Hostname: page-component-77c89778f8-sh8wx Total loading time: 0 Render date: 2024-07-17T23:16:47.177Z Has data issue: false hasContentIssue false
  • English
  • Français

The influence of center-surround antagonism on light adaptation in cones in the retina of the turtle

Published online by Cambridge University Press:  02 June 2009

Dwight A. Burkhardt
Dwight A. Burkhardt
Affiliation:
Departments of Psychology and Physiology and Graduate Program of Neuroscience, University of Minnesota, Minneapolis
Get access Rights & Permissions [Opens in a new window]

Abstract

The influence of center-surround antagonism on light adaptation in cone photoreceptors was investigated by intracellular recording from red-sensitive cones in the retina of the turtle, Pseudemys scripta elegans. Test flashes of 0.15-mm diameter were applied at the center of background fields of 0.25-mm or 2.2-mm diameter. Immediately upon expanding the background from 0.25 to 2.2 mm, the membrane potential depolarized by about 1–4 mV. The test flash response was enhanced if the depolarization was primarily due to synaptic feedback from horizontal cells, whereas the response was attenuated if the prolonged depolarization, an intrinsic response of the cone, was the dominant source of the depolarization. After several seconds, however, only the synaptic depolarization was maintained so maintained illumination of the large background field produced an enhancement of the cone's incremental sensitivity. The enhancement was examined in detail in steady-state conditions by obtaining amplitude-intensity measurements for centered test flashes on steady background fields over a large range of intensity. The effect of the large background field at any fixed intensity was fairly well described as a vertical (upward) shift of the amplitude-intensity curve obtained on the small field. This operation constitutes a quasi-subtractive mechanism of light adaptation and might provide a basis for the sort of subtractive mechanisms inferred from psychophysical studies of human vision. The enhancement was quantified by measuring the incremental sensitivity over four decades of background illumination. The magnitude of the enhancement increased with background intensity and then tended to stabilize at higher background intensities. The maximum difference in incremental sensitivity obtained on the large vs. small background field averaged 0.46 log unit (±0.12 s.d.). At higher background intensities, incremental sensitivity conformed to Weber's Law behavior about equally well for flashes applied on either small or large background fields. In sum, the present results provide evidence for an additional mechanism of light adaptation in cone photoreceptors by showing that the incremental light sensitivity, initially set by mechanisms in the outer segment, can be modulated some three-fold by synaptic feedback at the inner segment of the cone.

Keywords

Cone photoreceptorsLight adaptationWeber's LawSynaptic feedback
Type
Research Articles
Information
Visual Neuroscience , Volume 12 , Issue 5 , September 1995 , pp. 877 - 885
Copyright
Copyright © Cambridge University Press 1995

