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Light adaptation and color opponency of horizontal cells in the turtle retina

Published online by Cambridge University Press:  18 November 2003

GILAD TWIG ,
HANNA LEVY ,
ELITE WEINER  and
IDO PERLMAN
GILAD TWIG
Affiliation:
Department of Physiology and Biophysics, Bruce Rappaport Faculty of Medicine, Technion-Israel Institute of Technology and the Rappaport Institute, Haifa, Israel
HANNA LEVY
Affiliation:
Department of Physiology and Biophysics, Bruce Rappaport Faculty of Medicine, Technion-Israel Institute of Technology and the Rappaport Institute, Haifa, Israel
ELITE WEINER
Affiliation:
Department of Physiology and Biophysics, Bruce Rappaport Faculty of Medicine, Technion-Israel Institute of Technology and the Rappaport Institute, Haifa, Israel
IDO PERLMAN
Affiliation:
Department of Physiology and Biophysics, Bruce Rappaport Faculty of Medicine, Technion-Israel Institute of Technology and the Rappaport Institute, Haifa, Israel
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Abstract

Chromaticity-type (C-type) horizontal cells of the turtle retina receive antagonistic inputs from cones of different spectral types, and therefore their response to background illumination is expected to reflect light adaptation of the cones and the interactions between their antagonistic inputs. Our goal was to study the behavior of C-type horizontal cells during background illumination and to evaluate the role of wavelength in background adaptation. The photoresponses of C-type horizontal cells were recorded intracellularly in the everted eyecup preparation of the turtle Mauremys caspica during chromatic background illuminations. The voltage range of operation was either reduced or augmented, depending upon the wavelengths of the background and of the light stimuli, while the sensitivity to light was decreased by any background. The response–intensity curves were shifted to brighter intensities and became steeper as the background lights were made brighter regardless of wavelength. Comparing the effects of cone iso-luminant backgrounds on the Red/Green C-type horizontal cells indicated that background desensitization in these cells could not solely reflect background adaptation of cones but also depend upon response compression/expansion and changes in synaptic transmission. This leads to wavelength dependency of background adaptation in C-type horizontal cells, that is expressed as increased light sensitivity (smaller threshold elevation) and improved suprathreshold contrast detection when the wavelengths of the background and light stimuli were chosen to exert opponent effects on membrane potential.

Keywords

Light adaptationColor opponencyHorizontal cellsRetinaTurtle
Type
Research Article
Information
Visual Neuroscience , Volume 20 , Issue 4 , July 2003 , pp. 437 - 452
Copyright
2003 Cambridge University Press

