Hostname: page-component-7dd5485656-s6l46 Total loading time: 0 Render date: 2025-10-31T22:12:37.569Z Has data issue: false hasContentIssue false
  • English
  • Français

Biophysical processes in invertebrate photoreceptors: recent progress and a critical overview based on Limulus photoreceptors

Published online by Cambridge University Press:  17 March 2009

Károly Nagy
Károly Nagy
Affiliation:
Institut f¨r Biologie II, der Rheinisch-Westfälischen Technischen Hochschule Aachen, Kopernikusstr. 16, D-5100 Aachen
Get access Rights & Permissions [Opens in a new window]

Extract

Photoreceptor cells are special neurons which convert light to an electrical signal. The absorption of a photon by a rhodopsin molecule triggers a sequence of chemical processes leading to a change in the membrane voltage of the photoreceptor. The mechanism of this light-induced voltage change is different in vertebrates and invertebrates. Light causes a hyperpolarization in vertebrates, but a depolarization in invertebrate photoreceptors.

Information

Type
Research Article
Information
Quarterly Reviews of Biophysics , Volume 24 , Issue 2 , May 1991 , pp. 165 - 226
Copyright
Copyright © Cambridge University Press 1991

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

Adolph, A. R. (1964). Spontaneous slow potential fluctuations in the Limulus photoreceptor. J. gen. Physiol. 48, 297–322.Google Scholar
Adolph, A. R. (1968). Thermal and spectral sensitivities of discrete slow potentials in Limulus eye. J. Gen. Physiol. 52, 584–599.CrossRefGoogle ScholarPubMed
Ammann, D. (1986). Ionoselective Microelectrodes. Berlin, Heidelberg, New York, Tokyo: Springer-Verlag.Google Scholar
Bacigalupo, J., Chinn, K. & Lisman, J. E. (1986). Ion channels activated by light in Limulus ventral photoreceptors. J. gen. Physiol. 87, 73–89.Google Scholar
Bacigalupo, J. & Lisman, J. E. (1983). Single channel currents activated by light in Limulus ventral photoreceptors. Nature, Lond. 304, 268–270.CrossRefGoogle ScholarPubMed
Bacigalupo, J. & Lisman, J. E. (1984). Light-activated channels in Limulus ventral photoreceptors. Biophys. J. 45, 3–5.Google Scholar
Baker, P. F. & Dipolo, R. (1984). Axonal calcium and magnesium homeostasis. Curr. Top. Membr. Transp. 22, 195–247.CrossRefGoogle Scholar
Baverstock, J., Nobes, K. & Saibil, H. (1990). G-protein activation in squid photoreceptor membranes. Int. Symp. Signal Transduction in Photoreceptor Cells, abstr. p. 53. FRG: Jülich.Google Scholar
Bayer, D. S. & Barlow, R. B. (1978). Limulus ventral eye: physiological properties of photoreceptor cells in an organ culture medium. J. gen. Physiol. 72, 539–563.Google Scholar
Becker, U. W., Nuske, J. H. & Stieve, H. (1988). Phototransduction in the microvillar visual cell of Limulus: electrophysiology and biochemistry. In Progress in retinal research. (ed. Osborn, N. & Chader, J.), Vol. 8, pp. 229–253. Pergamon Press.Google Scholar
Berridge, M. J. (1983). Rapid accumulation of inositol trisphosphate reveals that agonists hydrolyse polyphosphoinositides instead of phosphatidylinositol. Biochem. J. 212, 849–858.Google Scholar
Berridge, M. J. & Irvine, R. F. (1984). Inositol trisphosphate, a novel second messenger in cellular signal transduction. Nature, Lond. 312, 315–321.CrossRefGoogle ScholarPubMed
Blinks, J. R., Wier, W. G., Hess, P. & Prendergast, F. G. (1982). Measurement of Ca2+ concentrations in living cells. Prog. Biophys. molec. Biol. 40, 1–114.Google Scholar
Bolsover, S. R. & Brown, J. E. (1982). Injection of guanosine and adenosine Nucleotides into Limulus ventral photoreceptor cells. J. Physiol., Lond. 332, 325–342.CrossRefGoogle ScholarPubMed
Bolsover, S. R. & Brown, J. E. (1985). Calcium ion, an intracellular messenger of light adaptation, also participates in excitation of Limulus photoreceptors. J. Physiol., Lond. 364, 384–393.CrossRefGoogle ScholarPubMed
Borsellino, A. & Fourtes, M. G. F. (1968). Responses to single photons in visual cells of Limulus. J. Physiol., Lond. 196, 507–539.CrossRefGoogle ScholarPubMed
