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Whole-cell recording of light-evoked photoreceptor responses in a slice preparation of the cuttlefish retina

Published online by Cambridge University Press:  02 August 2005

ABDESSLAM CHRACHRI ,
LISA NELSON  and
RODDY WILLIAMSON
ABDESSLAM CHRACHRI
Affiliation:
School of Biological Sciences, University of Plymouth, Plymouth, PL4 8AA, UK Marine Biological Association of the UK, Citadel Hill, Plymouth PL1 2PB, UK
LISA NELSON
Affiliation:
School of Biological Sciences, University of Plymouth, Plymouth, PL4 8AA, UK Marine Biological Association of the UK, Citadel Hill, Plymouth PL1 2PB, UK
RODDY WILLIAMSON
Affiliation:
School of Biological Sciences, University of Plymouth, Plymouth, PL4 8AA, UK Marine Biological Association of the UK, Citadel Hill, Plymouth PL1 2PB, UK
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Abstract

A new tissue slice preparation of the cuttlefish eye is described that permits patch-clamp recordings to be acquired from intact photoreceptors during stimulation of the retina with controlled light flashes. Whole-cell recordings using this preparation, from the retinas of very young Sepia officinalis demonstrated that the magnitude, latency, and kinetics of the flash-induced photocurrent are closely dependent on the magnitude of the flash intensity. Depolarizing steps to voltages more positive than −40 mV, from a membrane holding potential of −60 mV, induced a transient inward current followed by a larger, more sustained outward current in these early-stage photoreceptors. The latter current resembled the delayed rectifier (IK) already identified in many other nerve cells, including photoreceptors. This current was activated at −30 mV from a holding potential of −60 mV, had a sustained time course, and was blocked in a dose-dependent manner by tetraethylammonium chloride (TEA). The smaller, transient, inward current appeared at potentials more positive than −50 mV, reached peak amplitude at −30 mV and decreased with further depolarization. This current was characterized as the sodium current (INa) on the basis that it was inactivated at holding potentials above −40 mV, was blocked by tetrodotoxin (TTX) and was insensitive to cobalt.

Intracellular perfusion of the photoreceptors, via the patch pipette, demonstrated that U-73122 and heparin blocked the evoked photocurrent in a dose-dependent manner, suggesting the involvement of the phospholipase C (PLC) and inositol 1,4,5-triphosphate (InsP3), respectively, in the phototransduction cascade. Perfusion with cyclic GMP increased significantly the evoked photocurrent, while the inclusion of phorbol-12,13-dibutyrate reduced significantly the evoked photocurrent, supporting the involvement of cGMP and the diacylglycerol (DAG) pathways, respectively, in the cuttlefish transduction process.

Keywords

InvertebrateCephalopodPatch clampPhototransductionInsP3Cyclic-GMP
Type
Research Article
Information
Visual Neuroscience , Volume 22 , Issue 3 , May 2005 , pp. 359 - 370
Copyright
2005 Cambridge University Press

