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. 1990 Apr 1;95(4):733–753. doi: 10.1085/jgp.95.4.733

Weber and noise adaptation in the retina of the toad Bufo marinus

PMCID: PMC2216330  PMID: 2110969

Abstract

Responses to flashes and steps of light were recorded intracellularly from rods and horizontal cells, and extracellularly from ganglion cells, in toad eyecups which were either dark adapted or exposed to various levels of background light. The average background intensities needed to depress the dark-adapted flash sensitivity by half in the three cell types, determined under identical conditions, were 0.9 Rh*s- 1 (rods), 0.8 Rh*s-1 (horizontal cells), and 0.17 Rh*s-1 (ganglion cells), where Rh* denotes one isomerization per rod. Thus, there is a range (approximately 0.7 log units) of weak backgrounds where the sensitivity (response amplitude/Rh*) of rods is not significantly affected, but where that of ganglion cells (1/threshold) is substantially reduced, which implies that the gain of the transmission from rods to the ganglion cell output is decreased. In this range, the ganglion cell threshold rises approximately as the square root of background intensity (i.e. in proportion to the quantal noise from the background), while the maintained rate of discharge stays constant. The threshold response of the cell will then signal light deviations (from a mean level) of constant statistical significance. We propose that this type of ganglion cell desensitization under dim backgrounds is due to a post-receptoral gain control driven by quantal fluctuations, and term it noise adaptation in contrast to the Weber adaptation (desensitization proportional to the mean background intensity) of rods, horizontal cells, and ganglion cells at higher background intensities.

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Selected References

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  1. Aho A. C., Donner K., Hydén C., Reuter T., Orlov OYu Retinal noise, the performance of retinal ganglion cells, and visual sensitivity in the dark-adapted frog. J Opt Soc Am A. 1987 Dec;4(12):2321–2329. doi: 10.1364/josaa.4.002321. [DOI] [PubMed] [Google Scholar]
  2. Ashmore J. F., Falk G. An analysis of voltage noise in rod bipolar cells of the dogfish retina. J Physiol. 1982 Nov;332:273–297. doi: 10.1113/jphysiol.1982.sp014413. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. BARLOW H. B. Retinal noise and absolute threshold. J Opt Soc Am. 1956 Aug;46(8):634–639. doi: 10.1364/josa.46.000634. [DOI] [PubMed] [Google Scholar]
  4. BARLOW H. B. Temporal and spatial summation in human vision at different background intensities. J Physiol. 1958 Apr 30;141(2):337–350. doi: 10.1113/jphysiol.1958.sp005978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Barlow H. B., Levick W. R. Threshold setting by the surround of cat retinal ganglion cells. J Physiol. 1976 Aug;259(3):737–757. doi: 10.1113/jphysiol.1976.sp011492. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Baylor D. A., Fettiplace R. Kinetics of synaptic transfer from receptors to ganglion cells in turtle retina. J Physiol. 1977 Oct;271(2):425–448. doi: 10.1113/jphysiol.1977.sp012007. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. 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]
  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., Lamb T. D., Yau K. W. Responses of retinal rods to single photons. J Physiol. 1979 Mar;288:613–634. [PMC free article] [PubMed] [Google Scholar]
  10. Baylor D. A., Lamb T. D., Yau K. W. The membrane current of single rod outer segments. J Physiol. 1979 Mar;288:589–611. [PMC free article] [PubMed] [Google Scholar]
  11. Baylor D. A., Matthews G., Yau K. W. Two components of electrical dark noise in toad retinal rod outer segments. J Physiol. 1980 Dec;309:591–621. doi: 10.1113/jphysiol.1980.sp013529. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Baylor D. A. Photoreceptor signals and vision. Proctor lecture. Invest Ophthalmol Vis Sci. 1987 Jan;28(1):34–49. [PubMed] [Google Scholar]
  13. Byzov A. L., Kusnezova L. P. On the mechanisms of visual adaptation. Vision Res. 1971;Suppl 3:51–63. doi: 10.1016/0042-6989(71)90030-7. [DOI] [PubMed] [Google Scholar]
  14. Bäckström A. C., Reuter T. Receptive field organization of ganglion cells in the frog retina: contributions from cones, green rods and red rods. J Physiol. 1975 Mar;246(1):79–107. doi: 10.1113/jphysiol.1975.sp010881. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Copenhagen D. R., Donner K., Reuter T. Ganglion cell performance at absolute threshold in toad retina: effects of dark events in rods. J Physiol. 1987 Dec;393:667–680. doi: 10.1113/jphysiol.1987.sp016847. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Copenhagen D. R., Green D. G. The absence of spread of adaptation between rod photoreceptors in turtle retina. J Physiol. 1985 Dec;369:161–181. doi: 10.1113/jphysiol.1985.sp015894. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Copenhagen D. R., Hemilä S., Reuter T. Signal transmission through the dark-adapted retina of the toad (Bufo marinus). Gain, convergence, and signal/noise. J Gen Physiol. 1990 Apr;95(4):717–732. doi: 10.1085/jgp.95.4.717. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Copenhagen D. R., Owen W. G. Functional characteristics of lateral interactions between rods in the retina of the snapping turtle. J Physiol. 1976 Jul;259(2):251–282. doi: 10.1113/jphysiol.1976.sp011465. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Donner K. O., Hemilä S. Excitation and adaptation in the vertebrate rod photoreceptor. Med Biol. 1978 Apr;56(2):52–63. [PubMed] [Google Scholar]
  20. Donner K. Adaptation-related changes in the spatial and temporal summation of frog retinal ganglion cells. Acta Physiol Scand. 1987 Dec;131(4):479–487. doi: 10.1111/j.1748-1716.1987.tb08267.x. [DOI] [PubMed] [Google Scholar]
  21. Donner K., Grönholm M. L. Center and surround excitation in the receptive fields of frog retinal ganglion cells. Vision Res. 1984;24(12):1807–1819. doi: 10.1016/0042-6989(84)90012-9. [DOI] [PubMed] [Google Scholar]
  22. Donner K. Receptive fields of frog retinal ganglion cells: response formation and light-dark-adaptation. J Physiol. 1981;319:131–142. doi: 10.1113/jphysiol.1981.sp013896. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Dowling J. E., Ripps H. The proximal negative response and visual adaptation in the skate retina. J Gen Physiol. 1977 Jan;69(1):57–74. doi: 10.1085/jgp.69.1.57. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Dowling J. E. The site of visual adaptation. Science. 1967 Jan 20;155(3760):273–279. doi: 10.1126/science.155.3760.273. [DOI] [PubMed] [Google Scholar]
  25. Enroth-Cugell C., Shapley R. M. Adaptation and dynamics of cat retinal ganglion cells. J Physiol. 1973 Sep;233(2):271–309. doi: 10.1113/jphysiol.1973.sp010308. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Ewert J. P., Hock F. Movement-sensitive neurones in the toad's retina. Exp Brain Res. 1972;16(1):41–59. doi: 10.1007/BF00233373. [DOI] [PubMed] [Google Scholar]
  27. Fain G. L. Quantum sensitivity of rods in the toad retina. Science. 1975 Mar 7;187(4179):838–841. doi: 10.1126/science.1114328. [DOI] [PubMed] [Google Scholar]
  28. Fain G. L. Sensitivity of toad rods: Dependence on wave-length and background illumination. J Physiol. 1976 Sep;261(1):71–101. doi: 10.1113/jphysiol.1976.sp011549. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Green D. G., Dowling J. E., Siegel I. M., Ripps H. Retinal mechanisms of visual adaptation in the skate. J Gen Physiol. 1975 Apr;65(4):483–502. doi: 10.1085/jgp.65.4.483. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Green D. G., Powers M. K. Mechanisms of light adaptation in rat retina. Vision Res. 1982;22(2):209–216. doi: 10.1016/0042-6989(82)90120-1. [DOI] [PubMed] [Google Scholar]
  31. Greenblatt R. E. Adapting lights and lowered extracellular free calcium desensitize toad photoreceptors by differing mechanisms. J Physiol. 1983 Mar;336:579–605. doi: 10.1113/jphysiol.1983.sp014599. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Hemilä S., Reuter T. Longitudinal spread of adaptation in the rods of the frog's retina. J Physiol. 1981 Jan;310:501–528. doi: 10.1113/jphysiol.1981.sp013564. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. 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]
  34. Leeper H. F., Normann R. A., Copenhagen D. R. Evidence for passive electrotonic interactions in red rods of toad retina. Nature. 1978 Sep 21;275(5677):234–236. doi: 10.1038/275234b0. [DOI] [PubMed] [Google Scholar]
  35. Leibovic K. N., Dowling J. E., Kim Y. Y. Background and bleaching equivalence in steady-state adaptation of vertebrate rods. J Neurosci. 1987 Apr;7(4):1056–1063. doi: 10.1523/JNEUROSCI.07-04-01056.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. MATURANA H. R., LETTVIN J. Y., MCCULLOCH W. S., PITTS W. H. Anatomy and physiology of vision in the frog (Rana pipiens). J Gen Physiol. 1960 Jul;43(6):129–175. doi: 10.1085/jgp.43.6.129. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Reuter T., Donner K., Copenhagen D. R. Does the random distribution of discrete photoreceptor events limit the sensitivity of the retina? Neurosci Res Suppl. 1986;4:S163–S180. doi: 10.1016/0168-0102(86)90081-7. [DOI] [PubMed] [Google Scholar]
  38. Sakmann B., Creutzfeldt O. D. Scotopic and mesopic light adaptation in the cat's retina. Pflugers Arch. 1969;313(2):168–185. doi: 10.1007/BF00586245. [DOI] [PubMed] [Google Scholar]
  39. Sakmann B., Filion M. Light adaptation of the late receptor potential in the cat retina. Adv Exp Med Biol. 1972;24(0):87–93. doi: 10.1007/978-1-4684-8231-7_9. [DOI] [PubMed] [Google Scholar]
  40. Schwartz E. A. Responses of single rods in the retina of the turtle. J Physiol. 1973 Aug;232(3):503–514. doi: 10.1113/jphysiol.1973.sp010283. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Steinberg R. H. Incremental responses to light recorded from pigment epithelial cells and horizontal cells of the cat retina. J Physiol. 1971 Aug;217(1):93–110. doi: 10.1113/jphysiol.1971.sp009561. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Werblin F. S. Control of retinal sensitivity. II. Lateral interactions at the outer plexi form layer. J Gen Physiol. 1974 Jan;63(1):62–87. doi: 10.1085/jgp.63.1.62. [DOI] [PMC free article] [PubMed] [Google Scholar]

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