Brown, H. M. (1976). Intracellular Na+, K+ and Cl− activities in Balanus photoreceptors. J. gen. Physiol. 68, 281–296.Google Scholar
Brown, H. M., Rydqvist, B. & Moser, H. (1988). Intracellular calcium changes in Balanus photoreceptor. A study with calcium ion-selective electrodes and arsenazo III. Cell Calc. 9, 105–119.CrossRefGoogle ScholarPubMed
Brown, J. E. (1986). Calcium and light adaptation in invertebrate photoreceptors. In The Molecular Mechanism of Phototransduction, Dahlem Konferenzen (ed. Stieve, H.), pp. 231–240. Berlin, Heidelberg, New York, Tokyo: Springer-Verlag.Google Scholar
Brown, J. E. & Blinks, J. R. (1974). Changes in intracellular free calcium during illumination of invertebrate photoreceptors. Detection with aequorin. J. gen. Physiol. 64, 643–665.CrossRefGoogle ScholarPubMed
Brown, J. E., Brown, P. K. & Pinto, L. H. (1977). Detection of light-induced changes of intracellular ionized calcium concentration in Limulus ventral photoreceptors using arsenazo III. J. Physiol., Lond. 267, 299–320.Google Scholar
Brown, J. E. & Coles, J. A. (1979). Saturation of the response to light in Limulus ventral photoreceptor. J. Physiol., Lond. 296, 373–392.CrossRefGoogle ScholarPubMed
Brown, J. E., Faddis, M. N. & Combs, A. (1990). Guanine nucleotide metabolism in invertebrate phototransduction. Int. Symposium on Signal Transduction in Photoreceptor Cells. Julich, FRG. Abstr. p24.Google Scholar
Brown, J. E., Kaupp, U. B. & Malbon, C. C. (1984 a). 3′, 5′-cyclic adenosine monophosphate and adenylate cyclase in phototransduction by Limulus ventral photoreceptors. J. Physiol., Lond. 353, 523–539.Google Scholar
Brown, J. E. & Lisman, J. E. (1972). An electrogenic sodium pump in Limulus ventral photoreceptor cells. J. gen. Physiol. 59, 720–740.Google Scholar
Brown, J. E. & Lisman, J. E. (1975). Intracellular Ca modulates sensitivity and time scale in Limulus ventral photoreceptors. Nature, Lond. 258, 252–254.Google Scholar
Brown, J. E. & Mote, M. I. (1974). Ionic dependence of reversal voltage of the light response in Limulus ventral photoreceptors. J. gen. Physiol. 63, 337–350.Google Scholar
Brown, J. E. & Rubin, L. J. (1984). A direct demonstration that inositol trisphosphate induces an increase in intracellular calcium in Limulus photoreceptors. Biochim. biophys. Res. Commun. 125, 1137–1142.CrossRefGoogle ScholarPubMed
Brown, J. E. & Rubin, L. J. (1986). Signal transduction: the putative participation of inositol trisphosphates in Limulus photoreceptors. In Fortschritte der Zoologie. Membrane Control, Band 33 (ed. Liittgau, H. C.), pp. 321–331. Stuttgart, New York: Gustav Fischer Verlag.Google Scholar
Brown, J. E., Rubin, L. J., Ghalayini, A. J., Tarver, A. P., Irvine, R. F., Berridge, M. J. & Anderson, R. E. (1984 b). Myo-inositol polyphosphate may be a messenger for visual excitation in Limulus photoreceptors. Nature, Lond. 311, 160–163.Google Scholar
Calhoon, R., Tsuda, M. & Ebrey, G. (1980). A light activated GTPase from octopus photoreceptors. Biochim. biophys. Res. Commun. 94, 1452–1457.Google Scholar
Calman, B. G. & Chamberlain, S. C. (1982). Distinct lobes of Limulus ventral photoreceptors. II. Structure and ultrastructure. J. gen. Physiol. 80, 839–862.Google Scholar
Chinn, K. & Lisman, J. (1984 a). Calcium mediates the light-induced decrease in maintained K+ current in Limulus ventral photoreceptors. J. gen. Physiol. 84, 447–462.Google Scholar
Chinn, K. & Lisman, J. (1984 b). Light reduces the voltage-dependent inward current in Limulus ventral photoreceptors. J. gen. Physiol. 84, 463–473.CrossRefGoogle ScholarPubMed
Classen-Linke, I. & Stieve, H. (1986). The sensitivity of the ventral nerve photoreceptor of Limulus recovers after light adaptation in two phases of dark adaptation. Z. Naturf. 41c, 657–667.CrossRefGoogle Scholar
Cone, R. A. (1973). The internal transmitter model for visual excitation: some quantitative implication. In Biochemistry and Physiology of Visual Pigments (ed. Langer, H.), pp. 275–282. Berlin: Springer-Verlag.Google Scholar
