Skip to main content
    • Aa
    • Aa

Functional role of GABA in cat retina: II. Effects of GABAA antagonists

  • Thomas E. Frumkes (a1) (a2), Ralph Nelson (a1) and Renate Pflug (a3)

Putative GABAergic mechanisms were studied in the cat retina by exogenous application of the GABAA antagonists picrotoxin (PTX), native bicuculline (BCC), and bicuculline methyl bromide (BCC MeBr). When recording intracellular responses from horizontal cells (HCs) and amacrine cells as well as electroretinograms (ERGs), drugs were added to the perfusate used to maintain the isolated eyecup; when recording extracellular spikes from ganglion cells of anesthetized cats, drugs were introduced by iontophoretic injection. Both PTX and BCC MeBr had relatively little influence upon the response properties of HCs. In contrast, native BCC tended to decrease the amplitude of and to slow the photic response to light onset and both to quicken and to increase the amplitude of response to light offset; in the presence of native BCC, HC responses were dominated by a prominent spike-like “Off-overshoot.” The influence of GABAA agonists upon HC responses was not blocked by GABAA antagonists. ERG b−wave amplitude was reduced both by PTX and by native BCC, but was not influenced by BCC MeBr. Latency (time to half-peak) was increased by low doses of native BCC, and to a lesser extent PTX but not BCC MeBr. Rod-amacrine On-transient responses were increased in amplitude by PTX. Extracellular recordings from On- and Off- X and Y ganglion cell types became considerably more transient with application of either PTX, native BCC, or BCC MeBr; this tendency was greater in Off-type ganglion cells. Collectively, these results strengthen conclusions from the previous paper suggesting that GABA serves to slow onset and offset kinetics of retinal neurons, making them more sustained and less phasic. They also suggest that in mammalian retina heterogeneous types of GABAA receptors exist, segregated into different zones: a distal zone, sensitive only to native BCC, a central zone sensitive to both native BCC and PTX, and a proximal zone sensitive to native BCC, BCC methyl halides (BCC MeH), and PTX. Only the proximal zone obeys conventional GABAA pharmacology.

