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. 1991 Jul;60(1):217–237. doi: 10.1016/S0006-3495(91)82045-8

Light adaptation in turtle cones. Testing and analysis of a model for phototransduction.

D Tranchina 1, J Sneyd 1, I D Cadenas 1
PMCID: PMC1260053  PMID: 1653050

Abstract

Light adaptation in cones was characterized by measuring the changes in temporal frequency responses to sinusoidal modulation of light around various mean levels spanning a range of four log units. We have shown previously that some aspects of cone adaptation behavior can be accounted for by a biochemical kinetic model for phototransduction in which adaptation is mediated largely by a sigmoidal dependence of guanylate cyclase activity on the concentration of free cytoplasmic Ca2+, ([Ca2+]i) (Sneyd and Tranchina, 1989). Here we extend the model by incorporating electrogenic Na+/K+ exchange, and the model is put to further tests by simulating experiments in the literature. It accounts for (a) speeding up of the impulse response, transition from monophasic to biphasic waveform, and improvement in contrast sensitivity with increasing background light level, I0; (b) linearity of the response to moderate modulations around I0; (c) shift of the intensity-response function (linear vs. log coordinates) with change in I0 (Normann and Perlman, 1979); the dark-adapted curve adheres closely to the Naka-Rushton equation; (d) steepening of the sensitivity vs. I0 function with [Ca2+]i fixed at its dark level, [Ca2+]i dark; (Matthews et al., 1988, 1990); (e) steepening of the steady-state intensity-response function when [Ca2+]i is held fixed at its dark level (Matthews et al., 1988; 1990); (f) shifting of a steep template saturation curve for normalized photocurrent vs. light-step intensity when the response is measured at fixed times and [Ca2+]i is held fixed at [Ca2+]i dark (Nakatani and Yau, 1988). Furthermore, the predicted dependence of guanylate cyclase activity on [Ca2+] closely matches a cooperative inhibition equation suggested by the experimental results of Koch and Stryer (1988) on cyclase activity in bovine rods. Finally, the model predicts that some changes in response kinetics with background light will still be present, even when [Ca2+]i is held fixed at [Ca2]i dark.

