lavigne, M. & Wilson, M. (1987). Neurotransmitter-induced currents in retinal bipolar cells of the axolotl, ambystoma mexicanum. Journal of Physiology 387, 125–161.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Bormann, J. (1988). Electrophysiology of GABAA & GABAB receptor subtypes. Trends in Neurosciences 11, 112–116.Google Scholar
Brandon, C., Lam, D. M.-K., Su, Y. Y.T. & Wu, J.-Y. (1980). Immuno-cytochemical localization of GABA neurons in the rabbit and frog retina. Brain Research Bulletin (Suppl.) 5, 21–29.Google Scholar
Coleman, P.A., Massey, S.C. & Miller, R.F. (1986). Kynurenic acid distinguishes kainate and quisqualate receptors in the vertebrate retina. Brain Research 381, 172–175.CrossRefGoogle ScholarPubMed
Dick, E. & Miller, R.F. (1985). Extracellular K+-activity changes related to electroretinogram components I: Amphibian (I-type) retinas. Journal of General Physiology 85, 911–931.CrossRefGoogle ScholarPubMed
Eysteinsson, T., Frumkes, T.E., & Poulos, D. (1993). Alpha-aminopimelic acid: Another new tool for retinal research. ARVO 34, 1332.Google Scholar
Frumkes, T.E. & Eysteinsson, T. (1987). Suppressive rod-cone interaction in distal vertebrate retina: Intracellular records from Xenopus and necturus. Journal of Neurophysiology 57, 1361–1382.CrossRefGoogle ScholarPubMed
Gottlob, I., Wundsch, L. & Tuppy, F.K. (1988). The rabbit electroretinogram: Effect of GABA and its antagonists. Vision Research 28, 203–210.Google Scholar
Hollyfield, J.G., Rayborn, M.E., Sarthy, P.V. & Lam, D.M.K. (1979). The emergence, localization, and maturation of neurotransmitter systems during development of the retina in Xenopus laevis: I gamma-aminobutyric acid. Journal of Comparative Neurology 188, 587–598.CrossRefGoogle ScholarPubMed
Karwoski, C.J. & Proenza, L.M. (1977). Relationship between Müller cell responses, a local transretinal potential, and potassium flux. Journal of Neurophysiology 40, 244–259.Google Scholar
Katz, B.J., Wen, R., Zheng, J., Xu, Z. & IIOakley, B. (1991). M-wave of the toad electroretinogram. Journal of Neurophysiology 66, 1927–1940.CrossRefGoogle ScholarPubMed
Lerma, J., Herreras, O., Herranz, A.S., Munoz, D. & del Rio, R.M. (1984). In vivo effects of nipecotic acid on levels of extracellular GABA and taurine, and hippocampal excitability. Neuropharmacology 23, 595–598.Google Scholar
Lukasiewicz, P.D., Maple, B.R. & Werblin, F.S. (1994). A novel GABA receptor on bipolar cell terminals in the tiger salamander retina. Journal of Neuroscience 14, 1202–1212.CrossRefGoogle ScholarPubMed
Maguire, G., Maple, B., Lukasiewicz, P. & Werblin, F. (1989). GABA type B receptor modulation of L-type calcium channel current at bipolar cell terminals in the retina of the tiger salamander. Proceedings of the National Academy of Sciences of the U.S.A. 86, 10144–10147.CrossRefGoogle ScholarPubMed
Massey, S.C., Redburn, D.A., & Crawford, M.L.J. (1983). The effects of 2-amino-4-phosphonobutyric acid (APB) on the ERG and ganglion cell discharge of rabbit retina. Vision Research 23, 1607–1613.Google Scholar
Massey, S.C. & Miller, R.F. (1990). NMDA receptors of ganglion cells in rabbit retina. Journal of Neurophysiology 63, 16–30.CrossRefGoogle ScholarPubMed
Miller, R.F. & Dowling, J.E. (1970). Intracellular response of the Müller (glia) cells of mudpuppy retina: Their relation to the b-wave of the electroretinogram. Journal of Neurophysiology 33, 323–334.CrossRefGoogle Scholar
Miller, R.F., Frumkes, T.E., Slaughter, M.M. & Dacheux, R.F. (1981). Physiological and pharmacological basis of GABA and glycine action on neurons in the mudpuppy retina. I. Receptors, horizontal cells, bipolars, and G-cells. Journal of Neurophysiology 45, 743–763.CrossRefGoogle ScholarPubMed