Cooper, A., Dixon, S. F. & Tsuda, M. (1986). Photoenergetics of octopus rhodopsin. Convergent evolution of biological photon counters? Eur. Biophys. J. 13, 195–201.CrossRefGoogle ScholarPubMed
Corson, D. W. & Fein, A. (1980). The pH dependence of discrete wave frequency in Limulus ventral photoreceptors. Brain Res. 193, 558–561.Google Scholar
Corson, D. W. & Fein, A. (1983). Chemical excitation of Limulus photoreceptors. I. Phosphatase inhibitors induce discrete wave production in the dark. J. gen. Physiol. 82, 639–657.Google Scholar
Corson, D. W. & Fein, A. (1987). Inositol 1, 4, 5-trisphosphate induces bursts of calcium release inside limulus ventral photoreceptors. Brain Res. 423, 343–346.Google Scholar
Corson, D. W., Fein, A. & Schmidt, J. (1979). Two effects of phosphodiesterase inhibitors on Limulus ventral photoreceptors. Brain Res. 176, 365–368.Google Scholar
Corson, D. W., Fein, A. & Walthall, W. W. (1983). Chemical excitation of Limulus photoreceptors. II. Vanadate, GTP-γ-S and fluoride prolong excitation by dim flashes of light. J. gen. Physiol. 82, 659–677.Google Scholar
Deckert, A., Helrich, C. S. & Stieve, H. (1991 b). Multiple components in the light-induced current of Limulus ventral photoreceptors. Eur. Biophys. J. (submitted).Google Scholar
Deckert, A., Nagy, K. & Stieve, H. (1991 a). Components of the light-induced macroscopic current in Limulus ventral photoreceptor result from different ion channels. In Synapse-Transmission-Modulation (ed. Eisner, N. and Penzlin, H.). Stuttgart, New York: Georg Thieme Verlag.Google Scholar
Deckert, A. & Stieve, H. (1991). Electrogenic Na+/Ca2+ exchanger, the calcium link between intra- and extracellular space in the Limulus ventral nerve photoreceptor. J. Physiol., Lond. 433, 467–482.Google Scholar
Devary, O., Heichal, O., Blumenfield, A., Cassel, D., Suss, E., Barash, S., Rubinstein, C. T., Minke, B. & Selinger, Z. (1987). Coupling of photoexcited rhodopsin to inositol phospholipid hydrolysis in fly photoreceptors. Proc. natn. Acad. Sci. U.S.A. 84, 3939–3943.Google Scholar
Dirnberger, G., Keiper, W., Schnakenberg, J. & Stieve, H. (1985). Comparison of time constants of single channel patches, quantum bumps and noise analysis in Limulus ventral photoreceptors. J. Membrane. Biol. 83, 39–43.Google Scholar
Dodge, F. A., Knight, B. W. & Toyoda, J. (1968). Voltage noise in Limulus visual cells. Science, Wash. 160, 88–90.Google Scholar
Fain, G. L. & Lisman, J. E. (1981). Membrane conductances of photoreceptors. Prog. Biophys. Molec. Biol. 37, 91–147.Google Scholar
Fein, A. (1986). Blockade of visual excitation and adaptation in Limulus photoreceptors by GDP-ß-S. Science, Wash. 232, 1543–1545.CrossRefGoogle Scholar
Fein, A. & Charlton, J. S. (1977 a). Enhancement and phototransduction in the ventral eye of Limulus. J. gen. Physiol. 69, 553–569.CrossRefGoogle ScholarPubMed
Fein, A. & Charlton, J. S. (1977 b). A quantitative comparison of the effects of intracellular calcium injection and light adaptation on the photoresponse of Limulus ventral photoreceptors. J. gen. Physiol. 70, 591–600.CrossRefGoogle ScholarPubMed
Fein, A. & Corson, D. W. (1982). Internal injection of ATP can reduce discrete wave activity. Biol. Bull. mar. biol. Lab., Woods Hole 163, 395.Google Scholar
Fein, A. & DeVoe, R. D. (1973). Adaptation in the ventral eye of Limulus is functionally independent of the photochemical cycle, membrane potential and membrane resistance. J. gen. Physiol. 61, 273–289.CrossRefGoogle ScholarPubMed
Fein, A. & Lisman, J. (1975). Localized desensitization of Limulus photoreceptors produced by light or intracellular calcium ion injection. Science, Wash. 187, 1094–1096.Google Scholar
Fein, A. & Payne, R. (1989). Phototransduction in Limulus photoreceptors: roles of calcium and inositol trisphosphate. In Facets of Vision (ed. Stavenga, D. G. and Hardie, R. C.), pp. 173–185. Berlin, Heidelberg, New York: Springer-Verlag.Google Scholar
Fein, A., Payne, R., Corson, D. W., Berridge, M. J. & Irvine, R. F. (1984). Photoreceptor excitation and adaptation by inositol 1, 4, 5-trisphosphate. Nature, Lond. 311, 157–160.Google Scholar