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Selected References

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  1. Attwell D., Werblin F. S., Wilson M. The properties of single cones isolated from the tiger salamander retina. J Physiol. 1982 Jul;328:259–283. doi: 10.1113/jphysiol.1982.sp014263. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Barkdoll A. E., 3rd, Pugh E. N., Jr, Sitaramayya A. Calcium dependence of the activation and inactivation kinetics of the light-activated phosphodiesterase of retinal rods. J Gen Physiol. 1989 Jun;93(6):1091–1108. doi: 10.1085/jgp.93.6.1091. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Barnes S., Hille B. Ionic channels of the inner segment of tiger salamander cone photoreceptors. J Gen Physiol. 1989 Oct;94(4):719–743. doi: 10.1085/jgp.94.4.719. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Baylor D. A., Fuortes M. G., O'Bryan P. M. Receptive fields of cones in the retina of the turtle. J Physiol. 1971 Apr;214(2):265–294. doi: 10.1113/jphysiol.1971.sp009432. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Baylor D. A., Hodgkin A. L. Changes in time scale and sensitivity in turtle photoreceptors. J Physiol. 1974 Nov;242(3):729–758. doi: 10.1113/jphysiol.1974.sp010732. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Baylor D. A., Hodgkin A. L. Detection and resolution of visual stimuli by turtle photoreceptors. J Physiol. 1973 Oct;234(1):163–198. doi: 10.1113/jphysiol.1973.sp010340. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Baylor D. A., Hodgkin A. L., Lamb T. D. Reconstruction of the electrical responses of turtle cones to flashes and steps of light. J Physiol. 1974 Nov;242(3):759–791. doi: 10.1113/jphysiol.1974.sp010733. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Baylor D. A., Hodgkin A. L., Lamb T. D. The electrical response of turtle cones to flashes and steps of light. J Physiol. 1974 Nov;242(3):685–727. doi: 10.1113/jphysiol.1974.sp010731. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Baylor D. A., Nunn B. J., Schnapf J. L. The photocurrent, noise and spectral sensitivity of rods of the monkey Macaca fascicularis. J Physiol. 1984 Dec;357:575–607. doi: 10.1113/jphysiol.1984.sp015518. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Baylor D. A. Photoreceptor signals and vision. Proctor lecture. Invest Ophthalmol Vis Sci. 1987 Jan;28(1):34–49. [PubMed] [Google Scholar]
  11. Burkhardt D. A., Gottesman J., Thoreson W. B. Prolonged depolarization in turtle cones evoked by current injection and stimulation of the receptive field surround. J Physiol. 1988 Dec;407:329–348. doi: 10.1113/jphysiol.1988.sp017418. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Cervetto L., Lagnado L., Perry R. J., Robinson D. W., McNaughton P. A. Extrusion of calcium from rod outer segments is driven by both sodium and potassium gradients. Nature. 1989 Feb 23;337(6209):740–743. doi: 10.1038/337740a0. [DOI] [PubMed] [Google Scholar]
  13. Chappell R. L., Naka K., Sakuranaga M. Dynamics of turtle horizontal cell response. J Gen Physiol. 1985 Sep;86(3):423–453. doi: 10.1085/jgp.86.3.423. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Cobbs W. H., Barkdoll A. E., 3rd, Pugh E. N., Jr Cyclic GMP increases photocurrent and light sensitivity of retinal cones. Nature. 1985 Sep 5;317(6032):64–66. doi: 10.1038/317064a0. [DOI] [PubMed] [Google Scholar]
  15. Copenhagen D. R., Green D. G. Spatial spread of adaptation within the cone network of turtle retina. J Physiol. 1987 Dec;393:763–776. doi: 10.1113/jphysiol.1987.sp016852. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Daly S. J., Normann R. A. Temporal information processing in cones: effects of light adaptation on temporal summation and modulation. Vision Res. 1985;25(9):1197–1206. doi: 10.1016/0042-6989(85)90034-3. [DOI] [PubMed] [Google Scholar]
  17. Dawis S. M., Graeff R. M., Heyman R. A., Walseth T. F., Goldberg N. D. Regulation of cyclic GMP metabolism in toad photoreceptors. Definition of the metabolic events subserving photoexcited and attenuated states. J Biol Chem. 1988 Jun 25;263(18):8771–8785. [PubMed] [Google Scholar]
  18. Detwiler P. B., Hodgkin A. L. Electrical coupling between cones in turtle retina. J Physiol. 1979 Jun;291:75–100. doi: 10.1113/jphysiol.1979.sp012801. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Fain G. L., Matthews H. R. Calcium and the mechanism of light adaptation in vertebrate photoreceptors. Trends Neurosci. 1990 Sep;13(9):378–384. doi: 10.1016/0166-2236(90)90023-4. [DOI] [PubMed] [Google Scholar]