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References

REFERENCES

Bacigalupo, J., Johnson, E.C., Vergara, C., & Lisman, J.E. (1991). Light-dependent channels from excised patches of Limulus ventral photoreceptors are opened by cGMP. Proceeding of the National Academy of Sciences of the U.S.A. 88, 7938–7942.Google Scholar
Bacigalupo, J., Bautista, D.M., Brink, D.L., Hetzer, J.F., & O'Day, P.M. (1995). Cyclic-GMP enhances light-induced excitation and induces membrane currents in Drosophila retinal photoreceptors. Journal of Neuroscience 15, 7196–7200.Google Scholar
Baumann, A., Frings, S., Godde, M., Seifert, R., & Kaupp, U.B. (1994). Primary structure and functional expression of a Drosophila cyclic nucleotide-gated channel present in eyes and antennae. European Molecular Biology Organization Journal 13, 5040–5050.Google Scholar
Bayer, D.S. & Barlow, R.B. (1978). Limulus ventral eye: Physiological properties of photoreceptor cells in an organ culture medium. Journal of General Physiology 72, 539–563.Google Scholar
Bloomquist, B.T., Shortridge, R.D., Schneuwly, S., Perdew, M., Montell, C., Steller, H., Rubin, G., & Pak, W.L. (1988). Isolation of the putative phospholipase C gene of Drosophila, norpA, and its role in phototransduction. Cell 54, 723–733.Google Scholar
Brown, P.K. & Brown, P.S. (1958). Visual pigments of the octopus and cuttlefish. Nature 182, 1288–1290.Google Scholar
Brown, J.E. & Rubin, L.J. (1984). A direct demonstration that inositol-triphosphate induces an increase in intracellular calcium in Limulus photoreceptors. Biochemical and Biophysical Research Communications 125, 1137–1142.Google Scholar
Brown, J.E., Rubin, L.J., Ghalayini, A.J., Tarver, A.P., Irvine, R.F., Berridge, M.J., & Anderson, R.E. (1984). Myo-inositol polyphosphate may be a messenger for visual excitation in Limulus photoreceptors. Nature 311, 160–163.Google Scholar
Brown, J.E., Faddis, M., & Combs, A. (1992). Light does not induce an increase in cyclic GMP content of squid or Limulus photoreceptors. Experimental Eye Research 54, 403–410.Google Scholar
Brown, J.E. & Mote, M.I. (1974). Ionic dependence of reversal voltage of the light response in Limulus ventral photoreceptors. Journal of General Physiology 63, 337–350.Google Scholar
Bui, B.V. & Fortune, B. (2004). Ganglion cell contributions to the rat full-field electroretinogram. Journal of Physiology (London) 555, 153–173.Google Scholar
Chabre, M. & Deterre, P. (1989). Molecular mechanism of visual transduction. European Journal of Biochemistry 179, 255–266.Google Scholar
Chinn, K. & Lisman, J. (1984). Calcium mediates the light-induced decrease in maintained K′ current in Limulus ventral photoreceptors. Journal of General Physiology 84, 447–462.Google Scholar
Clark, R.B. & Duncan, G. (1978). Two components of extracellularly recorded photoreceptor potentials in the cephalopod retina: Differential effects of Na+, K+ and Ca2+. Biophysics of Structure and Mechanism 4, 263–300.Google Scholar
Cobb, C. & Williamson, R. (1999). Ionic mechanisms of phototransduction in photoreceptor cells from the epistellar body of the octopus Eledone cirrhosa. Journal of Experimental Biology 202, 977–986.Google Scholar
Cohen, A.I. (1973). An ultrastructural analysis of the photoreceptors of the squid and their synaptic connections I. Photoreceptive and non-synaptic regions of the retina. Journal of Comparative Neurology 147, 351–378.Google Scholar
Contzen, K., Richter, K.H., & Nagy, K. (1995). Selective inhibition of the phospholipase C pathway blocks one light-activated current component in Limulus photoreceptor. Journal of Comparative Physiology A 177, 601–610.Google Scholar
Dabdoub, A. & Payne, R. (1999). Protein kinase C activators inhibit the visual cascade in Limulus ventral photoreceptors at an early stage. Journal of Neuroscience 19, 10262–10269.Google Scholar