Fein, A. & Tsacopoulos, M. (1988). Light-induced oxygen consumption in Limulus ventral photoreceptors does not result from a rise in the intracellular sodium concentration. J. gen. Physiol. 91, 515–527.Google Scholar
Fourtes, M. G. F. & Hodgkin, A. L. (1964). Changes in time scale and sensitivity in the ommatidia of Limulus. J. Physiol., Lond. 172, 239–263.Google Scholar
Fourtes, M. G. F. & Yeandle, S. (1964). Probability of occurence of discrete potential waves in the eye of Limulus. J. gen. Physiol. 47, 443–463.Google Scholar
Goldring, M. A. & Lisman, J. E. (1983). Single photon transduction in Limulus photoreceptors and the Borsellino-Fourtes model. IEEE Trans. Sys. Man. Cybern. SMC 13, 727–731.CrossRefGoogle Scholar
Grzywacz, N. M. & Hillman, P. (1985). Statistical test of linearity of photoreceptor transduction process: Limulus passes, others fail. Proc. natn. Acad. Sci. U.S.A. 82, 232–235.Google Scholar
Grzywacz, N. M. & Hillman, P. (1988). Biophysical evidence that light adaptation in Limulus photoreceptors is due to a negative feedback. Biophys. J. 53, 337–348.Google Scholar
Grzywacz, N. M., Hillman, P. & Knight, B. W. (1988). The quantal source of area supralinearity of flash responses in Limulus photoreceptors. J. gen. Physiol. 91, 659–684.CrossRefGoogle ScholarPubMed
Hagins, W. A. (1972). The visual process: excitatory mechanism in the primary receptor cells. A. Rev. Biophys. Bioengng. 1, 131–158.Google Scholar
Hamill, O. P., Marty, A., Neher, E., Sakmann, B. & Sigworth, F. J. (1981). Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflügers. Arch. 391, 85–100.Google Scholar
Hanani, M. & Hillman, P. (1976). Adaptation and facilitation in the barnacle photoreceptor. J. gen. Physiol. 67, 235–249.Google Scholar
Helrich, C. S., Stieve, H. & Deckert, A. (1988). The reversal potential in Limulus ventral nerve photoreceptor is observed to depend on dark adaptation. In Sense Organs (ed. Eisner, N. and Bart, F. G.), p. 208. Stuttgart, New York: Thieme.Google Scholar
Hille, B. (1984). Ionic Channels of Excitable Membranes. Sinauer Associates Inc. Sunderland, Mass.Google Scholar
Hillman, P., Hochstein, S. & Minke, B. (1983). Transduction in invertebrate photoreceptors: role of pigment bistability. Physiol. Rev. 63, 668–772.Google Scholar
Ivens, I. & Stieve, H. (1984). Influence of the membrane potential on the intracellular light induced Ca2+-concentration change of the Limulus ventral photoreceptor monitored by arsenazo III under voltage clamp conditions. Z. Naturf. 39c, 986–992.CrossRefGoogle Scholar
Jan, L. Y. & Jan, Y. N. (1990). A superfamily of ion channels. Nature, Wash. 345, 672–672.CrossRefGoogle ScholarPubMed
Johnson, E. C., Robinson, P. R. & Lisman, J. E. (1986). Cyclic GMP is involved in the excitation of invertebrate photoreceptors. Nature, Lond. 324, 468–470.Google Scholar
Keiper, W., Schnakenberg, J. & Stieve, H. (1984). Statistical analysis of quantum bump parameters in Limulus ventral photoreceptors. Z. Naturforsch. 39c, 781–790.Google Scholar
Kirkwood, A., Weiner, D. & Lisman, J. E. (1989). An estimate of the number of G regulatory proteins activated per excitated rhodopsin in living Limulus ventral photoreceptors. Proc. natn. Acad. Sci. U.S.A. 86, 3872–3876.Google Scholar
Kraemer, P., Lederhofer, R. & Schnakenberg, J. (1989). A simple explanation for the large and widely differing time exponent of the initial response of Limulus photoreceptors. J. gen. Physiol. 94, 1117–1120.Google Scholar
Lamb, T. D. (1981). The involvement of rod photoreceptors in dark adaptation. Vis. Res. 21, 1773–1782.Google Scholar
Lederhofer, R., Schnakenberg, J. & Stieve, H. (1991). Stochastic treatment of bump latency and temporal overlapping in Limulus ventral photoreceptors. Z. Naturf. (In the Press.)Google Scholar
Leonard, R. J. & Lisman, J. E. (1981). Light modulates voltage-dependent potassium channels in Limulus ventral photoreceptors. Science, Wash. 212, 1273–1275.Google Scholar
Levine, E., Crain, E., Robinson, P. & Lisman, J. (1987). Nontransducing rhodopsin. J. gen. Physiol. 90, 575–586.Google Scholar
