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Photoreceptor cells dissociated from the compound lateral eye of the horseshoe crab, Limulus polyphemus, II: Function

Published online by Cambridge University Press:  02 June 2009

W. J. Brad Hanna ,
Edwin C. Johnson ,
Deborah Chaves  and
George H. Renninger
W. J. Brad Hanna
Affiliation:
Biophysics Interdepartmental Group, Department of Physics, University of Guelph, Guelph, Ontario, Canada
Edwin C. Johnson
Affiliation:
Department of Physiology, Marshall University School of Medicine, Huntington
Deborah Chaves
Affiliation:
Biophysics Interdepartmental Group, Department of Physics, University of Guelph, Guelph, Ontario, Canada
George H. Renninger
Affiliation:
Biophysics Interdepartmental Group, Department of Physics, University of Guelph, Guelph, Ontario, Canada
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Abstract

A combination of enzymatic digestions and mechanical disruption was used to isolate photoreceptor cells from the compound lateral eye of the horseshoe crab, Limulus polyphemus. The cells were maintained in a culture medium and tested for function using whole-cell and cell-attached patch configurations of the gigaseal technique. The cells dissociated from the eye generated spontaneous voltage and current bumps in the dark, and depolarized in a graded fashion to increasing intensities of light over several decades, producing responses similar to those of cells in vivo. Currents evoked during voltage clamp were similar to those in ventral photoreceptor cells of Limulus, although transient currents in the dark- and light-activated currents were smaller in isolated lateral eye cells, perhaps because of the slow speed and spatial nonuniformity of the clamp in these large cells. In addition to isolated cells, dissociation of the compound eye produced small clusters of cells and isolated ommatidia which were also tested for function. Comparison of the electrical characteristics of isolated cells with those of cells in small clusters and in their ommatidial matrix suggests that the electrical junctions normally connecting photoreceptor cells within an ommatidium are functional in the latter groups, but not in isolated cells. Cell-attached patches of rhabdomeral membrane of isolated cells contained light-activated channels, resembling those observed in ventral photoreceptor cells, but no voltage-activated channels. Similar patches of arhabdomeral membrane contained voltage-activated channels, but no light-activated channels. We conclude that this preparation is suitable for studies of processes involved in generating the light response in invertebrate photoreceptor cells.

Keywords

Isolated invertebrate photoreceptor cellsWhole-cell recordingsPatch clampReceptor potentialRhabdomeral- and arhabdomeral-segment ion channels
Type
Research Articles
Information
Visual Neuroscience , Volume 10 , Issue 4 , July 1993 , pp. 609 - 620
Copyright
Copyright © Cambridge University Press 1993

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References

Adolph, A.R. (1964). Spontaneous slow potential fluctuations in the Limulus photoreceptor. Journal of General Physiology 48, 297–322.CrossRefGoogle ScholarPubMed
Bacigalupo, J. & Lisman, J.E. (1983). Single-channel currents activated by light in Limulus ventral photoreceptors. Nature 304, 268–270.CrossRefGoogle ScholarPubMed
Barlow, R.B. Jr, & Kaplan, E. (1977). Properties of visual cells in the lateral eye of Limulus in situ. Intracellular recordings. Journal of General Physiology 69, 203–220.CrossRefGoogle ScholarPubMed
