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GABA-mediated component in the feedback response of turtle retinal cones

Published online by Cambridge University Press:  02 August 2005

T. TATSUKAWA ,
H. HIRASAWA ,
A. KANEKO  and
M. KANEDA
T. TATSUKAWA
Affiliation:
Department of Physiology, Keio University School of Medicine, Shinjuku-ku, Tokyo, Japan Present address of T. Tatsukawa: Laboratory of Cellular Neurobiology School of Life Science, Tokyo University of Pharmacy and Life Science, 1432-1 Horinouchi, Hachioji-shi, Tokyo 192-0392, Japan
H. HIRASAWA
Affiliation:
Department of Physiology, Keio University School of Medicine, Shinjuku-ku, Tokyo, Japan Present address of H. Hirasawa: Department of Neurobiology, Harvard Medical School, Boston, MA 02115, USA
A. KANEKO
Affiliation:
Department of Physiology, Keio University School of Medicine, Shinjuku-ku, Tokyo, Japan Present address of A. Kaneko: Seijoh University School of Rehabilitation, 2-172 Fukinodai, Tokai-shi, Aichi 476-8588, Japan
M. KANEDA
Affiliation:
Department of Physiology, Keio University School of Medicine, Shinjuku-ku, Tokyo, Japan
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Abstract

The negative feedback from horizontal cells to cone photoreceptors contributes to the formation of the receptive-field surround in cone photoreceptors. Recently, studies on the modulation of voltage-gated Ca2+ currents in cone photoreceptors have led to great progress in our understanding of the mechanism of horizontal-cone feedback. Another highly probable hypothesis is that GABA mediates this feedback. This hypothesis is supported by the facts that cone photoreceptors respond to GABA and that horizontal cells release GABA. However, GABA-mediated synaptic inputs from horizontal cells to cone photoreceptors have not been demonstrated. In the present study, we examined whether cone photoreceptors receive GABAergic inputs from horizontal cells using a slice patch technique in the turtle retina. When 1 mM of GABA was applied to the cone photoreceptors, GABA-induced currents were activated. GABA-induced currents reversed their polarity at the equilibrium potential of Cl−. The application of 30 μM of SR95531, an antagonist of GABAA receptors, alone did not produce any change in the holding currents. When 200 μM of pentobarbital was introduced to potentiate the GABAergic inputs to the cone photoreceptors, however, the inhibitory action of SR95531 on GABAergic inputs became detectable. The amplitude of the GABAergic inputs, potentiated by pentobarbital, increased when the horizontal cells were depolarized by the application of 20 μM of kainate, while the amplitude decreased when the horizontal cells were hyperpolarized by the application of 10 μM of CNQX. When the cone photoreceptors were voltage clamped at a potential at which the voltage-gated Ca2+ current was inactive, horizontal-cone feedback was not observed. However, the horizontal-cone feedback became detectable when the GABAergic inputs to the cone photoreceptors were potentiated by pentobarbital. We concluded that the contribution of GABAergic inputs from horizontal cells to cone pedicles in the formation of the receptive-field surround in cone photoreceptors is very limited but that the modulation of voltage-gated Ca2+ currents in cone photoreceptors is a physiologically relevant mechanism for horizontal-cone feedback.

Keywords

GABACone photoreceptorHorizontal cellRetinaTurtle
Type
Research Article
Information
Visual Neuroscience , Volume 22 , Issue 3 , May 2005 , pp. 317 - 324
Copyright
2005 Cambridge University Press