Levy, S. & Coles, J. A. (1977). Intracellular pH of Limulus ventral photoreceptors measured with a double barrelled pH microelectrode. Experientia 33, 553–554.Google Scholar
Levy, S. & Fein, A. (1985). Relationship between light sensitivity and intracellular free Ca concentration in Limulus ventral photoreceptors. A quantitative study using Caselective microelectrodes. J. gen. Physiol. 85, 805–841.Google Scholar
Lillywhite, P. G. (1977). Single photon signals and transduction in an insect eye. J. comp. Physiol. 122, 189–200.Google Scholar
Lisman, J. (1985). The role of metarhodopsin in the generation of spontaneous quantum bumps in ultraviolet receptors of Limulus median eye. Evidence for reverse reactions into an active state. J. gen. Physiol. 85, 171–187.Google Scholar
Lisman, J. E. & Bering, H. (1977). Electrophysiological measurements of the number of rhodopsin molecules in single Limulus photoreceptor. J. gen. Physiol. 70, 621–633.CrossRefGoogle Scholar
Lisman, J. E. & Brown, J. E. (1971). Two light-induced processes in the photoreceptor cells of Limulus ventral eye. J. gen. Physiol. 58, 544–561.CrossRefGoogle ScholarPubMed
Lisman, J. E. & Brown, J. E. (1972). The effects of intracellular injection of calcium and sodium ions on the light response of Limulus ventral photoreceptors. J. gen. Physiol. 59, 701–719.Google Scholar
Lisman, J. E. & Brown, J. E. (1975). Light-induced changes of sensitivity in Limulus ventral photoreceptors. J. gen. Physiol. 66, 473–488.Google Scholar
Lisman, J. & Goldring, M. (1985). Early events in visual transduction in Limulus photoreceptors. Neurosci. Res. Suppl. 2S, 101–117.Google Scholar
Lisman, J. E. & Shelin, Y. (1976). Analysis of the rhodopsin cycle in Limulus ventral photoreceptors using the early receptor potential, J. gen. Physiol. 68, 487–501.Google Scholar
Lisman, J. E., Schulmann, S., Sheline, Y. & Brown, P. K. (1981). Properties of the pH-sensitive site that controls the λmax of Limulus metarhodopsin. J. gen. Physiol. 77, 191–203.Google Scholar
Lisman, J. E. & Strong, J. A. (1979). The initiation of excitation and light adaptation in Limulus ventral photoreceptors. J. gen. Physiol. 73, 219–243.Google Scholar
Lisman, J. E., Fain, G. & O'Day, P. M. (1982). Voltage dependent conductances in Limulus ventral photoreceptors. J. gen. Physiol. 79, 187–209.Google Scholar
Maaz, G. & Stieve, H. (1980). The correlation of the receptor potential with the light induced transient increase in intracellular calcium-concentration measured by absorption change of arsenazo III injected into Limulus ventral nerve photoreceptor cell. Biophys. Struct. Mech. 6, 191–208.Google Scholar
Maaz, G., Nagy, K., Stieve, H. & Klomfass, J. (1981). The electrical light response of the Limulus ventral nerve photoreceptor, a superposition of distinct components – observable by variation of the state of light adaptation, J. comp. Physiol. 141, 303–310.Google Scholar
Martinez, J. & Srebro, R. (1976). Calcium and the control of discrete wave latency in the ventral photoreceptor of Limulus. J. Physiol., Lond. 261, 535–562.CrossRefGoogle ScholarPubMed
Meech, R. W. & Brown, H. M. (1976). Invertebrate photoreceptors: a survey of recent experiments on photoreceptors from Balanus and Limulus. Persp. exp. Biol. 1 333–331.Google Scholar
Millecchia, R. & Mauro, A. (1969 a). The ventral photoreceptor of Limulus. II. The basic photoresponse. J. gen. Physiol. 54, 310–330.Google Scholar
Millecchia, R. & Mauro, A. (1969 b). The ventral photoreceptor of Limulus. III. A voltage-clamp study. J. gen. Physiol. 54, 331–351.Google Scholar
Murray, G. C. (1966). Intracellular absorption difference spectrum of Limulus extraocular photolabile pigment. Science, Wash. 154, 1182–1183.Google Scholar
Nagy, K. (1987 a). Evidence for multiple open states of sodium channels in neuroblastoma cells. J. membrane Biol. 96, 251–262.Google Scholar
Nagy, K. (1987 b). Subconductance states of single sodium channels modified by chloramine-T and sea anemone toxin in neuroblastoma cells. Eur. Biophys. J. 5, 129–132.Google Scholar
Nagy, K. (1988). Mechanism of inactivation of single sodium channels after modification by chloramine-T, sea anemone toxin and scorpion toxin. J. membrane Biol. 106, 29–40.Google Scholar
Nagy, K. (1990 a). Kinetic properties of single ion channels activated by light in Limulus ventral nerve photoreceptors. Eur. Biophys. J. 19, 47–54.Google Scholar
Nagy, K. (1990 b). Kinetics of two types of light-activated single channels in Limulus ventral nerve photoreceptors.10th Int. Biophys. Congr.,Vancouver, abstr. p. 481.Google Scholar
Nagy, K. & Stieve, H. (1983). Changes in intracellular calcium ion concentration, in the course of dark adaptation measured by arsenazo III in Limulus photoreceptor. Biophys. Struct. Mech. 9, 207–223.CrossRefGoogle Scholar
Nagy, K. & Stieve, H. (1990 a). Light-activated single channel currents in Limulus ventral photoreceptors. Eur. Biophys. J. 18, 221–224.Google Scholar
Nagy, K. & Stieve, H. (1990 b). Properties of two light-activated channel types in Limulus ventral nerve photoreceptor. Int. Symp. Signal Transduction in Photoreceptor Cells, Jülich, abstr., p. 65.Google Scholar
Nagy, K., Stieve, H., Ivens, I. & Klomfass, J. (1982). Apparent delay between light-induced receptor current and receptor potential in the Limulus ventral nerve photoreceptor. Neurosci. Lett. 32, 149–153.Google Scholar
Nasi, E. (1991). Two light-dependent conductances in Lima rhabdomeric photoreceptors. J. Gen. Physiol. 97, 55–72.Google Scholar
Neher, E. & Sakmann, B. (1976). Single channel currents recorded from membrane of denervated muscle fibres. Nature, Lond. 260, 799–802.Google Scholar
O'Day, P. M. & Gray-Keller, M. P. (1989). Evidence for electrogenic Na+/Ca2+ exchange in Limulus ventral photoreceptors. J. gen. Physiol. 93, 473–492.CrossRefGoogle ScholarPubMed
O'Day, P. M. & Lisman, I. (1985). Octopamine enhances dark-adaptation in Limulus ventral photoreceptors. J. Neurosci. 5, 1490–1496.Google Scholar
O'Day, P. M., Lisman, J. E. & Goldring, M. (1982). Functional significance of voltage-dependent conductances in Limulus ventral photoreceptors. J. gen. Physiol. 79, 211–232.Google Scholar
Patlak, J. B. (1988). Sodium channel subconductance levels measured with a new variance-mean analysis. J. gen. Physiol. 92, 413–430.CrossRefGoogle ScholarPubMed
Payne, R. (1986). Phototransduction by microvillar photoreceptors of invertebrates: mediation of a visual cascade by inositol trisphosphate. Photochem. Photobiophys. 13, 373–397.Google Scholar
Payne, R., Corson, D. W. & Fein, A. (1986 a). Pressure injection of calcium both excites and adapts limulus ventral photoreceptors. J. gen. Physiol. 88, 107–126.Google Scholar
Payne, R., Corson, D. W., Fein, A. & Barridge, M. J. (1986 b). Excitation and adaptation of Limulus ventral nerve photoreceptors by inositol 1, 4, 5 trisphosphate result from a rise in intracellular calcium. J. gen. Physiol. 88, 127–142.Google Scholar
Payne, R. & Fein, A. (1983). Localized adaptation within the rhabdomeral lobe of Limulus ventral photoreceptors. J. gen. Physiol. 81, 767–769.Google Scholar
Payne, R. & Fein, A. (1986 a). Localization of the photocurrent of Limulus ventral nerve photoreceptors using a vibrating probe. Biophys. J. 50, 193–196.Google Scholar
Payne, R. & Fein, A. (1986 b). Initial response of Limulus ventral photoreceptors to bright flashes. Released calcium as a synergist to excitation. J. gen. Physiol. 87, 243–269.Google Scholar
Payne, R. & Fein, A. (1987). Inositol 1, 4, 5 trisphosphate releases calcium from specialized sites within Limulus photoreceptors. J. cell. Biol. 104, 933–937.CrossRefGoogle ScholarPubMed
Payne, R., Flores, M. F. & Fein, A. (1990). Feedback inhibition by calcium limits the release of calcium by inositol trisphosphate in Limulus ventral photoreceptors. Neuron 4, 547–555.Google Scholar
Payne, R., Walz, B., Levy, S. & Fein, A. (1988). The localization of calcium release by inositol trisphosphate in Limulus photoreceptors and its control by negative feedback. Phil. Trans. R. Soc. Lond. B320, 359–379.Google Scholar
Pepose, J. S. & Lisman, J. E. (1978). Voltage-sensitive potassium channels in Limulus ventral photoreceptors. J. gen. Physiol. 71, 101–120.Google Scholar
Rana, R. S. & Hokin, L. E. (1990). Role of phosphoinositides in transmembrane signalling. Physiol. Rev. 70, 115–164.Google Scholar
Rasmussen, H. & Goodman, D. P. B. (1977). Relationship between calcium and cyclic nucleotides in cell activation. Physiol. Rev. 57, 421–509.Google Scholar
Ritchie, J. M. (1973). Energetic aspects of nerve conduction: the relationship between heat production, electrical activity and metabolism. Progr. Biophys. molec. Biol. 26, 149–187.Google Scholar
Robinson, P. R., Wood, S. F., Szuts, E. Z., Fein, A., Hamm, H. E. & Lisman, J. E. (1990). Light-dependent GTP-binding proteins in squid photoreceptors. Biochem. J. 272, 79–85.Google Scholar
Rydqvist, B. & Brown, H. M. (1986). Intracellular free Mg2+ in Balanus photoreceptor measured with eriochrome blue. Ada. physiol. Scand. 127, 499–506.Google Scholar
Saibil, H. R. (1984). A light-stimulated increase of cyclic GMP in squid photoreceptors. FEBS Lett. 168, 213–216.Google Scholar
Schlösser, B. (1990). Einfluss von zyklischen Nukleotiden auf die Dunkeladaptation des ventralen Photorezeptors von Limulus polyphemus. Dissertation, RWTH Aachen.Google Scholar
Schnakenberg, J. (1989). Amplification and latency in photoreceptors: integrated or separated phenomena? Biol. Cybern. 60, 421–437.Google Scholar
Schnakenberg, J. & Keiper, W. (1986). Experimental results and physical ideas towards a model for quantum bumps in photoreceptors. In The molecular mechanism of Photoreception (ed. Stieve, H.), pp. 353–367. Berlin, Heidelberg, New York, Tokio: Springer.Google Scholar
Schnakenberg, J. & Wong, F. (1986). Potentials and limitations of noise analysis of light-induced conductance changes in photoreceptors. (ed. Stieve, H.), pp. 369–387. Berlin, Heidelberg, New York, Tokio: Springer.Google Scholar
Schreibmayer, W., Tritthart, H. A. & Schindler, H. (1989). The cardiac sodium channel shows a regular substrate pattern indicating synchronized activity of several ion pathways instead of one. Biochim. Biophys. Acta 986, 172–186.Google Scholar
Smith, T. G., Stell, W. K., Brown, J. E., Freeman, J. A. & Murray, G. C. (1968). A role for a sodium pump in photoreception in Limulus. Science, Wash, 162, 456–458.Google Scholar
Srebro, R. & Behbehani, M. (1972 a). Light adaptation of discrete waves in the Limulus photoreceptor. J. gen. Physiol. 60, 86–101.Google Scholar
Srebro, R. & Behbehani, M. (1972 b). The thermal origin of spontaneous activity in the Limulus photoreceptor. J. Physiol., Lond. 224, 349–361.Google Scholar
Stern, J., Chinn, K., Bacigalupo, J. & Lisman, J. E. (1982). Distinct lobes of Limulus ventral photoreceptors. I. Functional and anatomical properties of lobes revealed by removal of glial cells. J. gen. Physiol. 80, 825–837.Google Scholar
Stern, J., Chinn, K., Robinson, P. & Lisman, J. (1985). The effect of nucleotides on the rate of spontaneous quantum bumps in Limulus ventral photoreceptors. J. gen. Physiol. 85, 157–169.Google Scholar
Stieve, H. (1986 a). Introduction. In The Molecular Mechanism of Photoreception, Dahlem Konferenzen (ed. Stieve, H.), pp. 1–10. Berlin, Heidelberg, New York: Springer.Google Scholar
Stieve, H. (1986 b). Bumps, the elementary excitatory responses of invertebrates. In The Molecular Mechanism of Photoreception, Dahlem Konferenzen (ed. Stieve, H.), pp. 199–230. Berlin, Heidelberg, New York: Springer.Google Scholar
Stieve, H. & Andre, E. (1984). Octopamine modulates the sensitivity of Limulus ventral photoreceptor. Z. Naturf. 39c, 981–985.Google Scholar
Stieve, H. & Bruns, M. (1980). Dependence of bump rate and bump size in Limulus ventral nerve photoreceptors on light adaptation and calcium concentration. Biophys. Struct. Mech. 6, 271–285.Google Scholar
Stieve, H. & Bruns, M. (1983). Bump latency distribution and bump adaptation of Limulus ventral nerve photoreceptor in varied extracellular calcium concentration. Biophys. Struct. Mech. 9, 323–339.CrossRefGoogle Scholar