Barlow, R.B. Jr, Bolanowski, S.J. Jr, & Brachman, M.L. (1977). Efferent optic nerve fibers mediate circadian rhythms in the Limulus eye. Science 197, 86–89.CrossRefGoogle ScholarPubMed
Barlow, R.B. Jr, Chamberlain, S.C. & Levinson, J.Z. (1980). Limulus brain modulates the structure and function of the lateral eyes. Science 210, 1037–1039.CrossRefGoogle ScholarPubMed
Barlow, R.B. Jr, (1983). Circadian rhythms in the Limulus visual system. Journal of Neuroscience 3, 856–870.CrossRefGoogle ScholarPubMed
Barlow, R.B. Jr, Kaplan, E., Renninger, G.H. & Saito, T. (1987). Circadian rhythms in Limulus photoreceptors, 1. Intracellular studies. Journal of General Physiology 89, 353–378.CrossRefGoogle Scholar
Bass, L. & Moore, N.J. (1970). An electrochemical model for depolarization of a retinula cell of Limulus by a single photon. Biophysical Journal 10, 1–19.CrossRefGoogle ScholarPubMed
Battelle, B.-A. (1980). Neurotransmitter candidates in the visual system of Limulus polyphemus: Synthesis and distribution of octopamine. Vision Research 20, 911–922.CrossRefGoogle ScholarPubMed
Battelle, B.-A., Evans, J.A. & Chamberlain, S.C. (1982). Efferent fibers to Limulus eyes synthesize and release octopamine. Science 216, 1250–1252.CrossRefGoogle Scholar
Battelle, B.-A. & Evans, J. (1984). Octopamine release from centrifugal fibers of the Limulus peripheral visual system. Journal of Neurochemistry 42, 71–79.CrossRefGoogle ScholarPubMed
Battelle, B.-A. (1991). Regulation of retinal functions by octopaminergic efferent neurons in Limulus. In Progress in Retinal Research, Vol. 10, ed. Osborne, N. & Chader, J., pp. 333–355. Oxford, England: Pergamon Press.Google Scholar
Bayer, D.S. & Barlow, R.B. Jr, (1978). Limulus ventral eye: Physiological properties of photoreceptor cells in organ culture medium. Journal of General Physiology 72, 539–564.CrossRefGoogle ScholarPubMed
Behrens, M.E. & Wulff, V.J. (1965). Light-initiated responses of retinula and eccentric cells in the Limulus lateral eye. Journal of General Physiology 48, 1081–1093.CrossRefGoogle ScholarPubMed
Borsellino, A., Fuortes, M.G.F. & Smith, T.G. (1965). Visual responses in Limulus. Cold Spring Harbor Symposia on Quantitative Biology 30, 429–443.CrossRefGoogle ScholarPubMed
Brown, J.E., Harary, H.H. & Waggoner, A. (1979). Isopotentiality and an optical determination of series resistance in Limulus ventral photoreceptors. Journal of Physiology 296, 357–372.CrossRefGoogle Scholar
Cahill, G.M. & Besharse, J.C. (1992 a). Light-sensitive melatonin synthesis by Xenopus photoreceptors after destruction of the inner retina. Visual Neuroscience 8, 487–490.CrossRefGoogle ScholarPubMed
Cahill, G.M. & Besharse, J.C. (1992 b). Circadian rhythms of melatonin production by isolated photoreceptor layers from Xenopus Investigative Ophthalmology and Visual Science (Suppl.) 33, 739.Google Scholar
Calman, B.G. & Chamberlain, S.C. (1982). Distinct lobes of Limulus ventral photoreceptors. II. Structure and ultrastructure. Journal of General Physiology 80, 839–862.CrossRefGoogle ScholarPubMed
Chamberlain, S.C. & Barlow, R.B. Jr, (1977). Morphological correlates of efferent circadian activity and light adaptation in the Limulus lateral eye. Biological Bulletin 153, 418–419.Google Scholar
Chamberlain, S.C. & Barlow, R.B. Jr, (1984). Transient membrane shedding in Limulus photoreceptors: Control mechanisms under natural lighting. Journal of Neuroscience 4, 2792–2810.CrossRefGoogle ScholarPubMed
Chamberlain, S.C. & Fiacco, P.A. (1985). Models of circadian changes in Limulus ommatidia: Calculation of changes in acceptance angle, quantum catch, and quantum gain Investigative Ophthalmology and Visual Science (Suppl.) 26, 340.Google Scholar