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References

REFERENCES

Ammermuller, J., Weiler, R., & Perlman, I. (1995). Short-term effects of dopamine on photoreceptors, luminosity- and chromaticity-horizontal cells in the turtle retina. Visual Neuroscience 12, 403–412.Google Scholar
Ammermuller, J., Itzhaki, A., Weiler, R., & Perlman, I. (1998). UV-sensitive input to horizontal cells in the turtle retina. European Journal of Neuroscience 10, 1544–1552.Google Scholar
Asi, H. & Perlman, I. (1998). Neural interactions between cone photoreceptors and horizontal cells in the turtle (Mauremys caspica) retina. Visual Neuroscience 15, 1–13.Google Scholar
Baylor, D.A. & Hodgkin, A.L. (1973). Detection and resolution of visual stimuli by turtle photoreceptors. Journal of Physiology (London) 234, 163–198.Google Scholar
Baylor, D.A. & Hodgkin, A.L. (1974). Changes in time scale and sensitivity in turtle photoreceptors. Journal of Physiology (London) 242, 729–758.Google Scholar
Burkhardt, D.A. (1993). Synaptic feedback, depolarization, and color opponency in cone photoreceptors. Visual Neuroscience 10, 981–989.Google Scholar
Burkhardt, D.A. (1994). Light adaptation and photopigment bleaching in cone photoreceptors in situ in the retina of the turtle. Journal of Neuroscience 14, 1091–1105.Google Scholar
Burkhardt, D.A. (1995). The influence of center-surround antagonism on light adaptation in cones in the retina of the turtle. Visual Neuroscience 12, 877–885.Google Scholar
Copenhagen, D.R. & Green, D.G. (1987). Spatial spread of adaptation within the cone network of turtle retina. Journal of Physiology (London) 393, 763–776.Google Scholar
Djamgoz, M.B.A. (1984). Electrophysiological characterization of the spectral sensitivities of horizontal cells in the cyprinid fish retina. Vision Research 24, 1677–1687.Google Scholar
Djamgoz, M.B.A., Downing, J.E.C., Kirsch, M., Prince, D.J., & Wagner, H.-J. (1988). Plasticity of cone horizontal cell functioning in cyprinid fish retina: Effects of background illumination of moderate intensity. Journal of Neurocytology 17, 701–710.Google Scholar
D'zmura, M. & Singer, B. (1999). Contrast gain control. In Color Vision: From Molecular Genetics to Perception, ed. Gegenfurther, K. & Sharpe, L.T., pp. 369–385. Cambridge, UK: Cambridge University Press.
Eskew, R.T., Stromeyer, C.F., & Kronauer, R.E. (1994). Temporal properties of the red–green chromatic mechanism. Vision Research 34, 3127–3137.Google Scholar
Fahrenfort, I., Habets, R.L., Spekreijse, H., & Kamermans, M. (1999). Intrinsic cone adaptation modulates feedback efficiency from horizontal cells to cones. Journal of General Physiology 114, 511–524.Google Scholar
Fain, G.L. (1975). Interactions of rod and cone signals in the mudpuppy retina. Journal of Physiology (London) 252, 735–769.Google Scholar
Finkelstein, M.A. & Hood, D.C. (1982). Opponent color cells can influence detection of small, brief lights. Vision Research 22, 89–95.Google Scholar
Fuortes, M.G.F. & Simon, E.J. (1974). Interactions leading to horizontal cell responses in the turtle retina. Journal of Physiology (London) 240, 177–198.Google Scholar
Fuortes, M.G.F., Schwartz, E.A., & Simon, E.J. (1973). Colour dependence of cone responses in the turtle retina. Journal of Physiology (London) 234, 199–216.Google Scholar
Itzhaki, A. & Perlman, I. (1984). Light adaptation in luminosity horizontal cells in the turtle retina: Role of cellular coupling. Vision Research 24, 1119–1126.Google Scholar
Itzhaki, A. & Perlman, I. (1987). Light adaptation of red cones and L1-horizontal cells in the turtle retina: Effects of the background spatial pattern. Vision Research 27, 685–696.Google Scholar
Itzhaki, A., Malik, S., & Perlman, I. (1992). The spectral properties of short wavelength (blue) cones in the turtle retina. Visual Neuroscience 9, 235–241.Google Scholar
Kamermans, M., van Dick, B.W., & Spekreijse, H. (1991). Color opponency in the cone-driven horizontal cells in carp retina. Aspecific pathways between cones and horizontal cells. Journal of General Physiology 97, 819–843.Google Scholar
Kim, H.G. & Miller, R.F. (1992). Physiological and morphological correlations of horizontal cells in the mudppupy retina. Journal of Neurophysiology 67, 829–840.Google Scholar
Lamb, T.D. (1976). Spatial properties of horizontal cell responses in the turtle retina. Journal of Physiology (London) 263, 239–255.Google Scholar
Malchow, R.P. & Yazulla, S. (1988). Light adaptation of rod and cone luminosity horizontal cells of the retina of the goldfish. Brain Research 443, 222–230.Google Scholar
Millar, T.J. & Anderton, P.J. (1991). Effects of excitatory amino acids and their antagonists on the light response of luminosity and color-opponent horizontal cells in the turtle (Pseudemys scripta elegans) retina. Visual Neuroscience 6, 135–149.Google Scholar
Mullen, K.T. (1987). Spatial Influences on colour opponent contributions to pattern detection. Vision Research 27, 829–839.Google Scholar
Myhr, K.L., Dong, C.J., & McReynolds, J.S. (1994). Cones contribute to light-evoked, dopamine-mediated uncoupling of horizontal cells in the mudpuppy retina. Journal of Neurophysiology 72, 56–62.Google Scholar
Naka, K.I. & Rushton, W.A.H. (1966). S-potentials from colour units in the retina of fish (Cyprinidae). Journal of Physiology (London) 185, 536–555.Google Scholar
Normann, R.A. & Perlman, I. (1979a). The effects of background illumination on the photoresponses of red and green cones. Journal of Physiology (London) 286, 491–507.Google Scholar