Hide All
Bindokas V.P. & Ishida A.T. (1991). (—)-baclofen and γ-aminobutyric acid inhibit calcium currents in isolated retinal ganglion cells. Proceedings of the National Academy of Sciences of the U.S.A. 88, 1075910763.
Bolz J., Frumkes T.E., Voigt T. & Wässle H. (1985). Action and localization of gamma-aminobutyric acid in the cat retina. Journal of Physiology 362, 369393.
Cutting G.R., Curristin S., Zoghbi H., O'Hara B., Seldin M.F. & Uhl G.R. (1992). Identification of a putative γ-aminobutyric acid (GABA) receptor subunit rho2 cDNA and colocalization of the genes encoding rho2 (GABRR2) and rho1 (GABRR1) to human chromosome 6q14-q21 and mouse chromosome 4. Genomics 12, 801806.
Cutting G.R., Lu L., O'Hara B.F., Kasch L.M., Montrose-Rafizadeh C., Donovan D.M., Shimada S., Antonarakis S.E., Guggino W.B., Uhl G.R. & Kazazian H.H. Jr., (1991). Cloning of the γ-aminobutyric acid (GABA) ρ 1, cDNA: A GABA receptor subunit highly expressed in the retina. Proceedings of the National Academy of Sciences of the U.S.A. 88, 26732677.
Feigenspan A., Wässle H. & Bormann H. (1993). Pharmacology of GABA receptor Cl¯ channels in rat retinal bipolar cells. Nature 361, 159162.
Freed M.A., Nakamura Y. & Sterling P. (1983). Four types of amacrine in the cat retina that accumulate GABA. Journal of Comparative Neurology 219, 295304.
Freed M.A., Smith R.G. & Sterling P. (1987). Rod bipolar array in the cat retina: Pattern of input from rods and GABA-accumulating amacrine cells. Journal of Comparative Neurology 266, 445455.
Frishman L.J. & Linsenmeier R.A. (1982). Effects of picrotoxin and strychnine on non-linear responses of Y-type cat retinal ganglion cells. Journal of Physiology 324; 347363.
Frishman L.J. & Steinberg R.H. (1989). Light-evoked increases in [K+]0 in proximal portion of the dark-adapted cat retina. Journal of Neurophysiology 61, 12331243.
Frishman L.J., Yamamoto F., Bogucka J. & Steinberg R.H. (1990). Pharmacological separation of proximal and distal contributions to the dark-adapted ERG of cat retina. Investigative Ophthalmology and Visual Sciences 31, 390.
Frumkes T.E. & Nelson R. (1991). GABAergic transmission in distal mammalian retina. Neuroscience Abstracts 17, 13.
Frumkes T.E. & Nelson R. (1995). Functional role of GABA in cat retina: 1. Effects of GABAA agonists. Visual Neuroscience 12, 641650.
Frumkes T.E., Voigt T. & Wässle H. (1984). Functional organization of GABA and glycine input to cat retinal ganglion cells. Neuroscience Abstracts 10, 20.
Gottlob I., Wündsch L. & Tupply F.K. (1988). The rabbit electroretinogram: Effects of GABA and its antagonists. Vision Research 28, 203210.
Greferath U., Müller F., Wässle H., Shivers B. & Seeburg P. (1993). Localization of GABAA receptors in the rat retina. Visual Neuroscience 10, 551562.
Grigorenko E.V. & Yeh H.H. (1994). GABAA receptor subunit profiles in single photoreceptors and bipolar cells of the rat retina. Investigative Ophthalmology and Visual Sciences 35, 1364.
Hankins M.W. & Ruddock K.H. (1984). Electrophysiological effects of GABA on fish retinal horizontal cells are blocked by bicuculline but not by picrotoxin. Neuroscience Letters 44, 16.
Hughes T.E., Grünert U. & Karten H.J. (1991). GABAA receptors in the retina of the cat: An immunohistochemical study of wholemounts, sections, and dissociated cells. Visual Neuroscience 6, 229238.
Ikeda H. & Sheardown M.J. (1983). Transmitters mediating inhibition of ganglion cells in the cat retina: Iontophoretic studies in vivo. Neuroscience 8, 837853.
Ishida A.T. (1992). The physiology of GABAA receptors in retinal neurons. In Progress in Brain Research, Vol. 90: GABA in the Retina and Central Nervous System, ed. Mize R.R., Mark R.E. & Sillito A.M., pp. 2945. Amsterdam: Elsevier.
Kaneko A., Pinto L.H. & Tachibana M. (1989). Transient calcium current of retinal bipolar cells of the mouse. Journal of Physiology 410, 613629.
Kaneko A. & Tachibana M. (1986). Blocking effects of cobalt and related ions on the gamma-aminobutyric acid-induced current in turtle retinal cones. Journal of Physiology 373, 463479.
Karschin A. & Wässle H. (1990). Voltage- and transmitter-gated currents in isolated rod bipolar cells of rat retina. Journal of Neurophysiology 63, 860876.
Kirby A.W. & Enroth-Cugell C. (1976). The involvement of gamma-aminobutyric acid in the organization of cat retinal ganglion cell receptive fields. A study with picrotoxin and bicuculline. Journal of General Physiology 68, 465484.