Chamberlain, S.C. & Barlow, R.B. Jr, (1987). Control of structural rhythms in the lateral eye of Limulus: Interactions of light and efferent inputs. Journal of Neuroscience 7, 2135–2144.CrossRefGoogle Scholar
Cohen, H.A. (1973). Quantitative aspects of eccentric cell dendrite of the lateral eye of Limulus. Journal of Neurocytology 2, 429–439.CrossRefGoogle ScholarPubMed
DeVries, S.H. & Schwartz, E.A. (1992). Hemi-gap-junction channels in solitary horizontal cells of the catfish retina. Journal of Physiology 445, 201–230.CrossRefGoogle ScholarPubMed
Dowling, J.E. (1968). Discrete potentials in the dark-adapted eye of Limulus. Nature 217, 28–31.CrossRefGoogle Scholar
Fahrenbach, W.H. (1969). The morphology of the eyes of Limulus, II. Ommatidia of the compound eye. Zeitschrift für Zellforschung und Mikroskopische Anatomie 93, 451–483.CrossRefGoogle ScholarPubMed
Fahrenbach, W.H. (1970). The morphology of the Limulus visual system, III. The lateral rudimentary eye. Zeitschrift für Zellforschung und Mikroskopische Anatomie 105, 303–316.CrossRefGoogle Scholar
Fahrenbach, W.H. (1975). The visual system of the horseshoe crab Limulus polyphemus. International Review of Cytology 41, 283–349.Google ScholarPubMed
Fahrenbach, W.H. (1981). The morphology of the horseshoe crab (Limulus polyphemus) visual system. VII. Innervation of photoreceptor neurons by neurosecretory efferents. Cell and Tissue Research 216, 655–659.CrossRefGoogle ScholarPubMed
Fuortes, M.G.F. & Yeandle, S. (1964). Probability of occurrence of discrete potential waves in the eye of Limulus. Journal of General Physiology 47, 443–463.CrossRefGoogle ScholarPubMed
Gribakin, F.G. (1990). Sensornye retseptory: Evolyutsiya ionnogo okruzheniya retseptornoi membrany. Zhurnal Evolyutsionnoi Biokhimii Fiziologii 26, 574–580. Translation from Russian (1991). Sensory receptors: Evolution of the ionic environment of receptor membranes. Journal of Evolutionary Biochemistry and Physiology 26, 445–449.Google Scholar
Gribakin, F.G. (1992). Potassium in the ionic environment of the receptor membrane of sensory receptors: Why? Sensorniye Systemy 6(2), 5–14.Google Scholar
Hardie, R.C. (1991). Voltage-sensitive potassium channels in Drosophila photoreceptors. Journal of Neuroscience 11, 3079–3095.CrossRefGoogle ScholarPubMed
Hardie, R.C., Voss, D., Pongs, O. & Laughlin, S.B. (1991). Novel potassium channels encoded by the Shaker locus in Drosophila photoreceptors. Neuron 6, 477–486.CrossRefGoogle ScholarPubMed
Jinks, R.N., Hanna, W.J.B., Renninger, G.H. & Chamberlain, S.C. (1993). Photoreceptor cells dissociated from the compound lateral eye of the horseshoe crab, Limulus polyphemus, I: Structure and ultrastructure. Visual Neuroscience 10, 597–607.CrossRefGoogle ScholarPubMed
Johnson, E.C., Robinson, P.R. & Lisman, J.E. (1986). Cyclic GMP is involved in the excitation of invertebrate photoreceptors. Nature 324, 468–470.CrossRefGoogle ScholarPubMed
Johnson, E.C., Bacigalupo, J., Vergara, C. & Lisman, J.E. (1991). Multiple conductance states of the light-activated channel of Limulus ventral photoreceptors: Alteration of conductance states during light. Journal of General Physiology 97, 1187–1205.CrossRefGoogle ScholarPubMed
Johnson, E.C. & Bacigalupo, J. (1992). Spontaneous activity of the light-dependent channel irreversibly induced in excised patches from Limulus ventral photoreceptors. Journal of Membrane Biology 130, 33–47.CrossRefGoogle ScholarPubMed
Kaplan, E., Barlow, R.B. Jr, Renninger, G.H. & Purpura, K. (1990). Circadian rhythms in Limulus photoreceptors, II. Quantum bumps. Journal of General Physiology 96, 665–685.CrossRefGoogle ScholarPubMed
