Abstract
In recent years, our knowledge of the biochemical mechanisms underlying the transduction process in photoreceptors has expanded rapidly. However, a full picture of the temporal dynamics of these mechanisms remains elusive. To study the dynamics in the Limulus ventral photoreceptor, we measure its light-evoked transfer function under voltage clamp. Comparison of this transfer function to biochemically realistic theoretical models of transduction provides insights into the photoreceptor dynamics. This comparison supports the suggestion that the low-frequency behaviour of the Limulus photoreceptor, corresponding to light and dark adaptation, is that of a nonlinear negative feedback loop. The main reactions of this loop have time constants between about 1 and 40 s. Such a feedback loop does not account, however, for the high-frequency behaviour of the responses, which implies the existence of a further, fast-acting, mechanism.
Similar content being viewed by others
References
Ahlfors L (1979) Complex analysis. McGraw-Hill, New York
Bacigalupo J, Johnson E, Robinson P, Lisman JE (1990) Second messengers in invertebrate phototransduction. In: Hidalgo C, Bacigalupo J, Jaimqvich E, Vergara J (eds) Transduction in biological systems. Plenum Press, New York
Brown JE, Rubin LJ, Ghalayani AJ, Tarver AL, Irvine RF, Berridge MJ, Anderson RE (1984) Myo-inositol polyphosphate may be a messenger for visual excitation in Limulus photoreceptors. Nature 311:160–162
Brodie SE, Knight BW, Ratliff F (1978) The response of the Limulus retina to moving stimuli: a prediction by Fourier synthesis. J Gen Physiol 72:129–166
Dodge FA, Knight BW, Toyoda JI (1968) Voltage noise in Limulus visual cells. Science 160:88–90
Fein A, Payne R, Corson DW, Berridge MJ, Irvine RF (1984) Photoreceptor excitation and adaptation by inositol 1,4,5-trisphosphate. Nature 311:157–160
Grzywacz NM, Hillman P (1988) Biophysical evidence that light adaptation in Limulus photoreceptors is due to a negative feedback. Biophys J 53:337–348
Grzywacz NM, Hillman P, Knight BW (1988) The quantal source of area supralinearity of flash responses in Limulus photoreceptors. J Gen Physiol 91:659–684
Grzywacz NM, Hillman P, Knight BW (1992) The amplitudes of unit events in Limulus photoreceptors are modulated from an input that resembles the overall response. Biol Cybern (this issue)
Knight BW, Toyoda JI, Dodge FA (1970) A quantitative description of the dynamics of excitation and inhibition in the eye of Limulus. J Gen Physiol 56:421–437
Lisman JE, Brown JE (1972) The effects of intracellular iontophoretic injection of calcium and sodium ions on the light response of Limulus ventral photoreceptors. J Gen Physiol 59:701–719
Lisman JE, Brown JE (1975) Effects of intracellular injection of calcium buffers on light adaptation in Limulus ventral photoreceptors. J Gen Physiol 66:489–506
Nygaard RW, Frumkes TE (1982) LEDs: convenient, inexpensive sources for visual experimentation. Vision Res 22:435–440.
Pasino E. Marchiafava PL (1976) Transfer properties of rod and cone cells in the retina of the tiger salamander. Vision Res 16:381–386
Pinter RB (1966) Sinusoidal and delta function responses of visual cells of the Limulus eye. J Gen Physiol 49:656–693
Senturia DS, Wedlock BD (1975) Electronic circuits and applications. Wiley, New York
Thorson J, Biederman-Thorson M (1974) Distributed relaxation processes in sensory adaptation. Science 183:161–172
Toyoda JI, Coles J (1975) Rod response to sinusoidally flickering light. Vision Res 15:981–983
Author information
Authors and Affiliations
Additional information
This work was supported by grants from the Binational Science Foundation (BSF) Jerusalem, Israel and the Israel Academy of Sciences and Humanities, by NIH grant EY 1428, and by NSF grant DMS 8505442
Rights and permissions
About this article
Cite this article
Grzywacz, N.M., Hillman, P. & Knight, B.W. Response transfer functions of Limulus ventral photoreceptors: interpretation in terms of transduction mechanisms. Biol. Cybern. 66, 429–435 (1992). https://doi.org/10.1007/BF00197723
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00197723