Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Letter
  • Published:

Measurement of thermal contribution to photoreceptor sensitivity

Nature volume 403, pages 220–223 (2000)Cite this article

Abstract

Activation of a visual pigment molecule to initiate phototransduction requires a minimum energy, Ea, that need not be wholly derived from a photon, but may be supplemented by heat1. Theory2,3 predicts that absorbance at very long wavelengths declines with the fraction of molecules that have a sufficient complement of thermal energy, and that Ea is inversely related to the wavelength of maximum absorbance (λmax) of the pigment. Consistent with the first of these predictions, warming increases relative visual sensitivity to long wavelengths4,5,6,7,8. Here we measure this effect in amphibian photoreceptors with different pigments to estimate Ea (refs 2, 5,6,7) and test experimentally the predictions of an inverse relation between Ea and λmax. For rods and ‘red’ cones in the adult frog retina, we find no significant difference in Ea between the two pigments involved, although their λmax values are very different. We also determined Ea for the rhodopsin in toad retinal rods—spectrally similar to frog rhodopsin but differing in amino-acid sequence—and found that it was significantly higher. In addition, we estimated Ea for two pigments whose λmax difference was due only to a chromophore difference (A1 and A2 pigment, in adult and larval frog cones). Here Ea for A2 was lower than for A1. Our results refute the idea of a necessary relation between λmax and Ea, but show that the A1 → A2 chromophore substitution decreases Ea.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on SpringerLink
  • Instant access to the full article PDF.

USD 39.95

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Measurement of spectral sensitivities of rods and cones in the isolated retina.
Figure 2: Effect of temperature on sensitivity spectra.
Figure 3: Spectral sensitivities of frog tadpole ‘red’ cones (circles, 7.9?°C; squares, 24?°C).

Similar content being viewed by others

References

  1. St George, R. C. C. The interplay of light and heat in bleaching rhodopsin. J. Gen. Physiol. 35, 495–517 (1952).

    Article  CAS  Google Scholar 

  2. Stiles, W. S. in Trans. of the Optical Convention of the Worshipful Company of Spectacle Makers 97–107 (Spectacle Makers' Co., London, 1948).

    Google Scholar 

  3. Barlow, H. B. Purkinje shift and retinal noise. Nature 179, 255–256 (1957).

    Article  ADS  CAS  Google Scholar 

  4. de Vries, H. Der Einfluss der Temperatur des Auges auf die spektrale Empfindlichkeitskurve. Experientia 4, 357–358 (1948).

    Article  CAS  Google Scholar 

  5. Denton, E. J. & Pirenne, M. H. The visual sensitivity of the toad Xenopus laevis. J. Physiol. 125, 181–207 (1954).

    Article  CAS  Google Scholar 

  6. Lewis, P. R. A theoretical interpretation of spectral sensitivity curves at long wavelengths. J. Physiol. 130, 45–52 (1955).

    Article  CAS  Google Scholar 

  7. Srebro, R. A thermal component of excitation in the lateral eye of Limulus. J. Physiol. 187, 417–425 (1966).

    Article  CAS  Google Scholar 

  8. Lamb, T. D. Effects of temperature changes on toad rod photocurrents. J. Physiol. 346, 557–578 (1984).

    Article  CAS  Google Scholar 

  9. Lythgoe, J. N. in Sensory Biology of Aquatic Animals (eds Atema, J., Fay, R. R., Popper, A. N. & Tavolga, W. N.) 57–82 (Springer, New York, 1988).

    Book  Google Scholar 

  10. Goldsmith, T. H. in Facets of Vision (eds Stavenga, D. G. & Hardie, R. C.) 1–14 (Springer, Berlin, 1989).

    Book  Google Scholar 

  11. Donner, K., Firsov, M. L. & Govardovskii, V. I. The frequency of isomerization-like “dark” events in rhodopsin and porphyropsin rods of the bullfrog retina. J. Physiol. 428, 673–692 (1990).

    Article  CAS  Google Scholar 

  12. Firsov, M. L. & Govardovskii, V. I. Dark noise of visual pigments with different absorption maxima. Sensornye Sistemy 4, 25–34 (1990). (In Russian).

    Google Scholar 

  13. Bowmaker, J. K. et al. Visual pigments and the photic environment: The cottoid fish of Lake Baikal. Vision Res. 34, 591–606 (1994).

    Article  CAS  Google Scholar 

  14. Neitz, M., Neitz, J. & Jacobs, G. H. Spectral tuning of pigments underlying red–green color vision. Science 252, 971–974 (1991).

    Article  ADS  CAS  Google Scholar 

  15. Bridges, C. D. B. in Handbook of Sensory Physiology Vol. VII/1 (ed. Dartnall, H. J. A.) 417–480 (Springer, Berlin, 1972).

