Hostname: page-component-76c49bb84f-ndtt8 Total loading time: 0 Render date: 2025-07-08T14:15:54.898Z Has data issue: false hasContentIssue false
  • English
  • Français

The thermal contribution to photoactivation in A2 visual pigments studied by temperature effects on spectral properties

Published online by Cambridge University Press:  18 November 2003

PETRI ALA-LAURILA ,
RAULI-JAN ALBERT ,
PIA SAARINEN ,
ARI KOSKELAINEN  and
KRISTIAN DONNER
PETRI ALA-LAURILA
Affiliation:
Laboratory of Biomedical Engineering, Helsinki University of Technology, FIN-02015 HUT, Finland
RAULI-JAN ALBERT
Affiliation:
Laboratory of Biomedical Engineering, Helsinki University of Technology, FIN-02015 HUT, Finland
PIA SAARINEN
Affiliation:
Department of Biosciences, Division of Animal Physiology, FIN-00014 University of Helsinki, Finland
ARI KOSKELAINEN
Affiliation:
Laboratory of Biomedical Engineering, Helsinki University of Technology, FIN-02015 HUT, Finland
KRISTIAN DONNER
Affiliation:
Department of Biosciences, Division of Animal Physiology, FIN-00014 University of Helsinki, Finland
Get access Rights & Permissions [Opens in a new window]

Abstract

Effects of temperature on the spectral properties of visual pigments were measured in the physiological range (5–28°C) in photoreceptor cells of bullfrog (Rana catesbeiana) and crucian carp (Carassius carassius). Absorbance spectra recorded by microspectrophotometry (MSP) in single cells and sensitivity spectra recorded by electroretinography (ERG) across the isolated retina were combined to yield accurate composite spectra from ca. 400 nm to 800 nm. The four photoreceptor types selected for study allowed three comparisons illuminating the properties of pigments using the dehydroretinal (A2) chromophore: (1) the two members of an A1/A2 pigment pair with the same opsin (porphyropsin vs. rhodopsin in bullfrog “red” rods); (2) two A2 pigments with similar spectra (porphyropsin rods of bullfrog and crucian carp); and (3) two A2 pigments with different spectra (rods vs. long-wavelength-sensitive (L-) cones of crucian carp). Qualitatively, the temperature effects on A2 pigments were similar to those described previously for the A1 pigment of toad “red” rods. Warming caused an increase in relative sensitivities at very long wavelengths but additionally a small shift of λmax toward shorter wavelengths. The former effect was used for estimating the minimum energy required for photoactivation (Ea) of the pigment. Bullfrog rod opsin with A2 chromophore had Ea = 44.2 ± 0.9 kcal/mol, significantly lower (one-tailed P < 0.05) than the value Ea = 46.5 ± 0.8 kcal/mol for the same opsin coupled to A1. The A2 rod pigment of crucian carp had Ea = 42.3 ± 0.6 kcal/mol, which is significantly higher (one-tailed P < 0.01) than that of the L-cones in the same retina (Ea = 38.3 ± 0.4 kcal/mol), whereas the difference compared with the bullfrog A2 rod pigment is not statistically significant (two-tailed P = 0.13). No strict connection between λmax and Ea appears to exist among A2 pigments any more than among A1 pigments. Still, the A1 → A2 chromophore substitution in bullfrog opsin causes three changes correlated as originally hypothesized by Barlow (1957): a red-shift of λmax, a decrease in Ea, and an increase in thermal noise.

Keywords

PhotoreceptorSpectral sensitivityActivation energyPorphyropsinRetinal

Information

Type
Research Article
Information
Visual Neuroscience , Volume 20 , Issue 4 , July 2003 , pp. 411 - 419
Copyright
2003 Cambridge University Press

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.)