Deckert, A., Nagy, K., Helrich, C.S., & Steive, H. (1992). Three components in the light-induced current of Limulus ventral photoreceptor. Journal of Physiology (London) 453, 69–96.Google Scholar
Dong, C.J., Mcreynolds, J.S., & Qian, H.H. (1990). Time-dependent differential effects of cobalt ions on rod- and cone-driven responses in the isolated frog retina. Visual Neuroscience 4, 359–365.Google Scholar
Dowling, J.E. (1968). Discrete potentials in the dark-adapted eye of the crab Limulus. Nature 217, 28–31.Google Scholar
Duncan, G. & Pynsent, P.B. (1979). An analysis of the waveforms of photoreceptor potentials in the retina of the cephalopod Sepiola atlantica. Journal of Physiology 288, 171–188.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-triphosphate. Nature 311, 157–160.Google Scholar
Fein, A. & Cavar, S. (2000). Divergent mechanisms for phototransduction of invertebrate microvillar photoreceptors. Visual Neuroscience 17, 911–917.Google Scholar
Feng, J., Frank, T.M., & Fein, A. (1991). Excitation of Limulus photoreceptors by hydrolysis-resistant analogs of cGMP and cAMP. Brain Research 552, 291–294.Google Scholar
Frank, T.M. & Fein, A. (1991). The role of the inositol phosphate cascade in visual excitation of invertebrate microvillar photoreceptors. Journal of General Physiology 97, 697–723.Google Scholar
Gallemore, R.P. & Steinberg, R.H. (1991). Cobalt increases photoreceptor-dependent responses of the chick retinal pigment epithelium. Investigative Ophthalmology and Visual Science 32, 3041–3052.Google Scholar
Gomez, M. & Nasi, E. (1994). Blockade of light-sensitive conductance in hyperpolarizing photoreceptors of the scallop. Journal of General Physiology 104, 487–505.Google Scholar
Gomez, M. & Nasi, E. (1998). Membrane current induced by protein kinase C activators in rhabdomeric photoreceptors: Implications for visual excitation. Journal of Neuroscience 18, 5253–5263.Google Scholar
Hall, M.D., Hoon, M.A., Ryba, J.P., Pottinger, J.D.D., Keen, J.N., Saibil, H.R., & Findlay, B.C. (1991). Molecular cloning and primary structure of squid (Loligo forbsei) rhodopsin, a phospholipase C-directed G-protein-linked receptor. Biochemical Journal 274, 35–40.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. Pfügers Archives 391, 85–100.Google Scholar
Hardie, R.C. (1991a). Voltage-sensitive potassium channels in Drosophila photoreceptors. Journal of Neuroscience 11, 3079–3095.Google Scholar
Hardie, R.C. (1991b). Whole-cell recording of the light-induced current in dissociated Drosophila photoreceptors: Evidence for feedback by calcium permeating the light-sensitive channels. Proceedings of the Royal Society B (London) 245, 203–210.Google Scholar
Hardie, R.C & Raghu, P. (1998). Activation of heterologously expressed Drosophila TRPL channels: Ca2+ is not required and Ins(1,4,5)P3 is not sufficient. Cell Calcium 24, 153–163.Google Scholar
Hood, D.C., Frishman, L.J., Saszik, S., & Suresh Viswanathan, S. (2002). Retinal origins of the primate multifocal ERG: Implications for the human response. Investigative Ophthalmology and Visual Science 43, 1673–1685.Google Scholar
Hubbard, R. & St. George, R.C.C. (1958). The rhodopsin system of the squid. Journal of General Physiology 41, 501–528.Google Scholar
Huppertz, B. (1995). Evidence for a cGMP-gated cation channel in photoreceptor cell membranes of Sepia officinalis. Federation of European Biochemical Societies Letters 364, 189–192.Google Scholar
Johnson, E.C., Robinson, P.R., & Lisman, J.E. (1986). Cyclic GMP is involved in the excitation of invertebrate photoreceptors. Nature 324, 468–470.Google Scholar
Kaupp, U.B. & Koch, K.W. (1992). Role of cGMP and Ca2+ in vertebrate photoreceptor excitation and adaptation. Annual Review of Physiology 54, 153–175.Google Scholar
