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Different ionic conductances are modulated during the late receptor potential and the prolonged depolarizing afterpotential in Hermissenda type A photoreceptors

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Abstract

Wavelength-dependent, bistable phenomena were found in the receptor potential of Hermissenda crassicornis type A photoreceptors. Short exposure to blue light induced a prolonged depolarizing afterpotential (PDA) following the cessation of the light stimulus. Stronger adaptation to blue light, as caused by prolonged exposure and/or high intensity stimulation, effected a reduction in the early depolarizing transient of the late receptor potential (LRP) as elicited by subsequent stimuli. Vast separation of LRP emergence and PDA emergence could be obtained in photoreceptors in which a strong cancellation of the LRP was accomplished but a PDA still emerged after cessation of the light stimulus. Short exposure to yellow light cancelled the PDA, and stronger adaptation restored the LRP (opposite effect to blue light). The initial depolarizing part of the LRP had earlier been demonstrated to be mediated by the lightdependent increase of an inward conductance. In contrast, in this study the PDA was found to be accompanied by the reduction of an outward conductance, most likely a K+ conductance. A bistable photopigment system is thought to control the bistable receptor potential phenomenology by regulating the different membrane conductances during the LRP and the PDA.

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Abbreviations

LRP:

late receptor potential

PDA:

prolonged depolarizing afterpotential

PHA:

prolonged hyperpolarizing afterpotential

References

  • Alkon DL (1979) Voltage-dependent calcium and potassium ion conductances: a contingency mechanism for an associative learning model. Science 205:810–816

    Google Scholar 

  • Alkon DL, Sakakibara M (1985) Calcium activates and inactivates a photoreceptor soma potassium current. Biophys J 48:983–995

    Google Scholar 

  • Alkon DL, Shoukimas JJ, Heldman E (1982) Calcium-mediated decrease of voltage-dependent potassium current. Biophys J 40:245–250

    Google Scholar 

  • Alkon DL, Farley J, Sakakibara M, Hay B (1984) Voltage dependent calcium and calcium-activated potassium currents of a molluscan photoreceptor. Biophys J 46:606–614

    Google Scholar 

  • Alkon DL, Naito S, Kubota M, Chen C, Bank B, Smallwood J, Gallant P, Rasmussen H (1988) Regulation of Hermissenda K+ channels by cytoplasmic and membrane-associated C-kinase. J Neurochem 51:903–917

    Google Scholar 

  • Baumann F, Hadjilazaro B (1972) A depolarizing aftereffect of intense light in the drone visual receptor. Vision Res 12:17–31

    Google Scholar 

  • Blumenfeld A, Erusalimsky J, Heichal O, Selinger Z, Minke B (1985) Light-activated guanosinetriphosphatase in Musca eye membranes resembles the prolonged depolarizing afterpotential in photoreceptor cells. Proc Natl Acad Sci USA 82:7116–7120

    Google Scholar 

  • Brown HM, Cornwall MC (1975) Spectral correlates of a quasi-stable depolarization in barnacle photoreceptor following red light. J Physiol (Lond) 248:555–578

    Google Scholar 

  • Cornwall MC, Gorman ALF (1979) Contribution of calcium and potassium permeability changes to the off response of scallop hyperpolarizing photoreceptors. J Physiol (Lond) 291:207–232

    Google Scholar 

  • Detwiler PB (1976) Multiple light-evoked conductance changes in the photoreceptors of Hermissenda crassicornis. J Physiol (Lond) 256:691–708

    Google Scholar 

  • Farley J, Auerbach S (1986) Protein kinase C activation induces conductance changes in Hermissenda photoreceptors like those seen in associative learning. Nature 319:220–223

    Google Scholar 

  • Gorman ALF, McReynolds JS (1978) Ionic effects on the membrane potential of hyperpolarizing photoreceptors in scallop retina. J Physiol (Lond) 275:345–355

    Google Scholar 

  • Grossman Y, Schmidt JA, Alkon DL (1981) Calcium-dependent potassium conductance in the photoresponse of a nudibranch mollusk. Comp Biochem Physiol 68A:487–494

    Google Scholar 

  • Hadjilazaro B, Baumann F (1968) Afterpotentials of the visual cell of the honeybee drone. Helv Physiol Pharmacol Acta 26:CR351-CR352

    Google Scholar 

  • Hamdorf K (1979) The physiology of invertebrate visual pigments. In: Autrum H (ed) Handbook of sensory physiology Vol VII/6A: Comparative physiology and evolution of vision in invertebrates. Springer, Berlin Heidelberg New York, pp 145–224

    Google Scholar 

  • Hamdorf K, Razmjoo S (1979) Photoconvertible pigment states and excitation in Calliphora; the induction and properties of the prolonged depolarizing afterpotential. Biophys Struct Mech 5:137–161

    Google Scholar 

  • Hamdorf K, Rosner G (1973) Adaptation und Photoregeneration im Fliegenauge. J Comp Physiol 86:281–292

    Google Scholar 

  • Hamdorf K, Gogala M, Schwemer J (1971) Beschleunigung der “Dunkeladaptation” eines UV-Rezeptors durch sichtbare Strahlung. Z Vergl Physiol 75:189–199

    Google Scholar 

  • Hamdorf K, Paulsen R, Schwemer J (1973) Photoregeneration and sensitivity control of photoreceptors in invertebrates. In: Langer H (ed) Biochemistry and physiology of visual pigments. Springer, Berlin Heidelberg New York, pp 155–166

    Google Scholar 

  • Hardie RC (1991) Whole-cell recordings of the light induced current in dissociated Drosophila photoreceptors: evidence for feedback by calcium permeating the light-sensitive channels. Proc R Soc Lond B 245:203–210

    Google Scholar 

  • Hillman P, Hochstein S, Minke B (1976) Nonlocal interactions in the photoreceptor transduction process. J Gen Physiol 68:227–245

    Google Scholar 

  • Hillman P, Hochstein S, Minke B (1983) Transduction in invertebrate photoreceptors: role of pigment bistability. Physiol Rev 63:668–772

    Google Scholar 

  • Hochstein S, Minke B, Hillman P (1973) Antagonistic components of the late receptor potential in the barnacle photoreceptor arising from different stages of the pigment process. J Gen Physiol 62:105–128

    Google Scholar 

  • Lantz RC, Wong F, Mauro A (1977) Liability of prolonged depolarizing afterpotential in Balanus photoreceptors. J Gen Physiol 70:441–452

    Google Scholar 

  • Lester DS, Collin C, Etcheberrygaray R, Alkon DL (1991) Arachidonic acid and diacylglycerol act synergistically to activate protein kinase C in vitro and in vivo. Biochem Biophys Res Commun 179:1522–1528

    Google Scholar 

  • Minke B (1977) Drosophila mutant with a transducer defect. Biophys Struct Mech 3:59–63

    Google Scholar 

  • Minke B, Wu CF, Pak WL (1975) Induction of photoreceptor voltage noise in the dark in Drosophila mutant. Nature 258:84–87

    Google Scholar 

  • Nagy K (1991) Biophysical processes in invertebrate photoreceptors: recent progress and a critical overview based on Limulus photoreceptors. Q Rev Biophys 24:165–226

    Google Scholar 

  • Nasi E (1991) Two light-dependent conductances in Lima rhabdomeric photoreceptors. J Gen Physiol 97:55–72

    Google Scholar 

  • Nelson TJ, Collin C, Alkon DL (1990) Isolation of a G protein that is modified by learning and reduces potassium currents in Hermissenda. Science 247:1479–1483

    Google Scholar 

  • Nolte J, Brown JE (1972) Electrophysiological properties of cells in the median ocellus of Limulus. J Gen Physiol 59:167–185

    Google Scholar 

  • Paulsen R, Bentrop J (1984) Reversible phosphorylation of opsin induced by irradiation of blowfly retinae. J Comp Physiol A 155:39–45

    Google Scholar 

  • Sakakibara M, Alkon DL, DeLorenzo R, Goldenring JR, Neary JT, Heldman E (1986a) Modulation of calcium-mediated inactivation of ionic currents by Ca++/calmodulin-dependent protein kinase II. Biophys J 50:319–327

    Google Scholar 

  • Sakakibara M, Alkon DL, Neary JT, Heldman E, Gould R (1986b) Inositol trisphosphate regulation of photoreceptor membrane currents. Biophys J 50:797–803

    Google Scholar 

  • Tsukahara Y, Horridge GA, Stavenga DG (1977) Afterpotentials in dronefly retinula cells. J Comp Physiol 114:253–266

    Google Scholar 

  • West A, Barnes E, Alkon DL (1982) Primary changes of voltage responses during retention of associative learning. J Neurophysiol 48:1243–1255

    Google Scholar 

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Author notes

  1. H. -P. Höpp

    Present address: Max-Planck-Institut für Entwicklungsbiologie, Spemannstrasse 35, W-7400, Tübingen, FRG

Authors and Affiliations

  1. National Institute of Neural Disorders and Stroke, 20892, Bethesda, MD, USA

    H. -P. Höpp & D. L. Alkon

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  1. H. -P. Höpp
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  2. D. L. Alkon
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Höpp, H.P., Alkon, D.L. Different ionic conductances are modulated during the late receptor potential and the prolonged depolarizing afterpotential in Hermissenda type A photoreceptors. J Comp Physiol A 172, 47–55 (1993). https://doi.org/10.1007/BF00214714

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