Skip to main content
Log in

Fast-acting compressive and facilitatory nonlinearities in light-adapted fly photoreceptors

  • Research Articles
  • Published:
Annals of Biomedical Engineering Aims and scope Submit manuscript

Abstract

Light-adapted fly photoreceptor cells were stimulated with brief positive and negative contrast flashes (contrast=ΔI/I, I=intensity). Membrane potential responses to a wide range of flash intensities were well-fitted by a static nonlinearity followed by a compartmental model represented by a gamma function. However, the agreement improved if one parameter of the gamma function,n, varied quadratically with input light intensity. Response amplitude and time to peak were estimated from the fitted parameters. Response amplitude varied approximately linearly with contrast but showed nonlinear compression with the largest negative flashes. Reducing the background light level by 3 decades or hyperpolarizing the cell electrically produced stronger nonlinear compression with both contrast polarities. This is probably due to fast voltage-activated K+ channels. Responses to double flashes with varying time separations were well-fitted by summed gamma functions, allowing separation of the individual flash responses. There was no detectable time-dependent interaction between paired positive flashes at all separations. However, the response to two negative flashes was greater than the linear prediction at short separations, and this facilitatory nonlinearity decayed with a time constant of about 1 msec. The facilitation is probably related to resonant behavior in light-adapted photoreceptors and may be due to an IP3-induced intracellular Ca2+ release.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Autrum, H. Light and dark adaptation in invertebrates. In Handbook of Sensory Physiology VII/6C, edited by H. Autrum. New York: Springer-Verlag, 1981, pp. 1–91.

    Google Scholar 

  2. Baylor, D. A., A. L. Hodgkin, and T. D. Lamb. The electrical responses of turtle cones to flashes and steps of light.J. Physiol. 242:685–727, 1974.

    CAS  PubMed  Google Scholar 

  3. Bezprozvanny, I. Bell-shaped calcium-response curves of Ins(1,4,5)P3- and calcium-gated channels from endoplasmic reticulum of cerebellum.Nature 351:751–754, 1991.

    Article  CAS  PubMed  Google Scholar 

  4. Classen-Linke, I., and H. Stieve. The sensitivity of the ventral photoreceptor of Limulus recovers after light adaptation in two phases of dark adaptation.Z. Naturforsch. 41c:657–667, 1986.

    Google Scholar 

  5. Dubs, A. Non-linearity and light adaptation in the fly photoreceptor.J. Comp. Physiol. A 144:53–59, 1981.

    Google Scholar 

  6. Fein, A., and E. Z. Szuts. Photoreceptors: Their Role in Vision, Cambridge: Cambridge University Press, 1982, 212 pp.

    Google Scholar 

  7. French, A. S. Phototransduction in the fly compound eye exhibits temporal resonances and a pure time delay.Nature 283:200–202, 1980.

    CAS  PubMed  Google Scholar 

  8. French, A. S. The linear dynamic properties of phototransduction in the fly compound eye.J. Physiol. 308:385–401, 1980.

    CAS  PubMed  Google Scholar 

  9. French, A. S., and M. Järvilehto. The dynamic behaviour of photoreceptor cells in the fly in response to random (white noise) stimulation at a range of temperatures.J. Physiol. 274:311–322, 1978.

    CAS  PubMed  Google Scholar 

  10. French, A. S., and J. E. Kuster. Nonlinearities in locust photoreceptors during transduction of small numbers of photons.J. Comp. Physiol. A 156:645–652, 1985.

    Google Scholar 

  11. French, A. S., M. Korenberg, M. Järvilehto, E. Kouvalainen, M. Juusola, and M. Weckström. The dynamic nonlinear behaviour of fly photoreceptors evoked by a wide range of light intensities.Biophys. J. 65:832–839, 1993.

    CAS  PubMed  Google Scholar 

  12. Fuortes, M. G. F., and A. L. Hodgkin. Changes in time scale and sensitivity in the ommatidia ofLimulus.J. Physiol. 172:239–263, 1964.

    CAS  PubMed  Google Scholar 

  13. Hardie, R. C. Electrophysiological analysis of fly retina. I: Comparative properties of R1–6 and R7 and 8.J. Comp. Physiol. A 129:19–33, 1979.