  20. Forti S., Menini A., Rispoli G., Torre V. Kinetics of phototransduction in retinal rods of the newt Triturus cristatus. J Physiol. 1989 Dec;419:265–295. doi: 10.1113/jphysiol.1989.sp017873. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Goldberg N. D., Ames A. A., 3rd, Gander J. E., Walseth T. F. Magnitude of increase in retinal cGMP metabolic flux determined by 18O incorporation into nucleotide alpha-phosphoryls corresponds with intensity of photic stimulation. J Biol Chem. 1983 Aug 10;258(15):9213–9219. [PubMed] [Google Scholar]
  22. Haynes L., Yau K. W. Cyclic GMP-sensitive conductance in outer segment membrane of catfish cones. Nature. 1985 Sep 5;317(6032):61–64. doi: 10.1038/317061a0. [DOI] [PubMed] [Google Scholar]
  23. Hodgkin A. L., McNaughton P. A., Nunn B. J. Measurement of sodium-calcium exchange in salamander rods. J Physiol. 1987 Oct;391:347–370. doi: 10.1113/jphysiol.1987.sp016742. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Hodgkin A. L., Nunn B. J. Control of light-sensitive current in salamander rods. J Physiol. 1988 Sep;403:439–471. doi: 10.1113/jphysiol.1988.sp017258. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Itzhaki A., Perlman I. Light adaptation of red cones and L1-horizontal cells in the turtle retina: effect of the background spatial pattern. Vision Res. 1987;27(5):685–696. doi: 10.1016/0042-6989(87)90065-4. [DOI] [PubMed] [Google Scholar]
  26. Kawamura S., Murakami M. In situ cGMP phosphodiesterase and photoreceptor potential in gecko retina. J Gen Physiol. 1986 May;87(5):737–759. doi: 10.1085/jgp.87.5.737. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Kawamura S., Murakami M. Regulation of cGMP levels by guanylate cyclase in truncated frog rod outer segments. J Gen Physiol. 1989 Oct;94(4):649–668. doi: 10.1085/jgp.94.4.649. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Koch K. W., Stryer L. Highly cooperative feedback control of retinal rod guanylate cyclase by calcium ions. Nature. 1988 Jul 7;334(6177):64–66. doi: 10.1038/334064a0. [DOI] [PubMed] [Google Scholar]
  29. Lagnado L., Cervetto L., McNaughton P. A. Ion transport by the Na-Ca exchange in isolated rod outer segments. Proc Natl Acad Sci U S A. 1988 Jun;85(12):4548–4552. doi: 10.1073/pnas.85.12.4548. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Lamb T. D., McNaughton P. A., Yau K. W. Spatial spread of activation and background desensitization in toad rod outer segments. J Physiol. 1981;319:463–496. doi: 10.1113/jphysiol.1981.sp013921. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Lamb T. D., Simon E. J. Analysis of electrical noise in turtle cones. J Physiol. 1977 Nov;272(2):435–468. doi: 10.1113/jphysiol.1977.sp012053. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Lamb T. D. Sources of noise in photoreceptor transduction. J Opt Soc Am A. 1987 Dec;4(12):2295–2300. doi: 10.1364/josaa.4.002295. [DOI] [PubMed] [Google Scholar]
  33. Liebman P. A., Parker K. R., Dratz E. A. The molecular mechanism of visual excitation and its relation to the structure and composition of the rod outer segment. Annu Rev Physiol. 1987;49:765–791. doi: 10.1146/annurev.ph.49.030187.004001. [DOI] [PubMed] [Google Scholar]
  34. Lolley R. N., Racz E. Calcium modulation of cyclic GMP synthesis in rat visual cells. Vision Res. 1982;22(12):1481–1486. doi: 10.1016/0042-6989(82)90213-9. [DOI] [PubMed] [Google Scholar]
  35. Maricq A. V., Korenbrot J. I. Inward rectification in the inner segment of single retinal cone photoreceptors. J Neurophysiol. 1990 Dec;64(6):1917–1928. doi: 10.1152/jn.1990.64.6.1917. [DOI] [PubMed] [Google Scholar]
  36. Matthews H. R., Fain G. L., Murphy R. L., Lamb T. D. Light adaptation in cone photoreceptors of the salamander: a role for cytoplasmic calcium. J Physiol. 1990 Jan;420:447–469. doi: 10.1113/jphysiol.1990.sp017922. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Matthews H. R., Murphy R. L., Fain G. L., Lamb T. D. Photoreceptor light adaptation is mediated by cytoplasmic calcium concentration. Nature. 1988 Jul 7;334(6177):67–69. doi: 10.1038/334067a0. [DOI] [PubMed] [Google Scholar]
  38. Naka K. I., Itoh M. A., Chappell R. L. Dynamics of turtle cones. J Gen Physiol. 1987 Feb;89(2):321–337. doi: 10.1085/jgp.89.2.321. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Nakatani K., Yau K. W. Calcium and light adaptation in retinal rods and cones. Nature. 1988 Jul 7;334(6177):69–71. doi: 10.1038/334069a0. [DOI] [PubMed] [Google Scholar]