    Google Scholar 

  16. Reuter, T. Visual pigments and ganglion cell activity in the retinae of tadpoles and adult frogs (Rana temporaria L.). Acta Zool. Fenn. 122, 1–64 (1969).

    Google Scholar 

  17. Dartnall, H. J. A. & Lythgoe, J. N. The spectral clustering of visual pigments. Vision Res. 5, 81–100 (1965).

    Article  CAS  Google Scholar 

  18. Govardovskii, V. I., Fyhrquist, N., Reuter, T., Kuzmin, D. G. & Donner, K. In search of the visual pigment nomogram. Vis. Neurosci. (in the press).

  19. Koskelainen, A., Hemilä, S. & Donner, K. Spectral sensitivities of short- and long-wavelength sensitive cone mechanisms in the frog retina. Acta Physiol. Scand. 152, 115–124 (1994).

    Article  CAS  Google Scholar 

  20. Fyhrquist, N. et al. Rhodopsins from three frog and toad species: sequences and functional comparisons. Exp. Eye Res. 66, 295–305 (1998).

    Article  CAS  Google Scholar 

  21. Cooper, A. Energy uptake in the first step of visual excitation. Nature 282, 531–533 (1979).

    Article  ADS  CAS  Google Scholar 

  22. Lythgoe, R. J. & Quilliam, J. P. The thermal decomposition of visual purple. J. Physiol. 93, 24–38 (1938).

    Article  CAS  Google Scholar 

  23. Williams, T. P. & Milby, S. E. The thermal decomposition of some visual pigments. Vision Res. 8, 359–367 (1968).

    Article  CAS  Google Scholar 

  24. Barlow, H. B. Retinal noise and absolute threshold. J. Opt. Soc. Am. 46, 634–639 (1956).

    Article  ADS  CAS  Google Scholar 

  25. Baylor, D. A., Matthews, G. & Yau, K.-W. Two components of electrical dark noise in toad retinal rod outer segments. J. Physiol. 309, 591–621 (1980).

    Article  CAS  Google Scholar 

  26. Lamb, T. D. & Simon, E. J. Analysis of electrical noise in turtle cones. J. Physiol. 272, 435–468 (1977).

    Article  CAS  Google Scholar 

  27. Schnapf, J. L., Nunn, B. J., Meister, M. & Baylor, D. A. Visual transduction in cones of the monkey Macaca fascicularis¨. J. Physiol. 427, 681–713 (1990).

    Article  CAS  Google Scholar 

  28. Donner, K. Noise and the absolute thresholds of cone and rod vision. Vision Res. 32, 853–866 (1992).

    Article  CAS  Google Scholar 

  29. Barlow, R. B., Birge, R. R., Kaplan, E. & Tallent, J. R. On the molecular origin of photoreceptor noise. Nature 366, 64–66 (1993).

    Article  ADS  CAS  Google Scholar 

  30. Donner, K., Hemilä, S. & Koskelainen, A. Light adaptation of cone photoresponses studied at the photoreceptor and ganglion cell levels in the frog retina. Vision Res. 38, 19–36 (1998).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank V. I. Govardovskii for the nomogram-fitting program used for spectral analysis of pigments, H. Rita for statistical advice, C. Haldin and S. Pietilä for technical assistance, T. Reuter for comments on the manuscript, and Kilpisjärvi Biological Station for providing experimental animals. This work was supported by the Academy of Finland and by the Finnish Graduate Schools of Neuroscience and of Molecular Nanotechnology.

Author information

Authors and Affiliations

  1. Laboratory of Biomedical Engineering, PO Box 2200, Helsinki University of Technology, FIN-02015 HUT, Finland

    Ari Koskelainen & Petri Ala-Laurila

  2. Department of Biosciences, Division of Animal Physiology, FIN-00014 University of Helsinki, Finland

    Nanna Fyhrquist & Kristian Donner

Authors
  1. Ari Koskelainen
    View author publications

    Search author on:PubMed Google Scholar

  2. Petri Ala-Laurila
    View author publications

    Search author on:PubMed Google Scholar

  3. Nanna Fyhrquist
    View author publications

    Search author on:PubMed Google Scholar

  4. Kristian Donner
    View author publications

    Search author on:PubMed Google Scholar

Corresponding author

Correspondence to Ari Koskelainen.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Koskelainen, A., Ala-Laurila, P., Fyhrquist, N. et al. Measurement of thermal contribution to photoreceptor sensitivity. Nature 403, 220–223 (2000). https://doi.org/10.1038/35003242

Download citation

  • Received:

  • Accepted:

  • Issue date:

  • DOI: https://doi.org/10.1038/35003242

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing