Hostname: page-component-78c5997874-mlc7c Total loading time: 0 Render date: 2024-11-15T13:22:25.812Z Has data issue: false hasContentIssue false
  • English
  • Français

Retinal bipolar cells receive negative feedback input from GABAergic amacrine cells

Published online by Cambridge University Press:  02 June 2009

Masao Tachibana  and
Akimichi Kaneko
Masao Tachibana
Affiliation:
Department of Information Physiology, National Institute for Physiological Sciences, Okazaki 444, Japan
Akimichi Kaneko
Affiliation:
Department of Information Physiology, National Institute for Physiological Sciences, Okazaki 444, Japan
Get access Rights & Permissions [Opens in a new window]

Abstract

Bipolar cells make reciprocal synapses with amacrine cells in the inner plexiform layer; both feedforward connections and feedback connections are present. The physiological properties of the feedback synapse have not been well described. Since some amacrine cells are thought to be GABAergic, we examined bipolar cells for feedback input from γ-aminobtyric acid (GABA)ergic amacrine cells. Solitary bipolar cells were dissociated enzymatically from the goldfish retina. Cells were voltage clamped with a patch pipette and their GABA sensitivity was examined. GABA evoked responses in all bipolar cells with a large axon terminal, which were identified to be the rod dominant ON type, and in some bipolar cells with a small axon terminal. The highest GABA sensitivity was located at the axon terminal. The least effective dose was as low as 100 nM. A small insignificant response of high threshold was evoked when GABA was applied to the dendrite and soma. GABA increased the Cl conductance and caused membrane hyperpolarization. The bipolar cells had the GABAA receptor coupled with a benzodiazepine receptor. The GABA-evoked response was not susceptible to Co ions, which suppressed the GABA-induced responses in turtle cones by 50% at 5 fiM concentration. Incomplete desensitization was observed, suggesting that the GABAergic pathway seems capable of transmitting signals tonically. The present results strongly indicate that the rod-dominant ON-type bipolar cells and some bipolar cells with a small axon terminal receive negative feedback inputs from GABAergic amacrine cells.

Keywords

RetinaBipolar cellAmacrine cellγ-aminobutyric acid
Type
Research Article
Information
Visual Neuroscience , Volume 1 , Issue 3 , May 1988 , pp. 297 - 305
Copyright
Copyright © Cambridge University Press 1988