Article purchase

Temporarily unavailable

References

REFERENCES

Aho, A.-C., Donner, K., Hydén, C., Larsen, L.O., & Reuter, T. (1988). Low retinal noise in animals with low body temperature allows high visual sensitivity. Nature 334, 348–350.Google Scholar
Ala-Laurila, P., Saarinen, P., Albert, R., Koskelainen, A., & Donner, K. (2002). Temperature effects on spectral properties of red and green rods in toad retina. Visual Neuroscience 19, 781–792.Google Scholar
Allen, D.M. & McFarland, W.N. (1973). The effect of temperature on rhodopsin-porphyropsin ratios in a fish. Vision Research 13, 1303–1309.Google Scholar
Ashmore, J.F. & Falk, G. (1977). Dark noise in retinal bipolar cells and stability of rhodopsin in rods. Nature 270, 69–71.Google Scholar
Autrum, H. (1943). Uber kleinste Reize bei Sinnesorganen. Biologisches Zentralblatt 63, 209–236.Google Scholar
Barlow, H.B. (1956). Retinal noise and absolute threshold. Journal of the Optical Society of America 46, 634–639.Google Scholar
Barlow, H.B. (1957). Purkinje shift and retinal noise. Nature 179, 255–256.Google Scholar
Barlow, R.B., Birge, R.R., Kaplan, E., & Tallent, J.R. (1993). On the molecular origin of photoreceptor noise. Nature 366, 64–66.Google Scholar
Baylor, D.A., Matthews, G., & Yau, K.-W. (1980). Two components of electrical dark noise in toad retinal rod outer segments. Journal of Physiology 309, 591–621.Google Scholar
Bridges, C.D.B. (1956). The visual pigments of the rainbow trout (Salmo irideus). Journal of Physiology 134, 620–629.Google Scholar
Bridges, C.D.B. (1964). Effect of season and environment on the retinal pigments of two fishes. Nature 203, 191–192.Google Scholar
Bridges, C.D.B. (1967). Spectroscopic properties of porphyropsins. Vision Research 7, 349–369.Google Scholar
Bridges, C.D.B. (1972). The rhodopsin-porphyropsin visual system. In Handbook of Sensory Physiology, VII/1. Photochemistry of Vision, ed. Dartnall, H.J.A., pp. 417–480. Berlin-Heidelberg-New York: Springer.
Bridges, C.D.B. & Yoshikami, S. (1970). The rhodopsin-porphyropsin system in freshwater fishes—1. Effects of age and photic environment. Vision Research 10, 1315–1332.Google Scholar
Dartnall, H.J.A. (1955). Visual pigments of the bleak (Alburnus lucidus). Journal of Physiology 128, 131–156.Google Scholar
Dartnall, H.J.A. (1972). Photosensitivity. In Handbook of Sensory Physiology, Vol. VII/1. Photochemistry of Vision, ed. Dartnall, H.J.A. pp. 122–145. Berlin-Heidelberg-New York: Springer.
Dartnall, H.J.A. & Lythgoe, J.N. (1965). The spectral clustering of visual pigments. Vision Research 5, 81–100.Google Scholar
Dartnall, H.J.A., Kander, M.R., & Munz, F.W. (1961). Periodic changes in the visual pigment of a fish. In Progress in Photobiology, ed. Christensen, B.C. & Buchmann, B., pp. 203–213. Amsterdam: Elsevier.
Denton, E.J. & Pirenne, M.H. (1954). The visual sensitivity of the toad Xenopus laevis. Journal of Physiology 125, 181–207.Google Scholar
de Vries, H. (1948). Der Einfluss der Temperatur des Auges auf die spektrale Empfindlichkeitskurve. Experientia 4, 357–358.Google Scholar
Donner, K., Hemilä, S., & Koskelainen, A. (1988). Temperature-dependence of rod photoresponses from the aspartate-treated retina of the frog (Rana temporaria). Acta Physiologica Scandinavica 134, 535–541.Google Scholar
Donner, K., Firsov, M.L., & Govardovskii, V.I. (1990). The frequency of isomerization-like “dark” events in rhodopsin and porphyropsin rods of the bull-frog retina. Journal of Physiology 428, 673–692.Google Scholar
Firsov, M.L. & Govardovskii, V.I. (1990). Dark noise of visual pigments with different absorption maxima. Sensornye Sistemy 4, 25–34. (In Russian).Google Scholar
Firsov, M.L., Govardovskii, V.I., & Donner, K. (1994). Response univariance in bull-frog rods with two visual pigments. Vision Research 34, 839–847.Google Scholar
Firsov, M.L., Donner, K., & Govardovskii, V.I. (2002). pH and rate of “dark” events in toad retinal rods: Test of a hypothesis on the molecular origin of photoreceptor noise. Journal of Physiology 539, 837–846.Google Scholar
Fong, S.-L., Landers, R.A., & Bridges, C.D.B. (1985). Varieties of rhodopsin in frog rod outer segment membranes: Analysis by isoelectric focusing. Vision Research 25, 1387–1397.Google Scholar
Fyhrquist, N. (1999). Spectral and thermal properties of amphibian visual pigments related to molecular structure. Dissertationes Biocentri Viikki Universitatis Helsingiensis 18/99.
Goldsmith, T.H. (1989). Compound eyes and the world of vision research. In Facets of Vision, ed. Stavenga, D.G. & Hardie, R.C., pp. 1–14. Berlin-Heidelberg-New York: Springer-Verlag.
Govardovskii, V.I., Fyhrquist, N., Reuter, T., Kuzmin, D.G., & Donner, K. (2000). In search of the visual pigment template. Visual Neuroscience 17, 509–528.Google Scholar
Hárosi, F.I. (1994). An analysis of two spectral properties of vertebrate visual pigments. Vision Research 34, 1359–1367.Google Scholar
Kayada, S., Hisatomi, O., & Tokunaga, F. (1995). Cloning and expression of frog rhodopsin cDNA. Comparative Biochemistry and Physiology 110B, 599–604.Google Scholar
Koskelainen, A., Hemilä, S., & Donner, K. (1994). Spectral sensitivities of short- and long-wavelength sensitive cone mechanisms in the frog retina. Acta Physiologica Scandinavica 152, 115–124.Google Scholar
Koskelainen, A., Ala-Laurila, P., Fyhrquist, N., & Donner, K. (2000). Measurement of thermal contribution to photoreceptor sensitivity. Nature 403, 220–223.Google Scholar
Lewis, P.R. (1955). A theoretical interpretation of spectral sensitivity curves at long wavelengths. Journal of Physiology 130, 45–52.Google Scholar
Makino, C.L. & Dodd, R.L. (1996). Multiple visual pigments in a photoreceptor of the salamander retina. Journal of General Physiology 108, 27–34.Google Scholar
Makino, C.L., Groesbeek, M., Lugtenburg, J., & Baylor, D.A. (1999). Spectral tuning in salamander visual pigments studied with dihydroretinal chromophores. Biophysical Journal 77, 1024–1035.Google Scholar
Marks, W.B. (1965). Visual pigments of single goldfish cones. Journal of Physiology 178, 14–32.Google Scholar
Matthews, G. (1984). Dark noise in the outer segment membrane current of green rod photoreceptors from toad retina. Journal of Physiology 349, 607–618.Google Scholar
McFarland, W.N. & Allen, D.M. (1977). The effect of extrinsic factors on two distinctive rhodopsin-porphyropsin systems. Canadian Journal of Zoology 55, 1000–1009Google Scholar
Palacios, A.G., Varela, F.J., Srivastava, R., & Goldsmith, T.H. (1998). Spectral sensitivity of cones in the goldfish, Carassius auratus. Vision Research 38, 2135–2146.Google Scholar
Reuter, T. (1969). Visual pigments and ganglion cell activity in the retinae of tadpoles and adult frogs (Rana temporaria L.). Acta Zoologica Fennica 122, 1–64.Google Scholar
Reuter, T.E., White, R.H., & Wald, G. (1971). Rhodopsin and porphyropsin fields in the adult bullfrog retina. Journal of General Physiology 58, 351–371.Google Scholar
Rieke, F. & Baylor, D.A. (2000). Origin and functional impact of dark noise in retinal cones. Neuron 26, 181–186.Google Scholar
Röhlich, P., van Veen, T., & Szél, A. (1994). Two different visual pigments in one retinal cone cell. Neuron 13, 1159–1166.Google Scholar
Shand, J., Partridge, J.C., Archer, S.N., Potts, G.W., & Lythgoe, J.N. (1988). Spectral absorbance changes in the violet/blue sensitive cones of the juvenile pollack, Pollachius pollachius. Journal of Comparative Physiology A 163, 699–703.Google Scholar
Srebro, R. (1966). A thermal component of excitation in the lateral eye of Limulus. Journal of Physiology 187, 417–425.Google Scholar
Stell, W.K. & Hárosi, F.I. (1976). Cone structure and visual pigment content in the retina of the goldfish. Vision Research 16, 647–657.Google Scholar
St. George, R.C.C. (1952). The interplay of light and heat in bleaching rhodopsin. Journal of General Physiology 35, 495–517.Google Scholar
Stiles, W.S. (1948). The physical interpretation of the spectral sensitivity curve of the eye. In Transactions of the Optical Convention of the Worshipful Company of Spectacle Makers, pp. 97–107. London: Spectacle Makers' Co.
Tsin, A.T.C. & Beatty, D.D. (1980). Visual pigments and vitamins A in the adult bullfrog. Experimental Eye Research 30, 143–153.Google Scholar
Williams, T.P. & Milby, S.E. (1968). The thermal decomposition of some visual pigments. Vision Research 8, 359–367.Google Scholar
Wood, P. & Partridge, J.C. (1993). Opsin substitution induced in retinal rods of the eel (Anguilla anguilla (L.)): A model for G-protein-linked receptors. Proceedings of the Royal Society B (London) 254, 227–232.Google Scholar
Yoshizawa, T. (1972). The behaviour of visual pigments at low temperatures. In Handbook of Sensory Physiology, VII/1. Photochemistry of Vision, ed. Dartnall, H.J.A., pp. 147–179. Berlin–Heidelberg–New York: Springer.
Yoshizawa, T. & Horiuchi, S. (1969). Intermediates in the photolytic process of porphyropsin. Experimental Eye Research 8, 243–244.Google Scholar