Biophysics of structure and mechanism

, Volume 5, Issue 2–3, pp 187–196 | Cite as

Rapid photopigment conversions in blowfly visual sense cells consequences for receptor potential and pupillary response

  • Hans Muijser
  • Doekele G. Stavenga
Article

Abstract

Combined optical and electrophysiological experiments on the kinetics of visual pigment conversions in blowfly and the resulting pupillary response and late receptor potential are described. The photometrically detectable conversions of rhodopsin and metarhodopsin in the living wild type fly are completed within 0.5 ms. Prolonged pupillary responses and receptor potentials occur upon intense blue flashes. Subsequent intense red flashes abolish the prolonged responses in the case of both membrane potential and the pupil. The interrelation of potential and pupil is discussed.

Key words

Fly photoreceptor cells Visual pigment Receptor potential Pupillary response 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Atzmon, Z., Hillman, P., Hochstein, S.: Visual response in barnacle photoreceptors is not inititated by transition to and from metarhodopsin. Nature 274, 71–75 (1978)Google Scholar
  2. Bruno, M. S., Barnes, S. N., Goldsmith, T. H.: The visual pigment and visual cycle of the lobster, Homarus. J. Comp. Physiol. 120, 123–142 (1977)Google Scholar
  3. Fein, A., Cone, R. A.: Limulus rhodopsin: Rapid return of transient intermediates to the thermally stable state. Science 182, 495–497 (1973)Google Scholar
  4. Franceschini, N.: Sampling of the visual environment by the compound eye of the fly: Fundamentals and applications. In: Photoreceptor optics. Snyder, A. W., Menzel, R. (eds.), pp. 98–125. Berlin, Heidelberg, New York: Springer 1975Google Scholar
  5. Franceschini, N., Kirschfeld, K.: Le contrÔle automatique du flux lumineux dans l'oeil composé des Diptères. Propriétés spectrales, statiques et dynamiques du mécanisme. Biol. Cybern. 21, 181–203 (1976)Google Scholar
  6. Goldsmith, T. H.: The natural history of invertebrate visual pigments. In: Handbook of sensory physiology, Vol. VII/1. Dartnall, H. J. A. (ed.), pp. 685–719. Berlin, Heidelberg, New York: Springer 1972Google Scholar
  7. Goldsmith, T. H.: The effects of screening pigments on the spectral sensitivity of some crustacea with scotopic (superposition) eyes. Vision Res. 18, 475–482 (1978)Google Scholar
  8. Hamdorf, K.: Physiology of visual pigments in invertebrates. In: Handbook of sensory physiology, Vol. VII/6A. Autrum, H. (ed.), pp. 145–224. Berlin, Heidelberg, New York: Springer 1979Google Scholar
  9. Hamdorf, K., Paulsen, R., Schwemer, J.: Photoregeneration and sensitivity of photoreceptors of invertebrates. In: Biochemistry and physiology of visual pigments. Langer, H.(ed.), pp. 155–166. Berlin, Heidelberg, New York: Springer 1973Google Scholar
  10. Hamdorf, K., Razmjoo, S.: The prolonged depolarizing afterpotential and its contribution to the understanding of photoreceptor function. Biophys. Struct. Mech. 3, 163–170 (1977)Google Scholar
  11. Hamdorf, K., Rosner, G.: Adaptation und Photoregeneration im Fliegenauge. J. Comp. Physiol. 86, 281–292 (1973)Google Scholar
  12. Hamdorf, K., Schwemer, J.: Photoregeneration and the adaptation process in insect photoreceptors. In: Photoreceptor optics. Snyder, A. W., Menzel, R. (eds.), pp. 263–289. Berlin, Heidelberg, New York: Springer 1975Google Scholar
  13. Hillman, P., Dodge, F. A., Hochstein, S., Knight, B. W., Minke, B.: Rapid dark recovery of the invertebrate early receptor potential. J. Gen. Physiol. 62, 77–86 (1973)Google Scholar
  14. Hochstein, S., Minke, B., Hillman, P.: Antagonistic components of the late receptor potential in the barnacle photoreceptor arising from different stages of the pigment process. J. Gen. Physiol. 62, 105–128 (1973)Google Scholar
  15. Höchstem, S., Minke, B., Hillman, P., Knight, B. W.: The kinetics of visual pigments. I. Mathematical analysis. Biol. Cybernetics 30, 23–32 (1978)Google Scholar
  16. Kirschfeld, K., Franceschini, N.: Ein Mechanismus zur Steuerung des Lichtflusses in den Rhabdomeren des Komplexauges von Musca. Kybernetik 6, 13–22 (1969)Google Scholar
  17. Kirschfeld, K., Franceschini, N., Minke, B.: Evidence for a sensitising pigment in fly photoreceptors. Nature 269, 386–390 (1977)Google Scholar
  18. Lisman, J. E., Bering, H.: Electrophysiological measurement of the number of rhodopsin molecules in single Limulus photoreceptors. J. Gen. Physiol. 70, 621–633 (1977)Google Scholar
  19. Lisman, J. E., Sheline, Y.: Analysis of the rhodopsin cycle in Limulus ventral photoreceptors using the early receptor potential. J. Gen. Physiol. 68, 487–501 (1976).Google Scholar
