Advertisement

Voltage-Gated Ion Channels in Human Photoreceptors: Na+ and Hyperpolarization-Activated Cation Channels

  • Ei-ichi Miyachi
  • Fusao Kawai
Conference paper
Part of the Keio University International Symposia for Life Sciences and Medicine book series (KEIO, volume 11)

Abstract

A light stimulus hyperpolarizes photoreceptors in biochemical processes in the outer segment and reduces the release of neurotransmitter by decreasing a Ca2+ influx at their synaptic terminals [1–6]. The photovoltage is shaped by voltage-gated channels in the inner segment [7–11]. Major voltage-gated currents measured in vertebrate photoreceptors are an L-type Ca2+ current, a delayed rectifier K+ current, a fast transient K+ current, and a hyperpolarization-activated cation current (h current) [7, 9, 10, 12]. Although mammalian photoreceptors are commonly thought to be nonspiking neurons [7, 9–11, 13], electrophysiological recordings with suction electrodes show that the termination of a light stimulus induces spike-like current responses in monkey photoreceptors [14]. This raises the possibility that primate photoreceptors may be able to generate action potentials. However, this hypothesis still remains uncertain, as there are few voltage recordings from primate photoreceptors [11, 15, 16]. Using the patch-clamp technique, we examined whether human rod photoreceptors can elicit action potentials, and also investigated the role of the voltage-gated currents for rod voltage responses.