  40. Nicol G. D., Bownds M. D. Calcium regulates some, but not all, aspects of light adaptation in rod photoreceptors. J Gen Physiol. 1989 Aug;94(2):233–259. doi: 10.1085/jgp.94.2.233. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Normann R. A., Perlman I. The effects of background illumination on the photoresponses of red and green cones. J Physiol. 1979 Jan;286:491–507. doi: 10.1113/jphysiol.1979.sp012633. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. O'Bryan P. M. Properties of the depolarizing synaptic potential evoked by peripheral illumination in cones of the turtle retina. J Physiol. 1973 Nov;235(1):207–223. doi: 10.1113/jphysiol.1973.sp010385. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Pugh E. N., Jr, Cobbs W. H. Visual transduction in vertebrate rods and cones: a tale of two transmitters, calcium and cyclic GMP. Vision Res. 1986;26(10):1613–1643. doi: 10.1016/0042-6989(86)90051-9. [DOI] [PubMed] [Google Scholar]
  44. Pugh E. N., Jr, Lamb T. D. Cyclic GMP and calcium: the internal messengers of excitation and adaptation in vertebrate photoreceptors. Vision Res. 1990;30(12):1923–1948. doi: 10.1016/0042-6989(90)90013-b. [DOI] [PubMed] [Google Scholar]
  45. Purpura K., Tranchina D., Kaplan E., Shapley R. M. Light adaptation in the primate retina: analysis of changes in gain and dynamics of monkey retinal ganglion cells. Vis Neurosci. 1990 Jan;4(1):75–93. doi: 10.1017/s0952523800002789. [DOI] [PubMed] [Google Scholar]
  46. Ratto G. M., Payne R., Owen W. G., Tsien R. Y. The concentration of cytosolic free calcium in vertebrate rod outer segments measured with fura-2. J Neurosci. 1988 Sep;8(9):3240–3246. doi: 10.1523/JNEUROSCI.08-09-03240.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Schnapf J. L., Nunn B. J., Meister M., Baylor D. A. Visual transduction in cones of the monkey Macaca fascicularis. J Physiol. 1990 Aug;427:681–713. doi: 10.1113/jphysiol.1990.sp018193. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Sitaramayya A., Harkness J., Parkes J. H., Gonzalez-Oliva C., Liebman P. A. Kinetic studies suggest that light-activated cyclic GMP phosphodiesterase is a complex with G-protein subunits. Biochemistry. 1986 Feb 11;25(3):651–656. doi: 10.1021/bi00351a021. [DOI] [PubMed] [Google Scholar]
  49. Sneyd J., Tranchina D. Phototransduction in cones: an inverse problem in enzyme kinetics. Bull Math Biol. 1989;51(6):749–784. doi: 10.1007/BF02459659. [DOI] [PubMed] [Google Scholar]
  50. Stryer L. Cyclic GMP cascade of vision. Annu Rev Neurosci. 1986;9:87–119. doi: 10.1146/annurev.ne.09.030186.000511. [DOI] [PubMed] [Google Scholar]
  51. Torre V. The contribution of the electrogenic sodium-potassium pump to the electrical activity of toad rods. J Physiol. 1982 Dec;333:315–341. doi: 10.1113/jphysiol.1982.sp014456. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Tranchina D., Gordon J., Shapley R. M. Retinal light adaptation--evidence for a feedback mechanism. 1984 Jul 26-Aug 1Nature. 310(5975):314–316. doi: 10.1038/310314a0. [DOI] [PubMed] [Google Scholar]
  53. Tranchina D., Gordon J., Shapley R. Spatial and temporal properties of luminosity horizontal cells in the turtle retina. J Gen Physiol. 1983 Nov;82(5):573–598. doi: 10.1085/jgp.82.5.573. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Tranchina D., Gordon J., Shapley R., Toyoda J. Linear information processing in the retina: a study of horizontal cell responses. Proc Natl Acad Sci U S A. 1981 Oct;78(10):6540–6542. doi: 10.1073/pnas.78.10.6540. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Tranchina D., Peskin C. S. Light adaptation in the turtle retina: embedding a parametric family of linear models in a single nonlinear model. Vis Neurosci. 1988;1(4):339–348. doi: 10.1017/s0952523800004119. [DOI] [PubMed] [Google Scholar]
  56. Wessling-Resnick M., Johnson G. L. Allosteric behavior in transducin activation mediated by rhodopsin. Initial rate analysis of guanine nucleotide exchange. J Biol Chem. 1987 Mar 15;262(8):3697–3705. [PubMed] [Google Scholar]
  57. Yau K. W., Baylor D. A. Cyclic GMP-activated conductance of retinal photoreceptor cells. Annu Rev Neurosci. 1989;12:289–327. doi: 10.1146/annurev.ne.12.030189.001445. [DOI] [PubMed] [Google Scholar]
  58. Yau K. W., Nakatani K. Electrogenic Na-Ca exchange in retinal rod outer segment. Nature. 1984 Oct 18;311(5987):661–663. doi: 10.1038/311661a0. [DOI] [PubMed] [Google Scholar]
  59. Yau K. W., Nakatani K. Light-induced reduction of cytoplasmic free calcium in retinal rod outer segment. Nature. 1985 Feb 14;313(6003):579–582. doi: 10.1038/313579a0. [DOI] [PubMed] [Google Scholar]

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