Normann, R.A. & Perlman, I. (1979b). Signal transmission from red cones to horizontal cells in turtle retina. Journal of Physiology (London) 286, 509–524.Google Scholar
Normann, R.A. & Perlman, I. (1979c). Evaluating sensitivity changing mechansims in light-adapted photoreceptors. Vision Research 19, 391–394.Google Scholar
Normann, R.A. & Anderton, P.J. (1983). The incremental sensitivity curve of turtle cone photoreceptors. Vision Research 23, 1731–1733.Google Scholar
Normann, R.A. & Perlman, I. (1990). Background and bleaching adaptation in luminosity type horizontal cells in the isolated turtle retina. Journal of Physiology (London) 421, 321–341.Google Scholar
Normann, R.A., Perlman, I., & Daly, S.J. (1986). The effects of continuous superfusion of L-aspartate and L-glutamate on horizontal cells of the turtle retina. Vision Research 26, 259–268.Google Scholar
Perlman, I. & Normann, R.A. (1979). Short-wavelength input to luminosity-type horizontal cells in the turtle retina. Vision Research 19, 903–906.Google Scholar
Perlman, I. & Ammermuller, J. (1994). The receptive field size of L1 horizontal cells in the turtle retina: The effects of dopamine and background light. Journal of Neurophysiology 72, 2786–2795.Google Scholar
Perlman, I. & Normann, R.A. (1998). Light adaptation and sensitivity controlling mechanisms in vertebrate photoreceptors. Progress in Retinal and Eye Research 17, 523–563.Google Scholar
Perlman, I., Normann, R.A., Itzhaki, A., & Daly, S.J. (1985). Chromatic and spatial information processing by red cones and L-type horizontal cells in the turtle retina. Vision Research 25, 543–549.Google Scholar
Perlman, I., Itzhaki, A., Malik, S., & Alpern, M. (1994). The action spectra of cone photoreceptors in the turtle (Mauremys caspica) retina. Visual Neuroscience 11, 243–252.Google Scholar
Piccolino, M. (1995). The feedback synapse from horizontal cells to cone photoreceptors in the vertebrate retina. Progress in Retinal and Eye Research 14, 141–196.Google Scholar
Piccolino, M., Neyton, J., & Gerschnefeld, H.M. (1981). Center-surround antagonistic organization in small-field luminosity horizontal cells of turtle retina. Journal of Neurophysiology 45, 363–375.Google Scholar
Schneeweis, D.M. & Green, D.G. (1995). Spectral properties of turtle cones. Visual Neuroscience 12, 333–344.Google Scholar
Stone, S., Witkovsky, P., & Schutte, M. (1990). A chromatic horizontal cell in the Xenopus retina: Intracellular staining and synaptic pharmacology. Journal of Neurophysiology 64, 1683–1694.Google Scholar
Stromeyer, C.F., Lee, J., & Eskew, R.T. (1992). Peripheral chromatic sensitivity for flashes: A post-receptoral red–green asymmetry. Vision Research 32, 1865–1873.Google Scholar
Thoreson, W.B. & Burkhardt, D.A. (1990). Effects of synaptic blocking agents on the depolarizing responses of turtle cones evoked by surround illumination. Visual Neuroscience 5, 571–583.Google Scholar
Tranchina, D., Sneyd, J., & Cadenas, I.D. (1991). Light adaptation in turtle cones. Testing and analysis of a model for phototransduction. Biophysical Journal 60, 217–237.Google Scholar
Twig, G., Levy, H., & Perlman, I. (2001). Turtle C-type horizontal cells act as push–pull devices. Visual Neuroscience 18, 893–900.Google Scholar
Twig, G., Levy, H., & Perlman, I. (2002). Spatial-chromatic interactions in C-type horizontal cells of the turtle (Mauremys caspica) retina. Visual Neuroscience 19, 71–84.Google Scholar
Valeton, J.M. & Van Norren, D. (1983). Light adaptation of primate cones: An analysis based on extracellular data. Vision Research 23, 1539–1547.Google Scholar
van de Grind, W.A., Lankheet, M.J.M., van Wezel, R.J.A., Rowe, M.H., & Hulleman, J. (1996). Gain control and hyperpolarization level in cat horizontal cells as a function of light and dark adaptation. Vision Research 36, 3969–3985.Google Scholar
Ventura, D.F., DeSouza, J.M., Devoe, R.D., & Zana, Y. (1999). UV responses in the retina of the turtle. Visual Neuroscience 16, 191–204.Google Scholar
Ventura, D.F., Zana, Y., DeSouza, J.M., & Devoe, R.D. (2001). Ultraviolet colour opponency in the turtle retina. Journal of Experimental Biology 204, 2527–2534.Google Scholar
Verweij, J., Kamermans, M., & Spekreijse, H. (1996). Horizontal cells feedback to cones by shifting the cone calcium-current activation range. Vision Research 36, 3943–3953.Google Scholar
Vigh, J. & Witkovsky, P. (1999). Sub-millimolar cobalt selectively inhibits the receptive-field surround of retinal neurons. Visual Neuroscience 16, 159–168.Google Scholar
Wagner, H.-J. & Djamgoz, M.B.A. (1993). Spinules: A case for retinal synaptic plasticity. Trends in Neuroscience 16, 210–206.Google Scholar
Weiler, R. & Wagner, H.-J. (1984). Light-dependent change of cone-horizontal cell interactions in carp retina. Brain Research 298, 1–9.Google Scholar
Witkovsky, P., Gabriel, R., Krizaj, D., & Akopian, A. (1995). Feedback from luminosity horizontal cells mediates depolarizing responses of chromaticity horizontal cells in Xenopus retina. Proceedings of the National Academy of Sciences of the U.S.A. 92, 3556–3560.Google Scholar
Yang, X.L., Fan, T.X., & Shen, W. (1994). Effects of prolonged darkness on light responsiveness and spectral sensitivity of cone horizontal cells in carp retina in vivo. Journal of Neuroscience 14, 326–334.Google Scholar
Yazulla, S. (1976). Cone input to horizontal cells in the turtle retina. Vision Research 16, 727–735.Google Scholar