  20. Lo, M.-V. C., Pak, W. L.: Desensitisation of peripheral photoreceptors shown by blue-induced decrease in transmittance of Drosophila rhabdomeres. Nature 273, 772–774 (1978)Google Scholar
  21. Miller, W. H.: Mechanisms of photomechanical movement. In: Photoreceptor optics. Snyder, A. W., Menzel, R. (eds.), pp. 415–428. Berlin, Heidelberg, New York: Springer 1975Google Scholar
  22. Miller, W. H., Cawthon, D. F.: Pigment granule movement in Limulus photoreceptors. Invest. Ophthalmol. 13, 401–405 (1974)Google Scholar
  23. Minke, B., Hochstein, S., Hillman, P.: Antagonistic process as source of visible-light suppression of afterpotential in Limulus UV photoreceptors. J. Gen. Physiol. 62, 787–791 (1973)Google Scholar
  24. Minke, B., Hochstein, S., Hillman, P.: Derivation of a quantitative kinetic model for a visual pigment from observations of early receptor potential. Biophys. J. 14, 490–512 (1974)Google Scholar
  25. Minke, B., Hochstein, S., Hillman, P.: The kinetics of visual pigments. II. Application to measurements on a bistable pigment system. Biol. Cybernetics 30, 33–43 (1978)Google Scholar
  26. Muijser, H.: The receptor potential of retinular cells of the blowfly Calliphora: the role of sodium, potassium and calcium ions. J. Comp. Physiol., submitted (1979)Google Scholar
  27. Muijser, H., Leutscher-Hazelhoff, J. T., Stavenga, D. G., Kuiper, J. W.: Photopigment conversions expressed in receptor potential and membrane resistance of blowfly visual sense cells. Nature 254, 520–522 (1975)Google Scholar
  28. Nolte, J., Brown, J. E.: Ultraviolet-induced sensitivity to visible light in ultraviolet receptors of Limulus. J. Gen. Physiol. 59, 186–200 (1972)Google Scholar
  29. Olivo, R. F., Larsen, M. E.: Brief exposure to light initiates screening pigment migration in retinula cells of the crayfish, Procambarus. J. Comp. Physiol. 125, 91–96 (1978)Google Scholar
  30. Pak, W. L., Lidington, K. J.: Fast electrical potential from a long-lived, long-wavelength photoproduct of fly visual pigment. J. Gen. Physiol. 63, 740–756 (1974)Google Scholar
  31. Razmjoo, S., Hamdorf, K.: Visual sensitivity and the variation of total pigment content in the blowfly photoreceptor membrane. J. Comp. Physiol. 105, 279–286 (1976)Google Scholar
  32. Stark, W. S., Ivanyshyn, A. M., Greenberg, R. M.: Sensitivity and photopigments of R1–6, a two-peaked photoreceptor, in Drosophila, Calliphora, and Musca. J. Comp. Physiol. 121, 289–305 (1977)Google Scholar
  33. Stavenga, D. G.: Adaptation in the compound eye. Proc. Int. Union Physiol. Sc. IX, 532, XXV Int. Congr. Munich (1971)Google Scholar
  34. Stavenga, D. G.: Dark regeneration of invertebrate visual pigments. In: Photoreceptor optics. Snyder, A. W., Menzel, R. (eds.), pp. 290–295. Berlin, Heidelberg, New York: Springer 1975Google Scholar
  35. Stavenga, D. G.: Fly visual pigments. Difference in visual pigments of blowfly and dronefly retinula cells. J. Comp. Physiol. 111, 137–152 (1976)Google Scholar
  36. Stavenga, D. G.: Pseudopupils of compound eyes. In: Handbook of sensory physiology, Vol. VII/6A. Autrum, H. (ed.), pp. 357–439. Berlin, Heidelberg, New York: Springer 1979Google Scholar
  37. Stavenga, D. G., Flokstra, J. H., Kuiper, J. W.: Photopigment conversions expressed in pupil mechanism of blowfly visual sense cells. Nature 253, 740–742 (1975)Google Scholar
  38. Stavenga, D. G., Numan, J. A. J., Tinbergen, J., Kuiper, J. W.: Insect pupil mechanisms. II. Pigment migration in retinula cells of butterflies. J. Comp. Physiol. 113, 73–93 (1977)Google Scholar
  39. Stavenga, D. G., Zantema, A., Kuiper, J. W.: Rhodopsin processes and the function of the pupil mechanisms in flies. In: Biochemistry and physiology of visual pigments. Langer, H. (ed.), pp. 175–180. Berlin, Heidelberg, New York: Springer 1973Google Scholar
  40. Stephenson, R. S., Pak, W. L.: Metarhodopsin potential of Drosophila: corneal positive component due to second-order neurons. Biophys. J. 21, 172a (1978)Google Scholar
  41. Strong, J., Lisman, J.: Initiation of light adaptation in barnacle photoreceptors. Science 200, 1485–1487 (1978)Google Scholar
  42. Tsukahara, Y., Horridge, G. A., Stavenga, D. G.: Afterpotentials in dronefly retinula cells. J. Comp. Physiol. 114, 253–266 (1977)Google Scholar

Copyright information

© Springer-Verlag 1979

Authors and Affiliations

  • Hans Muijser
    • 1
  • Doekele G. Stavenga
    • 1
  1. 1.Biophysical DepartmentLaboratorium voor Algemene Natuurkunde, Rijksuniversiteit GroningenGroningenThe Netherlands

Personalised recommendations