Kirby A.W. & Schweitzer-Tong D.E. (1981 a). GABA-antagonists and spatial summation in Y-type cat retinal ganglion cells. Journal of Physiology 312, 335344.
Kirby A.W. & Schweitzer-Tong D.E. (1981 b). GABA-antagonists alter spatial summation in receptive-field centres of rod- but not conedriven cat retinal ganglion Y-cells. Journal of Physiology (London) 320, 303308.
Kolb H. & West R.W. (1977). Synaptic connections of the interplexiform cell in the retina of the cat. Journal of Neurocytology 6, 155170.
Lipton S.A. & Tauk D.L. (1987). Voltage-dependent conductances of solitary ganglion cells dissociated from the rat retina. Journal of Physiology 385, 361391.
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, 12021212.
Naarendorp F. & Sieving P.A. (1990). The scotopic threshold response of the cat ERG is suppressed selectively by GABA and glycine. Vision Research 31, 115.
Nelson R., Frumkes T.E. & Pflug R. (1992). The relative potency of GABAA antagonists is different in inner and outer mammalian retina. Investigative Ophthalmology and Visual Sciences 33, 1032.
Nelson R. & Kolb H. (1985). A17: A broad-field amacrine cell in the rod system of the cat retina. Journal of Neurophysiology 54, 592614.
Newman E.A. (1987). Distribution of potassium conductance in mammalian Müller (glial) cells: A comparative study. Journal of Neuroscience 7, 24232432.
Oakley B. II, & Green D.G. (1976). Correlation of light-induced changes in retinal extracellular potassium concentration with c−wave of the electroretinogram. Journal of Neurophysiology 39, 11171133.
Olsen R.W., Ban M., Miller T. & Johnston G.A.R. (1975). Chemical instability of the GABA antagonist bicuculline under physiological conditions. Brain Research 98, 383387.
Perlman I. & Normann R.A. (1990). The effects of GABA and related drugs on horizontal cells in the isolated turtle retina. Visual Neuroscience 5, 469477.
Saito H.-A. (1981). The effects of strychnine and bicuculline on the responses of X- and Y-cells of the isolated eye-cup preparation of the cat. Brain Research 212, 243248.
Saito H.-A. (1983). Pharmacological and morphological differences between X- and Y-type ganglion cells in the cat's retina. Vision Research 23, 12991308.
Shimada S., Cutting G. & Uhl G.R. (1992). γ-aminobutyric acid A or C receptor? γ-aminobutyric acid ρ 1, receptor RNA induces bicuculline-, barbiturate-, and benzodiazepine-insensitive γ-aminobutyric acid responses in Xenopus oocytes. Molecular Pharmacology 41, 683687.
Steinberg R.H., Frishman L.J. & Sieving P.A. (1991). Negative components of the electroretinogram from proximal retina and photoreceptor. In Progress in Retinal Research, Vol. 10, ed. Osborne N. & Chader G., pp. 121160. Oxford: Pergamon Press.
Stockton R.A. & Slaughter M.M. (1991). Depolarizing actions of GABA and glycine upon amphibian retinal horizontal cells. Journal of Neurophysiology 65, 680692.
Stone S. & Witkovsky P. (1984). The actions of γ-aminobutyric acid, glycine and their antagonists upon horizontal cells of the Xenopus retina. Journal of Physiology 353, 249264.
Suzuki S., Tachibana M. & Kaneko A. (1990). Effects of glycine and GABA on isolated bipolar cells of the mouse retina. Journal of Physiology 421, 645662.
Tachibana M. (1981). Membrane properties of solitary horizontal cells isolated from goldfish retina. Journal of Physiology 321, 141161.
Ueda Y., Kaneko A. & Kaneda M. (1992). Voltage-dependent ionic currents in solitary horizontal cells isolated from cat retina. Journal of Neurophysiology 68, 11431150.
Wu S.M. & Dowling J.E. (1980). Effects of GABA and glycine on the distal cells of the cyprinid retina. Brain Research 199, 401414.
Yang X.L. & Wu S.M. (1989). Effects of prolonged light exposure, GABA, and glycine on horizontal cell responses of tiger salamander retina. Journal of Neurophysiology 61, 10251035.
Yeh H.H., Lee M.B. & Cheun J.E. (1990). Properties of GABA-activated whole-cell currents in bipolar cells of the rat retina. Visual Neuroscience 4, 349357.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

Visual Neuroscience
  • ISSN: 0952-5238
  • EISSN: 1469-8714
  • URL: /core/journals/visual-neuroscience
Please enter your name
Please enter a valid email address
Who would you like to send this to? *



Full text views

Total number of HTML views: 0
Total number of PDF views: 4 *
Loading metrics...

Abstract views

Total abstract views: 106 *
Loading metrics...

* Views captured on Cambridge Core between September 2016 - 19th October 2017. This data will be updated every 24 hours.