Stieve, H. & Klomfass, J. (1983). Distribution and bump latency and bump shape parameters in dependence on adaptation and external Ca2+ concentration in Limulus photoreceptor. Abstr. Jahrestagung, Deutsche Gesellschaft für Biophysik, Neuherberg.Google Scholar
Stieve, H., Pflaum, M., Klomfass, J. & Gaube, H. (1985). Calcium/sodium competition in the gating of light-activated membrane conductance studied by voltage clamp technique in Limulus ventral nerve photoreceptor. Z. Naturforsch. 40c, 278–291.Google Scholar
Stieve, H., Reuss, H., Hennig, H. T. & Klomfass, J. (1990). Single photon evoked events of the ventral nerve photoreceptor cell of Limulus. Facilitation, adaptation and dependence on lowered external calcium. Z. Naturf. (submitted).Google Scholar
Stieve, H. & Schlösser, B. (1989). The light energy dependence of the Limulus photoreceptor current in two defined states of adaptation. Z. Naturf. 44c, 999–1014.Google Scholar
Stieve, H., Schnakenberg, J., Huhn, A. & Reuss, H. (1986). An automatic gain control in the Limulus photoreceptor. In Progress in Zoology. Membrane Control of Cellular activity, vol 33. (ed. Lüttgau, H. C.), pp. 367–376. Stuttgart: Gustav Fischer.Google Scholar
Streb, H., Irvine, R. F., Berridge, M. J. & Schulz, I. (1983). Release of Ca2+ from a non-mitochondrial store in pancreatic acinar cells by inositol 1, 4, 5 trisphosphate. Nature, Lond. 306, 67–69.Google Scholar
Strong, J. & Lisman, J. (1978). Initiation of light-adaptation in barnacle photoreceptors. Science, Wash. 200, 1485–1487.Google Scholar
Tillotson, D. (1979). Inactivation of Ca conductance dependent on entry of Ca ions in molluscan neurons. Proc. natn. Acad. Sci. U.S.A. 76, 1497–1500.Google Scholar
Tsuda, M. (1987). Photoreception and phototransduction in invertebrate photoreceptors. Photochem. Photobiol. 45, 915–931.Google Scholar
Tsuda, M. & Tsuda, T. (1990). Two distinct light regulated G-proteins in octopus photoreceptors. Biochim. biophys. Acta 1052, 204–210.Google Scholar
Vandenberg, C. A. & Montal, M. (1984 a). Light regulated biochemical events in invertebrate photoreceptors. 1. Light-activated guanosine-triphosphate, guanine nucleotide binding and cholera toxin catalysed labelling of squid photoreceptor membranes. Biochemistry 23, 2339–2347.Google Scholar
Vandenberg, C. A. & Montal, M. (1984 b). Light regulated biochemical events in invertebrate photoreceptors. 2. Light-regulated phosphorylation of rhodopsin and phosphoinositides in squid photoreceptor membranes. Biochemistry 23, 2347–2352.Google Scholar
Vuong, T. M., Chabre, M. & Streyer, L. (1984). Millisecond activation of transducin in the cyclic nucleotide cascade of vision. Nature, Lond. 311, 659–661.Google Scholar
Wagner, R., Ryba, N. & Uhl, R. (1989). Calcium regulates the rate of rhodopsin disactivation and the primary amplification step in visual transduction. FEBS Lett. 242, 249–254.Google Scholar
Walz, B. & Baumann, O. (1989). Calcium-sequestering cell organelles: in situ localization, morphological and functional characterization. Progr. Histochem. Cytochem. 20, 1–47.Google Scholar
Walz, B. & Fein, A. (1983). Evidence for calcium-sequestering smooth ER in Limulus ventral photoreceptors. Inv. Ophthalm. Vis. Sci. Suppl. 24, 281.Google Scholar
Wong, F. (1978). Nature of light-induced conductance changes in ventral photoreceptors of Limulus. Nature, Lond. 276, 76–79.Google Scholar
Wong, F., Knight, B. W. & Dodge, F. A. (1980). Dispersion of latencies in photoreceptors of Limulus and the adapting-bump model. J. gen. Physiol. 76, 517–537.Google Scholar
Wong, F., Knight, B. W. & Doge, F. A. (1982). Adapting bump model for ventral photoreceptors of Limulus. J. gen. Physiol. 79, 1089–1113.Google Scholar
Yamamoto, D., Yeh, J. Z. & Narahashi, T. (1984). Voltage-dependent calcium block of normal and tetramethrin-modified single sodium channels. Biophys. J. 45, 337–344.Google Scholar
Yeandle, S. & Spiegler, J. B. (1973). Light-evoked and spontaneous discrete waves in the ventral nerve photoreceptor of Limulus. J. gen. Physiol. 61, 552–571.Google Scholar