Kishigami, A., Ogasawara, T., Watanabe, Y., Hirata, M., Maeda, T., Hayashi, F., & Tsukahara, Y. (2001). Inositol-1,4,5-triphosphate-binding proteins controlling the phototransduction cascade of invertebrate visual cells. Journal of Experimental Biology 204, 487–493.Google Scholar
Kramer, R.H. & Molokanova, E. (2001). Modulation of cyclic-nucleotide-gated channels and regulation of vertebrate phototransduction. Journal of Experimental Biology 204, 2921–2931.Google Scholar
Leonard, R.J. & Lisman, J.E. (1981). Light modulates voltage-dependent potassium channels in Limulus ventral photoreceptors. Science 212, 1273–1275.Google Scholar
Lisman, J.E. & Brown, J.E. (1972). The effects of intracellular iontophoretic injection of calcium and sodium ions on the light response of Limulus ventral photoreceptors. Journal of General Physiology 59, 701–719.Google Scholar
Lisman, J.E. & Brown, J.E. (1975). Effects of intracellular injections of calcium buffers on light adaptation in Limulus ventral photoreceptors. Journal of General Physiology 66, 489–506.Google Scholar
Lisman, J.E., Fain, G., & O'Day, P. (1982). Voltage-dependent conductances in Limulus ventral photoreceptors. Journal of General Physiology 79, 187–209.Google Scholar
Marcotti, W., Johnson, S.L., Holley, M.C., & Kros, C.J. (2003). Developmental changes in the expression of potassium currents of embryonic, neonatal and mature mouse inner hair cells. Journal of Physiology (London) 548, 383–400.Google Scholar
Mojet, M.H. (1993). Dual role for extracellular calcium in blowfly phototransduction. Journal of Comparative Physiology A 173, 335–346.Google Scholar
Naef, A. (1928). Cephalopoda: Embryology. Enfield, New Hampshire: Science Publishers, Inc. Vol. II, pp. 461.
Nagy, K. & Contzen, K. (1997). Inhibition of phospholipase C by U-73122 blocks one component of the receptor current in Limulus photoreceptors. Visual Neuroscience 14, 995–998.Google Scholar
Nasi, E. (1991a). Two light-dependent conductances in Lima rhabdomeric photoreceptors. Journal of General Physiology 97, 55–72.Google Scholar
Nasi, E. (1991b). Whole-cell clamp of dissociated photoreceptors from the eye of Lima scabra. Journal of General Physiology 97, 35–54.Google Scholar
Nasi, E. & Gomez, M.P. (1992). Electrophysiological recordings in solitary photoreceptors from the retina of squid, Loligo pealei. Visual Neuroscience 8, 349–358.Google Scholar
Neher, E. (1992). Correction for liquid junction potentials in patch clamp experiments. Methods in Enzymology 207, 123–131.Google Scholar
Nelson, L. (2003). An investigation of the phototransduction cascade and temporal characteristics of the retina of the cuttlefish, Sepia officinalis. Ph.D. Thesis, University of Plymouth.
O'Day, P.M, Lisman, J.E., & Goldring, M. (1982). Functional significance of voltage dependent conductances in Limulus ventral photoreceptors. Journal of General Physiology 79, 211–232.Google Scholar
Ovchinnikov, Yu.-A., Abdulaev, N.G., Zolotarev, A.S., Artamonov, I.D., Bespalov, I.A., Dergachev, A.E., & Tsuda, M. (1988). Octopus rhodopsin. Amino acid sequence deduced from cDNA. Federation of European Biochemical Societies Letters 232, 69–72.Google Scholar
Payne, R. (1990). Dynamics of the release of calcium by light and inositol 1,4,5-triphosphate in Limulus ventral photoreceptors. In Transduction in Biological Systems, ed. Hilgado, C., Bacigalupo, J., Jaimovich, E. & Vergara, J., pp. 9–25. New York: Plenum Publishing Corporation.
Payne, R., Corson, D.W., Fein, A., & Berridge, M.J. (1986). Excitation and adaptation of Limulus ventral photoreceptors by inositol 1,4,5-trisphosphate result from a rise in intracellular calcium. Journal of General Physiology 88, 127–142.Google Scholar
Payne, R., Walz, B., Levy, S., & Fein, A. (1988). The localization of calcium release by inositol triphosphate in Limulus photoreceptors and its control by negative feedback. Philosophical Transactions Royal Society B 320, 359–379.Google Scholar