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References

REFERENCES

Akaike, N., Inomata, N., & Yakushiji, T. (1989). Differential effects of extra- and intracellular anions on GABA-activated currents in bullfrog sensory neurons. Journal of Neurophysiology 62, 1388–1399.Google Scholar
Akaike, N. & Kaneda, M. (1989). Glycine-induced chloride current in acutely isolated rat hypothalamic neurons. Journal of Neurophysiology 62, 1400–1409.Google Scholar
Ayoub, G.S. & Lam, D.M.K. (1985). The content and release of endogenous GABA in isolated horizontal cells of the goldfish retina. Vision Research 25, 1187–1193.Google Scholar
Baylor, D.A, Fuortes, M.G., & O'Bryan, P.M. (1971). Receptive fields of cones in the retina of the turtle. Journal of Physiology 214, 265–294.Google Scholar
Fatima-Shad, K. & Barry, P.H. (1993). Anion permeation in GABA- and glycine-gated channels of mammalian cultured hippocampal neurons. Proceedings of the Royal Society B (London) 253, 69–75.Google Scholar
Gerschenfeld, H.M. & Piccolino, M. (1980). Sustained feedback effects of L-horizontal cells on turtle cones. Proceedings of the Royal Society B (London) 206, 465–480.Google Scholar
Hirasawa, H. & Kaneko, A. (2003). pH changes in the invaginating synaptic cleft mediate feedback from horizontal cells to cone photoreceptors by modulating Ca2+ channels. Journal of General Physiology 122, 657–671.Google Scholar
Kaneda, M., Wakamori, M., & Akaike, N. (1989). GABA-induced chloride current in rat isolated Purkinje cells. American Journal of Physiology 256, C1153–C1159.Google Scholar
Kaneko, A. & Tachibana, M. (1986). Effects of gamma-aminobutyric acid on isolated cone photoreceptors of the turtle retina. Journal of Physiology 373, 443–461.Google Scholar
Kolb, H. & Jones, J. (1982). Light and electron microscopy of the photoreceptors in the retina of the red-eared slider, Pseudemys scripta elegans. Journal of Comparative Neurology 209, 331–338.Google Scholar
Lam, D.M. & Steinman, L. (1971). The uptake of (-3H) aminobutyric acid in the goldfish retina. Proceedings of the National Academy of Sciences of the U.S.A. 68, 2777–2781.Google Scholar
Macdonald, R.L. & Olsen, R.W. (1994). GABAA receptor channels. Annual Review of Neuroscience 17, 569–602.Google Scholar
Marc, R.E., Stell, W.K., Bok, D., & Lam, D.M.K. (1978). GABA-ergic pathways in the goldfish retina. Journal of Comparative Neurology 182, 221–246.Google Scholar
Ohtsuka, T. (1984). Fluorescence from colorless oil droplets: A new criterion for identification of cone photoreceptors. Neuroscience Letters 52, 241–245.Google Scholar
Ohtsuka, T. (1985). Relation of spectral types to oil droplets in cones of turtle retina. Science 229, 874–877.Google Scholar
Parker, I., Gundersen, C.B., & Miledi, R. (1986). Actions of pentobarbital on rat brain receptors expressed in Xenopus Oocytes. Journal of Neuroscience 6, 2290–2297.Google Scholar
Piccolino, M. & Gerschenfeld, H.M. (1978). Activation of a regenerative calcium conductance in turtle cones by peripheral stimulation. Proceedings of the Royal Society B (London) 201, 300–315.Google Scholar
Piccolino, M. & Gerschenfeld, H.M. (1980). Characteristics and ionic processes involved in feedback spikes of turtle cones. Proceedings of the Royal Society B (London) 206, 439–463.Google Scholar
Rabow, L.E., Russek, S., & Farb, D.H. (1995). From ion currents to genomic analysis: Recent advances in GABAA receptor research. Synapse 21, 189–274.Google Scholar
Schwartz, E.A. (1982). Calcium-independent release of GABA from isolated horizontal cells of the toad retina. Journal of Physiology 323, 211–227.Google Scholar
Schwartz, E.A. (1987). Depolarization without calcium can release gamma-aminobutyric acid from retinal neuron. Science 238, 350–355.Google Scholar
Suzuki, S., Tachibana, M., & Kaneko, A. (1990). Effects of glycine and GABA on isolated bipolar cells of the mouse retina. Journal of Physiology 421, 645–662.Google Scholar
Tachibana, M. & Kaneko, A. (1984). G-aminobutyric acid acts at axon terminals of turtle photoreceptors: difference in sensitivity among cell types. Proceedings of the National Academy of Sciences of the U.S.A. 81, 7961–7964.Google Scholar
Verweij, J., Kamermans, M., & Spekreijse, H. (1996). Horizontal cells feed back to cones by shifting the cone calcium-current activation range. Vision Research 36, 3943–3953.Google Scholar
Yazulla, S. (1981). GABA-ergic synapses in the goldfish retina: An autoradiographic study of 3H-muscimol and 3H-GABA binding. Journal of Comparative Neurology 200, 83–93.Google Scholar
Yazulla, S. & Kleinschmidt, J. (1982). Dopamine blocks carrier-mediated release of GABA from retinal horizontal cells. Brain Research 233, 211–215.Google Scholar
Yazulla, S. & Kleinschmidt, J. (1983). Carrier-mediated release of GABA from retinal horizontal cells. Brain Research 263, 63–75.Google Scholar