Miller, R.F. & Slaughter, M.M. (1986). Excitatory amino acid receptors of the retina: Diversity of subtypes and conductance mechanisms. Trends in Neuroscience 9, 211–218.CrossRefGoogle Scholar
Mosinger, J.L., Studholme, K.M. & Yazulla, S. (1986). Immunocyto-chemical localization of GABA in the retina: A species comparison. Experimental Eye Research 42, 631–644.CrossRefGoogle Scholar
Naarendorp, F. & Sieving, P.A. (1991). The scotopic threshold response of the cat ERG is suppressed selectively by GABA and glycine. Vision Research 31, 1–15.Google Scholar
Newman, E.A. & Odette, L.L. (1984). Model of electroretinogram b-wave generation: A test of the K+ hypothesis. Journal of Neurophysiology 51, 164–182.CrossRefGoogle ScholarPubMed
Slaughter, M.M. & Bai, S.-H. (1989). Differential effects of baclofen on sustained and transient cells in the mudpuppy retina. Journal of Neurophysiology 6, 374–381.Google Scholar
Slaughter, M.M. & Miller, R.F. (1981). 2-Amino-4-phosphonobutyric acid: An new pharmacological tool for retinal research. Science 211, 182–185.Google Scholar
Slaughter, M.M. & Miller, R.F. (1983 a). The role of EAA transmitters in the mudpuppy retina: An analysis with kainic acid and N-methyl aspartate. Journal of Neuroscience 3, 1701–1711.CrossRefGoogle Scholar
Slaughter, M.M. & Miller, R.F. (1983 b). An excitatory amino acid antagonist blocks cone input to sign-conserving synapse. Science 219, 1230.CrossRefGoogle Scholar
Slaughter, M.M. & Miller, R.F. (1983 c). Bipolar cells in the mudpuppy use an EAA neurotransmitter. Nature 303, 537–538.CrossRefGoogle Scholar
Stockton, R. & Slaughter, M.M. (1989). The b-wave of the electroretinogram: A reflection of ON-bipolar cell activity. Journal of General Physiology 93, 101–122.Google Scholar
Stockton, R.A. & Slaughter, M.M. (1991). Depolarizing actions of GABA and Glycine on amphibian retinal horizontal cells. Journal of Neurophysiology 65, 680–692.CrossRefGoogle ScholarPubMed
Stone, S. & Witkovsky, P. (1984). The actions of gamma-aminobutyric acid, glycine, and their antagonists upon horizontal cells of the Xenopus retina. Journal of Physiology 353, 249–264.CrossRefGoogle ScholarPubMed
Stone, S. & Schutte, M. (1991). Physiological and morphological properties of OFF-center bipolar cells in the Xenopus retina: Effects of glycine and GABA. Visual Neuroscience 7, 363–376.Google Scholar
Tachibana, M. & Kaneko, A. (1988). Retinal bipolar cells receive negative feedback input from GABAergic amacrine cells. Visual Neuroscience 1, 297–307.CrossRefGoogle ScholarPubMed
Tian, N. & Slaughter, M.M. (1994). Pharmacology of the GABA/B receptor in amphibian retina. Brain Research 660, 267–274.Google Scholar
Witkovsky, P., Stone, S. & Ripps, H. (1985). Pharmacological modification of the light-induced responses of Müller (glial) cells in the amphibian retina. Brain Research 328, 111–120.Google Scholar
Woodward, R.M., Polenzani, L., & Miledi, R. (1992). Characterization of bicuculline/baclofen-insensitive GABA receptors expressed in Xenopus oöcytes. I. Effects of Cl−-channel inhibitors. Molecular Pharmacology 42, 165–173.Google Scholar
Wu, S.M. (1986). Effects of GABA on cones and bipolar cells of the tiger salamanda retina. Brain Research 365, 70–77.CrossRefGoogle ScholarPubMed
Yang, C.Y. & Yazulla, S. (1988). Localization of putative GABAergic neurons in the larval tiger salamander retina by immunocytochemical and autoradiographic methods. Journal of Comparative Neurology 277, 96–108.CrossRefGoogle ScholarPubMed