Peretz, A., Abitbol, I., Sobko, A., Wu, C., & Attali, B. (1998). A Ca2+/Calmodulin-dependent protein kinase modulates Drosophila photoreceptor K+ currents: A role in shaping the photoreceptor potential. Journal of Neuroscience 18, 9153–9162.Google Scholar
Piccoli, G., Gomez, M., & Nasi, E. (2002). Role of protein kinase C in light adaptation of molluscan microvillar photoreceptors. Journal of Physiology 543, 481–494.Google Scholar
Pinto, L.H. & Brown, J.E. (1977). Intracellular recordings from photoreceptors of the squid (Loligo pealeii). Journal of Computational Physiology A 122, 241–250.Google Scholar
Ranganathan, R., Malicki, D.M., & Zuker, C.S. (1995). Signal transduction in Drosophila photoreceptors. Annual Review of Neuroscience 18, 283–317.Google Scholar
Roebroek, J.G.H. & Stavenga, D.C. (1990). Insect pupil mechanisms. IV. Spectral characteristics and light intensity dependence in the blowfly Calliphora erythrocephala. Journal of Comparative Physiology A 166, 537–543.Google Scholar
Saibil, H.R. (1984). A light-stimulated increase of cyclic GMP in squid photoreceptors. Federation of European Biochemical Societies Letters 168, 213–216.Google Scholar
Sakakibara, M., Inoue, H., & Yoshioka, T. (1998). Evidence for the involvement of inositol trisphosphate but not cyclic nucleotides in visual transduction in Hermissenda eye. Journal of Biological Chemistry 273, 20795–20801.Google Scholar
Schneeweis, D.M. & Schnapf, J.L. (1999). The photovoltage of macaque cone photoreceptors: Adaptation, noise, and kinetics. Journal of Neuroscience 19, 1203–1216.Google Scholar
Seidou, M., Ohtsu, K., Yamasia, Z., Narita, K., & Kito, Y. (1993). The nucleotide content of the octopus photoreceptor cells. No changes in the octopus retina immediately following an intense light flash. Zoological Science 10, 275–279.Google Scholar
Smith, D.P., Ranganathan, R., Hardy, R.W., Marx, J., Tsuchida, T., & Zuker, C.S. (1991). Photoreceptor deactivation and retinal degeneration mediated by a photoreceptor-specific protein kinase C. Science 254, 1478–1484.Google Scholar
Stryer, L. (1986). Cyclic GMP cascade of vision. Annual Review of Neuroscience 9, 87–119.Google Scholar
Ukhanov, U. & Walz, B. (2001). The phosphoinositide signaling cascade is involved in photoreception in the leech Hirudo medicinalis. Journal of Comparative Physiology A 186, 1171–1183.Google Scholar
Walz, B., Zimmermann, B., & Ukhanov, K. (2000). Light-dependent repetitive Ca2+ spikes induced by extracellular application of neomycin in honeybee drone photoreceptors. Journal of Comparative Physiology A 5, 497–503.Google Scholar
Weckstrom, M., Hardie, R.C., & Laughlin, S.B. (1991). Voltage-activated potassium channels in blowfly photoreceptors and their role in light adaptation. Journal of Physiology (London) 440, 635–657.Google Scholar
Weeks, R.I. & Duncan, G. (1974). Photoreception by a cephalopod retina: Response dynamics. Experimental Eye Research 19, 493–509.Google Scholar
Wood, S.F., Szuts, E.Z., & Fein, A. (1989). Inositol triphosphate production in squid photoreceptors. Activation by light, aluminum fluoride, and guanine nucleotides. Journal of Biological Chemistry 264, 12970–12976.Google Scholar
Wulff, V.J. & Mendez, C. (1973). Effect of manganous chloride and tetrodotoxin on Limulus lateral eye retinular cell. Vision Research 13, 2327–2333.Google Scholar
Yamamoto, T., Tasaki, K., Sugawara, Y., & Tonosaki, A. (1965). The fine structure of octopus retina. Journal of Cell Biology 25, 345–359.Google Scholar
Yarfitz, S. & Hurley, J.B. (1994). Transduction mechanisms of vertebrate and invertebrate photoreceptors. Journal of Biological Chemistry 269, 14329–14332.Google Scholar
Zonana, H.V. (1961). Fine structure of the squid retina. Johns Hopkins Hospital Bulletin 109, 185–205.Google Scholar