    Google Scholar 

  14. Hardie, R. C. Functional organization of the fly retina. In: progress in Sensory Physiology, Vol. 5, edited by D. Ottoson. New York: Springer-Verlag, 1985, pp. 1–79.

    Google Scholar 

  15. Hardie, R. C. whole-cell recordings of the light-induced current in dissociatedDrosophila photoreceptors: evidence for feedback by calcium permeating the light sensitive channels.Proc. R. Soc. Lond. B 245:203–210, 1991.

    Google Scholar 

  16. Juusola, M. Linear and nonlinear contrast coding in light adapted blowfly photoreceptors.J. Comp. Physiol. A 172: 511–521, 1993.

    Article  Google Scholar 

  17. Juusola, M., and M. Weckström. Band-pass filtering by voltage-dependent membrane in an insect photoreceptor.Neurosci. Lett. 154:84–88, 1993.

    Article  CAS  PubMed  Google Scholar 

  18. Laughlin, S. B., J. Howard, and B. Blakeslee. Synaptic limitations to contrast coding in the retina of the blowfly.Calliphora.Proc. R. Soc. Lond. B 231:437–467, 1987.

    CAS  PubMed  Google Scholar 

  19. Laughlin, S. B., and M. Weckström Fast and slow photoreceptors—a comparative study of the functional diversity of coding and conductances in theDiptera.J. Comp. Physiol. A 172:593–609, 1993.

    Article  Google Scholar 

  20. Leutscher-Hazelhoff, J. T. Linear and non-linear performance of transducer and pupil in Calliphora retinula cells.J. Physiol. 246:333–350, 1975.

    CAS  PubMed  Google Scholar 

  21. Payne, R., and J. Howard Response of an insect photoreceptor: A simple log-normal model.Nature 290:415–416, 1984.

    Google Scholar 

  22. Pece, A. E. C., and A. S. French. Sublinear summation of responses in locust photoreceptors.J. Comp. Physiol. A 170:729–738, 1992.

    Article  Google Scholar 

  23. Pinter, R. B. Sinusoidal and delta function responses of visual cells of theLimulus eye.J. Gen. Physiol. 49:565–593, 1966.

    Article  CAS  PubMed  Google Scholar 

  24. Press, W. H., B. P. Flannery, S. A. Teukolsky, and W. T. Vetterling. Numerical Recipes in C. Cambridge: Cambridge University Press, 1990, 735 pp.

    Google Scholar 

  25. Spekreijse, H., and H. Oostings. Linearizing: A method for analysing and synthesizing non-linear systems.Kybernetik 7:22–31, 1970.

    Article  CAS  PubMed  Google Scholar 

  26. Waltz, B. Enhancement of sensitivity in photoreceptors of the honey bee drone by light and by Ca2+.J. Comp. Physiol. A 170:605–613, 1992.

    Google Scholar 

  27. Weckström, M., E. Kouvalainen, and M. Järvilehto. Nonlinearities in response properties of insect visual cells: An analysis in time and frequency domains.Acta Physiol. Scand. 132:103–113, 1988.

    PubMed  Google Scholar 

  28. Weckström, M., R. C. Hardie, and S. B. Laughlin. Voltage-activated potassium channels in blowfly photoreceptors and their role in light adaptation.J. Physiol. 440:635–657, 1991.

    PubMed  Google Scholar 

  29. Weckström, M., M. Juusola, and S. B. Laughlin. Presynaptic enhancement of signal transients in photoreceptor terminals in the compound eye.Proc. R. Soc. Lond. B 250: 83–89, 1992.

    Google Scholar 

  30. Wong, F., B. W. Knight, and F. A. Dodge. Dispersion of latencies in photoreceptors of Limulus and the adapting bump model.J. Gen. Physiol. 76:517–537, 1980.

    CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Weckström, M., Juusola, M., Uusitalo, R.O. et al. Fast-acting compressive and facilitatory nonlinearities in light-adapted fly photoreceptors. Ann Biomed Eng 23, 70–77 (1995). https://doi.org/10.1007/BF02368302

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02368302

Keywords

Navigation