Kass, L. & Renninger, G.H. (1988). Circadian change in function of Limulus ventral photoreceptors. Visual Neuroscience 1, 3–11.CrossRefGoogle ScholarPubMed
Kass, L., Pelletier, J.L., Renninger, G.H. & Barlow, R.B. Jr, (1988). Efferent neurotransmission of circadian rhythms in Limulus lateral eye, II. Intracellular recordings in vitro. Journal of Comparative Physiology A 164, 95–105.CrossRefGoogle ScholarPubMed
Kass, L., Renninger, G.H., Zhang, H.-J. & Pelletier, J.L. (1990). Whole-cell recordings from Limulus ventral photoreceptors Investigative Ophthalmology and Visual Science (Suppl.) 31, 389.Google Scholar
Kass, L., Pelletier, J.L. & Zhang, H.-J. (1991). Circadian clock modulates light-activated conductances and quantal bumps in Limulus ventral photoreceptors Investigative Ophthalmology and Visual Science (Suppl.) 32, 672.Google Scholar
Kass, L., & Zhang, H.-J. (1992). Clock controls gain in Limulus photoreceptor by changing voltage-dependent conductances Investigative Ophthalmology and Visual Science (Suppl.) 33, 1327.Google Scholar
Kass, L., Renninger, G.H., Zhang, H.-J., Russell, M. & Pelletier, J.L. (1993). Whole-cell recording from Limulus ventral photoreceptor cells (in preparation).Google Scholar
Kier, C.K. & Chamberlain, S.C. (1990). Dual controls for screening pigment movement in photoreceptors of the Limulus lateral eye: Circadian efferent input and light. Visual Neuroscience 4, 237–255.CrossRefGoogle ScholarPubMed
Lasansky, A. (1967). Cell junctions in ommatidia of Limulus. Journal of Cell Biology 33, 365–383.CrossRefGoogle ScholarPubMed
Lisman, J.E., Fain, G.L. & O’Day, P.M. (1982). Voltage-dependent conductances in Limulus ventral photoreceptors. Journal of General Physiology 79, 187–209.CrossRefGoogle ScholarPubMed
Millecchia, R. & Mauro, A. (1969 a). The ventral photoreceptor cells of Limulus, II. The basic photoresponse. Journal of General Physiology 54, 310–330.CrossRefGoogle ScholarPubMed
Millecchia, R. & Mauro, A. (1969 b). The ventral photoreceptor cells of Limulus, III. A voltage-clamp study. Journal of General Physiology 54, 311–351.Google Scholar
Nagy, K. & Stieve, H. (1990). Light-activated single channel current in Limulus ventral photoreceptors. European Biophysics Journal 18, 221–224.CrossRefGoogle Scholar
Nagy, K. (1991). Biophysical processes in invertebrate photoreceptors: Recent progress and a critical overview based on Limulus photoreceptors. Quarterly Review of Biophysics 24, 165–226.CrossRefGoogle Scholar
Nasi, E. (1991). Whole-cell clamp of dissociated photoreceptors from the eye of Lima scabra. Journal of General Physiology 97, 35–54.CrossRefGoogle ScholarPubMed
Nasi, E. & Gomez, M. (1992). Electrophysiological recordings in solitary photoreceptors from the retina of squid, Loligo pealei. Visual Neuroscience 8, 349–358.CrossRefGoogle ScholarPubMed
Neher, E. (1992). Ion channels for communication between and within cells. Science 256, 498–502.CrossRefGoogle ScholarPubMed
O’Day, P.M. (1991). Sodium-calcium exchange in invertebrate photoreceptors. Annals of the New York Academy of Sciences 639, 285–299.CrossRefGoogle ScholarPubMed
O’Day, P.M. & Lisman, J.E. (1985). Octopamine enhances dark adaptation in Limulus ventral photoreceptors. Journal of Neuroscience 5, 1490–1496.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Ogden, D.C. & Stanfield, P.R. (1987). Introduction to single channel recording. In Microelectrode Techniques, ed. Standen, N.B., Gray, P.T.A. & Whittaker, M.J., pp. 63–81. Cambridge, England: Company of Biologists, Ltd.Google Scholar
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.CrossRefGoogle ScholarPubMed