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

REFERENCES

Barnes, S. & Deschene, M.C. (1992). Contribution of Ca and Ca-activated CI channels to regenerative depolarization and membrane bistability of cone photoreceptors. Journal of Neurophysiology 68, 745–755.CrossRefGoogle Scholar
Baylor, D.A. (1987). Photoreceptor signals and vision. Investigative Ophthalmology and Visual Science 28, 34–49.Google ScholarPubMed
Baylor, D.A., Fuortes, M.G.F. & O'Bryan, P.M. (1971). Receptive fields of cones in the retina of the turtle. Journal of Physiology (London) 214, 265–294.CrossRefGoogle ScholarPubMed
Baylor, D.A. & Hodgkin, A.L. (1974). Changes in time scale and sensitivity in turtle photoreceptors. Journal of Physiology (London) 242, 729–753.CrossRefGoogle ScholarPubMed
Burkhardt, D.A. (1974). Sensitization and center-surround antagonism in Necturus retina. Journal of Physiology (London) 236, 593–610.CrossRefGoogle Scholar
Burkhardt, D.A. (1993). Synaptic feedback, depolarization, and color opponency in cone photoreceptors. Visual Neuroscience 10, 981–989.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Burkhardt, D.A., Gottesman, J. & Thoreson, W.B. (1988). Prolonged depolarization in turtle cones evoked by current injection and stimulation of the receptive field surround. Journal of Physiology (London) 407, 329–348.CrossRefGoogle ScholarPubMed
Burkhardt, D.A., Gottesman, J. & Thoreson, W.B. (1989). An eye-cup slice preparation for intracellular recording in vertebrate retinas. Journal of Neuroscience Methods 28, 179–187.CrossRefGoogle Scholar
Burkhardt, D.A., Zhang, S. & Gottesman, J. (1991). Prolonged depolarization in rods in situ. Visual Neuroscience 6, 607–614.CrossRefGoogle ScholarPubMed
Byzov, A.L. (1969). On the role of horizontal cells in the mechanism of retinal adaptation. Neurophysiology 1–2, 160–166.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.CrossRefGoogle ScholarPubMed
Daly, S.J. & Normann, R.A. (1985). Temporal information processing in cones: Effects of light adaptation on temporal summation and modulation. Vision Research 25, 1197–1206.CrossRefGoogle ScholarPubMed
Dowling, J.E. (1987). The Retina: An Approachable Part of the Brain. Cambridge, Massachusetts: Belknap Press.Google Scholar
Fain, G.L. (1989). Cytoplasmic calcium as the messenger for light adaptation in salamander rods. Journal of Physiology (London) 416, 215–243.CrossRefGoogle ScholarPubMed
Fain, G.L. & Matthews, H.R. (1990). Calcium and the mechanism of light adaptation in vertebrate photoreceptors. Trends in Neuroscience 13, 378–384.CrossRefGoogle ScholarPubMed
Hayhoe, M.M. (1990). Spatial interactions and models of adaptation. Vision Research 30, 957–965.CrossRefGoogle ScholarPubMed
Hayhoe, M.M., Levin, M.E. & Koshel, R.J. (1992). Subtractive processes in light adaptation. Vision Research 32, 323–333.CrossRefGoogle ScholarPubMed
Hayhoe, M.M. & Smith, M.V. (1989). The role of spatial filtering in sensitivity regulation. Vision Research 29, 457–469.CrossRefGoogle ScholarPubMed
Itzhaki, A. & Perlman, I. (1987). Light adaptation of red cones and LI-horizontal cells in the turtle retina: Effect of the background spatial pattern. Vision Research 27, 685–696.CrossRefGoogle ScholarPubMed
Kaneko, A. & Tachibana, M. (1986a). Effects of gamma-aminobutyric acid on isolated cone photoreceptors of the turtle retina. Journal of Physiology (London) 373, 463–479.CrossRefGoogle ScholarPubMed
Kaneko, A. & Tachibana, M. (1986b). Blocking effects of cobalt and related ions on the gamma-aminobutyric acid-induced current in turtle retinal cones. Journal of Physiology (London) 373, 463–479.CrossRefGoogle ScholarPubMed
Karwoski, C.J. & Burkhardt, D.A. (1976). Ganglion cell responses of the mudpuppy retina to flashing and moving stimuli. Vision Research 16, 1483–1495.CrossRefGoogle ScholarPubMed
Kleinschmidt, J. & Dowling, J.E. (1975). Intracellular recordings from gecko photoreceptors during light and dark adaptation. Journal of General Physiology 66, 617–648.CrossRefGoogle ScholarPubMed
Normann, R.A. & Anderton, P.J. (1983). The incremental sensitivity curve of turtle cone photoreceptors. Vision Research 23, 1731–1733.CrossRefGoogle ScholarPubMed
Normann, R.A. & Perlman, I. (1979). The effects of background illumination on the photoresponses of red and green cones. Journal of Physiology (London) 286, 491–507.CrossRefGoogle ScholarPubMed
Piccolino, M., Neyton, J. & Gerschenfeld, H.M. (1980). Characteristics and ionic processes involved in the feedback spikes in turtle cones. Proceedings of the Royal Society B 206, 439–469.Google ScholarPubMed
Pugh, E.N. & Lamb, T.D. (1990). Cyclic GMP and calcium: The internal messengers of excitation and adaptation in vertebrate photoreceptors. Vision Research 30, 1923–1948.CrossRefGoogle ScholarPubMed
Purpura, K., Tranchina, D., Kaplan, E. & Shapley, R.M. (1990). Light adaptation in the primate retina: Analysis of changes in gain and dynamics of monkey retinal ganglion cells. Visual Neuroscience 4, 75–93.CrossRefGoogle ScholarPubMed
Shapley, R. & Enroth-Cugell, C. (1984). Visual adaptation and retinal gain control. In Progress in Retinal Research, ed. Osborne, N.N. & Chader, C.T., pp. 263–346. Oxford: Pergamon.Google Scholar
Siminoff, R. (1985). Modeling the effects of a negative feedback circuit from horizontal cells to cones on the impulse response of cones and horizontal cells. Biological Cybernetics 52, 307–313.CrossRefGoogle ScholarPubMed
Tachibana, M. & Kaneko, A. (1984). Gamma-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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Thoreson, W.B. & Burkhardt, D.A. (1991). Ionic influences on the prolonged depolarization of turtle cones in situ. Journal of Neurophysiology 65, 96–110.CrossRefGoogle ScholarPubMed
Tranchina, D., Gordon, J. & Shapley, R.M. (1984). Retinal light adaptation-evidence for a feedback mechanism. Nature 310, 314–316.CrossRefGoogle ScholarPubMed
Tranchina, D. & Peskin, C.S. (1988). Light adaptation in the turtle retina: Embedding a parametric family of linear models in a single nonlinear model. Visual Neuroscience 1, 339–348.CrossRefGoogle Scholar
Walraven, J., Enroth-Cugell, C., Hood, D.C., MacLeod, D.I.A. & Schnapf, J.L. (1990). The control of visual sensitivity: Recep-toral and postreceptoral processes. In Visual Perception: The Neurophysiological Foundations, ed. Spillman, L. & Werner, J.S., pp. 53–102. New York: Academic Press.CrossRefGoogle Scholar
Werblin, F.S. (1974). Control of retinal sensitivity. II. Lateral inter actions at the outer plexiform layer. Journal of General Physiology 63, 62–87.CrossRefGoogle Scholar
Westheimer, G. (1967). Spatial interaction in human cone vision. Journal of Physiology (London) 190, 139–154.CrossRefGoogle ScholarPubMed
Whittle, P. (1994). The psychophysics of contrast-brightness. In Lightness, Brightness and Transparency, ed. Gilchrist, A.L., pp. 35–110. Hillsdale, New Jersey: Lawrence Erlbaum Associates.Google Scholar
Witkovsky, P. & Shi, S.P. (1990). Slow light and dark adaptation of horizontal cells in the Xenopus retina: A role for endogenous dopamine. Visual Neuroscience 5, 405–413.CrossRefGoogle ScholarPubMed
Wu, S.M. (1991). Input-output relations of the feedback synapse between horizontal cells and cones in the tiger salamander retina. Journal of Neurophysiology 65, 1197–1206.CrossRefGoogle ScholarPubMed
Wu, S.M. (1992). Feedback connections and operation of the outer plexiform layer of the retina. Current Opinion in Neurobiology 2, 462–468.CrossRefGoogle ScholarPubMed
Yau, K.-W. (1994). Phototransduction mechanism in retinal rods and cones. Investigative Ophthalmology and Visual Science 35, 9–32.Google ScholarPubMed