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

Ayoub, G.S. & Lam, D.M.K. (1984). The release of γ-aminobutyric acid from horizontal cells of the goldfish (Carassius auratus) retina. Journal of Physiology 355, 191–214.CrossRefGoogle ScholarPubMed
Baylor, D.A., Fuortes, M.G.F. & O'Bryan, P.M. (1971). Receptive field of cones in the retina of the turtle. Journal of Physiology 214, 265–294.CrossRefGoogle ScholarPubMed
Burkhardt, D.A. (1977). Responses and receptive-field organization of cones in perch retinas. Journal of Neurophysiology 40, 53–62.CrossRefGoogle ScholarPubMed
Burkhardt, D.A. & Hassin, G. (1978). Influences of cones upon chromatic- and luminosity-type horizontal cells in pikeperch retinas. Journal of Physiology 281, 125–137.CrossRefGoogle ScholarPubMed
Famiglietti, E.V. Jr., Kaneko, A. & Tachibana, M. (1977). Neuronal architecture of ON and OFF pathways to ganglion cells in carp retina. Science 198, 1267–1269.CrossRefGoogle Scholar
Fuortes, M.G.F. & Simon, E.J. (1974). Interactions leading to horizontal cell responses in the turtle retina. Journal of Physiology 240, 177–198.CrossRefGoogle ScholarPubMed
Gahwiler, B.H. & Brown, D.A. (1985). GABAB-receptor-activated K+ current in voltage clamped CA3 pyramidal cells in hippocampal cultures. Proceedings of National Academy of Science (USA) 82, 1558–1562.CrossRefGoogle ScholarPubMed
Hamill, O.P., Marty, A., Neher, E., Sakmann, B. & SIGWORTH, F.J. (1981). Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Plfugers Archiev 391, 85–100.CrossRefGoogle ScholarPubMed
Hattori, K., Oomura, Y. & Akaike, N. (1986). Diazepam action on γ-aminobutyric acid-activated chloride currents in internally perfused frog sensory neurons. Cellular and Molecular Neurobiology 6, 307–323.CrossRefGoogle ScholarPubMed
Hill, D.R. & Bowery, N.G. (1981). 3H-baclofen and 3H-GABA bind to bicuculline-insensitive GABAB sites in rat brain. Nature 290, 149–152.CrossRefGoogle Scholar
IshiDA, A.T., Kaneko, A. & Tachibana, M. (1984). Responses of solitary retinal horizontal cells from Carassius auratus to L-glutamate and related amino acids. Journal of Physiology 348, 255–270.CrossRefGoogle ScholarPubMed
Kaneko, A. & Tachibana, M. (1985). A voltage-clamp analysis of membrane currents in solitary bipolar cells dissociated from Carassius auratus. Journal of Physiology 358, 131–152.CrossRefGoogle ScholarPubMed
Kaneko, A. & Tachibana, M. (1986). Blocking effects of cobalt and related ions on the γ-aminobutyric acid-induced current in turtle retinal cones. Journal of Physiology 373, 463–479.CrossRefGoogle ScholarPubMed
Kaneko, A. & Tachibana, M. (1987). Effects of transmitter candidates on bipolar cells dissociated from the goldfish retina. Neuroscience Research Supplement 5, S186.CrossRefGoogle Scholar
Kondo, H. & Toyoda, J.-I. (1983). Gaba and glycine effects on the bipolar cells of the carp retina. Vision Research 23, 1259–1264.CrossRefGoogle ScholarPubMed
Lam, D.M.K. & Steinman, L. (1971). The uptake of [γ-3H] aminobutyric acid in the goldfish retina. Proceedings of National Academy of Science (USA) 68, 2777–2781.CrossRefGoogle ScholarPubMed
Lam, D.M.K., Su, Y.Y.T., Swain, L., Marc, R.E., Brandon, C. & Wu, J.-Y. (1979). Immunocytochemical localization of L-glutamic acid decarboxylase in the goldfish retina. Nature 278, 565–567.CrossRefGoogle ScholarPubMed
Marc, R.E., Stell, W.K., Bok, D. & Lam, D.M.K. (1978). GABAergic pathways in the goldfish retina. Journal of Comparative Neurology 182, 221–246.CrossRefGoogle ScholarPubMed
Murakami, M., Shimoda, Y., Nakatani, K., Miyachi, E. & Watanabe, S. (1982 a). Gaba-mediated negative feedback from horizontal cells to cones in carp retina. Japanese Journal of Physiology 32, 911–926.Google ScholarPubMed
Murakami, M., Shimoda, Y., Nakatani, K., Miyachi, E. & Watanabe, S. (1982 b). Gaba-mediated negative feedback and color opponency in carp retina. Japanese Journal of Physiology 32, 927–935.Google ScholarPubMed
Naka, K-I. (1977). Functional organization of catfish retina. Journal of Neurophysiology 40, 26–43.CrossRefGoogle ScholarPubMed
Saito, T. & Kujiraoka, T. (1982). Physiological and morphological identification of two types of on-center bipolar cells in the carp retina. Journal of Comparative Neurology 205, 161–170.CrossRefGoogle ScholarPubMed
Saito, T., Kujiraoka, T., Yonaha, T. & Chino, Y. (1985). Reexamination of photoreceptor-bipolar connectivity patterns in carp retina: HRP-EM and Golgi-EM studies. Journal of Comparative Neurology 236, 141–160.CrossRefGoogle ScholarPubMed
Stell, W.K., Lightfoot, D.O., Wheeler, T.G. & Leeper, H.F. (1975). Goldfish retina: functional polarization of cone horizontal cell dendrites and synapses. Science 190, 989–990.CrossRefGoogle ScholarPubMed
Stell, W.K. & Lightfoot, D.O. (1975). Color-specific interconnections of cones and horizontal cells in the retina of the goldfish. Journal of Comparative Neurology 159, 473–502.CrossRefGoogle ScholarPubMed
Tachibana, M. & Kaneko, A. (1984). γ-Aminobutyric acid acts at axon terminals of turtle photoreceptors: difference in sensitivity among cell types. Proceedings of National Academy of Science (USA) 81, 7961–7964.CrossRefGoogle ScholarPubMed
Tachibana, M. & Kaneko, A. (1987). γ-Aminobutyric acid exerts a local inhibitory action on the axon terminal of bipolar cells: evidence for negative feedback from amacrine cells. Proceedings of National Academy of Science (USA) 84, 3501–3505.CrossRefGoogle ScholarPubMed
Toyoda, J-I. & Fujmoto, M. (1984). Application of transretinal current stimulation for the study of bipolar-amacrine transmission. Journal of General Physiology 84, 915–925.CrossRefGoogle Scholar
Umino, O. & Watanabe, K. (1987). Neural mechanism of chromatic adaptation of L-type external horizontal cells (LEHC) in carp retina. Journal of the Physiological Society of Japan 49, 451.Google Scholar
Witkovsky, P. & Dowling, J.E. (1969). Synaptic relationships in the plexiform layers of carp retina. Zeitschrift fiir Zellforschung 100, 60–82.CrossRefGoogle ScholarPubMed
Wu, J.-Y., Brandon, C., SU, Y.Y.T. & Lam, D.M.K. (1981). Immunocytochemical and autoradiographic localization of Gaba system in the vertebrate retina. Molecular Cell Biochemistry 39, 229–238.CrossRefGoogle ScholarPubMed
Yazulla, S. (1976). Cone input to horizontal cells in the turtle retina. Vision Research 16, 727–735.CrossRefGoogle ScholarPubMed
Yazulla, S. (1981). Gabaergic synapses in the goldfish retina: an autoradiographic study of 3H-muscimol and 3H-GABA binding. Journal of Comparative Neurology 200, 83–93.CrossRefGoogle ScholarPubMed
Yazulla, S. & Brecha, N. (1980). Binding and uptake of the GABA analogue, 3H-muscimol, in the retinas of goldfish and chicken. Investigative Ophthalmology and Visual Science 19, 1415–1426.Google ScholarPubMed
Yazulla, S., Studholme, K. & Wu, J-Y. (1986). Comparative distribution of 3H-GABA uptake and GAD immunoreactivity in goldfish retinal amacrine cells: a double-label analysis. Journal of Comparative Neurology 224, 149–162.CrossRefGoogle Scholar
Yazulla, S., Studholme, K. & Wu, J-Y. (1987). GABAergic input to the synaptic terminals of mb bipolar cells in the goldfish retina. Brain Research 411, 400–405.CrossRefGoogle Scholar
Zucker, C., Yazulla, S. & Wu, J-Y. (1984). Non-correspondence of [3H]GABA uptake and GAD localization in goldfish amacrine cells. Brain Research 298, 154–158.CrossRefGoogle ScholarPubMed