Phillips, C.L., Bacigalupo, J. & O’Day, P.M. (1992). Inward rectification in Limulus ventral photoreceptors. Visual Neuroscience 8, 19–25.CrossRefGoogle ScholarPubMed
Pierce, M.E., Sheshbaradaran, H., Zhang, S., Applebury, M.I. & Takahashi, J.S. (1992). Circadian regulation of red cone opsin gene expression in embryonic photoreceptors in retinal cell culture Investigative Ophthalmology and Visual Science (Suppl.) 33, 1398.Google Scholar
Ranganathan, R., Harris, G.L., Stevens, C.F. & Zuker, C.S. (1991). A Drosophila mutant defective in extracellular calcium-dependent photoreceptor deactivation and rapid desensitization. Nature 354, 230–232.CrossRefGoogle ScholarPubMed
Renninger, G.H., Kaplan, E. & Barlow, R.B. Jr, (1984). A circadian clock increases the gain of photoreceptor cells of the Limulus lateral eye. Biological Bulletin 167, 532.Google Scholar
Renninger, G.H., Kass, L., Pelletier, J.L. & Schimmel, R. (1988). The eccentric cell of the Limulus lateral eye: Encoder of circadian changes in visual responses. Journal of Comparative Physiology A 163, 259–270.CrossRefGoogle Scholar
Renninger, G.H., Schimmel, R. & Farrell, C.A. (1989). Octopamine modulates function in the Limulus lateral eye. Visual Neuroscience 3, 83–94.CrossRefGoogle ScholarPubMed
Renninger, G.H. (1990). Photoreceptor cells dissociated from the Limulus lateral eye Investigative Ophthalmology and Visual Science (Suppl.) 31, 389.Google Scholar
Sakmann, B. (1992). Elementary steps in synaptic transmission revealed by currents through single ion channels. Science 256, 503–512.CrossRefGoogle ScholarPubMed
Smith, T.G., Baumann, F. & Fuortes, M.G.F. (1965). Electrical connections between visual cells in the ommatidium of Limulus. Science 147, 1446–1448.CrossRefGoogle ScholarPubMed
Smith, T.G. & Baumann, F. (1969). The functional organization within the ommatidium of the lateral eye of Limulus. In Mechanisms of Synaptic Transmission (Progress of Brain Research, Vol. 31), ed. Akert, K. & Waser, P.G., pp. 313–349. Amsterdam: Elsevier.CrossRefGoogle Scholar
Smotherman, M.S. & Kass, L. (1992). cAMP and PKA mediate circadian rhythms in photoreceptor function of Limulus Investigative Ophthalmology and Visual Science (Suppl.) 33, 1035.Google Scholar
Stern, J.H. & Lisman, J.E. (1982). Internal dialysis of Limulus ventral photoreceptors. Proceedings of the National Academy of Sciences of the U.S.A. 79, 7580–7584.CrossRefGoogle ScholarPubMed
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. Journal of General Physiology 80, 825–837.CrossRefGoogle ScholarPubMed
Stieve, H. & André, E. (1984). Octopamine modulates the sensitivity of Limulus ventral photoreceptors. Zeitschrift für Naturforschung 39c, 981–985.CrossRefGoogle Scholar
Weckström, M., Hardie, R.C. & Laughlin, S.B. (1991). Voltage-activated potassium channels in blowfly photoreceptors and their role in light adaptation. Journal of Physiology 440, 635–657.CrossRefGoogle ScholarPubMed
Yeandle, S.S. (1958). Evidence of quantized slow potentials in the eye of Limulus. American Journal of Ophthalmology 46(3), Part 2, 82–87.Google Scholar
Zhang, H.-J. & Kass, L. (1993). Mechanism for circadian clock control of photoreceptor gain in Limulus (in preparation).Google Scholar
Zhang, H.-J., Kass, L., Pelletier, J.K. & Renninger, G.H. (1990). Modulation of voltage-dependent conductances in Limulus ventral photoreceptors by octopamine and forskolin Investigative Ophthalmology and Visual Science (Suppl.) 31, 389.Google Scholar
Zhang, H.-J. (1991). Modulation of photoreceptor conductances by a circadian clock in Limulus. Ph.D. Thesis. University of Maine, Orono, Maine.Google Scholar