Key words

Retina Photoreceptor Voltage-gated channel Sodium channel h channel 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Lipton SA, Ostroy SE, Dowling JE (1977) Electrical and adaptive properties of rod photoreceptors in Bufo marinus. I. Effects of altered extracellular Ca2+ levels. J Gen Physiol 70: 747–770PubMedCrossRefGoogle Scholar
  2. 2.
    Copenhagen DR, Jahr CE (1989) Release of endogenous excitatory amino acids from turtle photoreceptors. Nature 341: 536–539PubMedCrossRefGoogle Scholar
  3. 3.
    Wässle H, Boycott BB (1991) Functional architecture of the mammalian retina. Physiol Rev 71: 447–480PubMedGoogle Scholar
  4. 4.
    Masland RH (1996) Processing and encoding of visual information in the retina. Curr Opin Neurobiol 6: 467–474PubMedCrossRefGoogle Scholar
  5. 5.
    Savchenko A, Barnes S, Kramer RH (1997) Cyclic-nucleotide-gated channels mediate synaptic feedback by nitric oxide. Nature 390: 694–698PubMedGoogle Scholar
  6. 6.
    DeVries SH, Schwartz EA (1999) Kainate receptors mediate synaptic transmission between cones and “Off” bipolar cells in a mammalian retina. Nature 397: 157–160PubMedCrossRefGoogle Scholar
  7. 7.
    Bader CR, Bertrand D, Schwartz EA (1982) Voltage-activated and calcium-activated currents studied in solitary rod inner segments from the salamander retina. J Physiol 331: 253–284PubMedGoogle Scholar
  8. 8.
    Barnes S, Hille B (1989) Ionic channels of the inner segment of tiger salamander cone photoreceptors. J Gen Physiol 94: 719–743PubMedCrossRefGoogle Scholar
  9. 9.
    Maricq AV, Korenbrot JI (1990) Inward rectification in the inner segment of single retinal cone photoreceptors. J Neurophysiol 64: 1917–1928PubMedGoogle Scholar
  10. 10.
    Yagi T, Macleish PR (1994) Ionic conductances of monkey solitary cone inner segments. J Neurophysiol 71: 656–665PubMedGoogle Scholar
  11. 11.
    Schneeweis DM, Schnapf JL (1995) Photovoltage of rods and cones in the macaque retina. Science 268: 1053–1056PubMedCrossRefGoogle Scholar
  12. 12.
    Wollmuth LP, Hille B (1992) Ionic selectivity of Ih channels of rod photoreceptors in tiger salamanders. J Gen Physiol 100: 749–765PubMedCrossRefGoogle Scholar
  13. 13.
    Berry MJ, Brivanlou IH, Jordan TA, et al. (1999) Anticipation of moving stimuli by the retina. Nature 398: 334–338PubMedCrossRefGoogle Scholar
  14. 14.
    Schnapf JL, Nunn BJ, Meister M, et al. (1990) Visual transduction in cones of the monkey Macaca fascicularis. J Physiol 427: 681–713PubMedGoogle Scholar
  15. 15.
    Schneeweis DM, Schnapf JL (1999) The photovoltage of macaque cone photoreceptors: adaptation, noise, and kinetics. J Neurosci 19: 1203–1216PubMedGoogle Scholar
  16. 16.
    Schneeweis DM, Schnapf JL (2000) Noise and light adaptation in rods of the macaque monkey. Vis Neurosci 17: 659–666PubMedCrossRefGoogle Scholar
  17. 17.
    Fain GL, Quandt FN, Bastian BL, et al. (1978) Contribution of a caesium-sensitive conductance increase to the rod photoresponse. Nature 272: 466–469PubMedCrossRefGoogle Scholar
  18. 18.
    Kawai F, Horiguchi M, Suzuki H, et al. (2001) Na+ action potentials in human photoreceptors. Neuron 30: 451–458PubMedCrossRefGoogle Scholar
  19. 19.
    Calkins DJ, Sterling P (1999) Evidence that circuits for spatial and color vision segregate at the first retinal synapse. Neuron 24: 313–321PubMedCrossRefGoogle Scholar
  20. 20.
    Pugh EN Jr, Nikonov S, Lamb TD (1999) Molecular mechanisms of vertebrate photoreceptor light adaptation. Curr Opin Neurobiol 9: 410–418PubMedCrossRefGoogle Scholar
  21. 21.
    Kawai F, Sterling P (1999) AMPA receptor activates a G-protein that suppresses a cGMP-gated current. J Neurosci 19: 2954–2959PubMedGoogle Scholar
  22. 22.
    Werblin FS (1978) Transmission along and between rods in the tiger salamander retina. J Physiol 280: 449–470PubMedGoogle Scholar
  23. 23.
    Hamill OP, Marty A, Neher E, et al. (1981) Improved patch-clamp techniques for high resolution current recording from cells and cell-free membrane patches. Pflügers Arch 391: 85–100PubMedCrossRefGoogle Scholar
  24. 24.
    Kawai F, Horiguchi M, Suzuki H, et al. (2002) Modulation by hyperpolarizationactivated cation currents of voltage responses in human rods. Brain Res 943: 4855CrossRefGoogle Scholar
  25. 25.
    Yau K-W, Baylor DA (1989) Cyclic GMP-activated conductance of retinal photoreceptor cells. Annu Rev Neurosci 12: 289–327PubMedCrossRefGoogle Scholar
  26. 26.
    Torre V, Ashmore JF, Lamb TD, et al. (1995) Transduction and adaptation in sensory receptor cells. J Neurosci 15: 7757–7768PubMedGoogle Scholar
  27. 27.
    Kawai F, Kurahashi T, Kaneko A (1996) T type Ca2+ channel lowers the threshold of spike generation in the newt olfactory receptor cell. J Gen Physiol 108: 525–535PubMedCrossRefGoogle Scholar
  28. 28.
    Wang GY, Ratto G, Bisti S, et al. (1997) Functional development of intrinsic properties in ganglion cells of the mammalian retina. J Neurophysiol 78: 2895–2903PubMedGoogle Scholar
  29. 29.
    Hidaka S, Ishida AT (1998) Voltage-gated Na+ current availability after step- and spike-shaped conditioning depolarizations of retinal ganglion cells. Pflügers Arch 436: 436–508CrossRefGoogle Scholar
  30. 30.
    Tabata T, Ishida AT (1999) A zinc-dependent Cl current in neuronal somata. J Neurosci 19: 5195–5204PubMedGoogle Scholar
  31. 31.
    Hagiwara S, Kakahashi K (1974) The anomalous rectification and cation selectivity of the membrane of a starfish egg cell. J Membr Biol 18: 61–80PubMedCrossRefGoogle Scholar
  32. 32.
    Tachibana M (1983) Ionic currents of solitary horizontal cells isolated from goldfish retina. J Physiol 345: 329–351PubMedGoogle Scholar
  33. 33.
    Hestrin S (1987) The properties and function of inward rectification in rod photoreceptors of the tiger salamander. J Physiol 390: 319–333PubMedGoogle Scholar
  34. 34.
    Fain GL, Gerschenfeld HM, Quandt FN (1980) Calcium spikes in toad rods. J Physiol 303: 495–513PubMedGoogle Scholar
  35. 35.
    Gerschenfeld HM, Piccolino M, Neyton J (1980) Feed-back modulation of cone synapses by L-horizontal cells of turtle retina. J Exp Biol 89: 177–192PubMedGoogle Scholar
  36. 36.
    Piccolino M, Gerschenfeld HM (1980) Characteristics and ionic processes involved in feedback spikes of turtle cones. Proc R Soc Lond B Biol Sci 206: 439–463PubMedCrossRefGoogle Scholar
  37. 37.
    Maricq AV, Korenbrot JI (1988) Calcium and calcium-dependent chloride currents generate action potentials in solitary cone photoreceptors. Neuron 1: 503–515PubMedCrossRefGoogle Scholar
  38. 38.
    Nowycky MC, Fox AP, Tsien RW (1985) Three types of neuronal calcium channel with different calcium agonist sensitivity. Nature 316: 440–443PubMedCrossRefGoogle Scholar
  39. 39.
    Kaneko A, Pinto LH, Tachibana M (1989) Transient calcium current of retinal bipolar cells of the mouse. J Physiol 410: 613–629PubMedGoogle Scholar
  40. 40.
    Mayer ML, Westbrook GL (1983) A voltage-clamp analysis of inward (anomalous) rectification in mouse spinal sensory ganglion neurones. J Physiol 340: 19–45PubMedGoogle Scholar
  41. 41.
    DiFrancesco D (1984) Characterization of the pace-maker current kinetics in calf Purkinje fibres. J Physiol 348: 341–367PubMedGoogle Scholar
  42. 42.
    McCormick DA, Pape HC (1990) Properties of a hyperpolarization-activated cation current and its role in rhythmic oscillation in thalamic relay neurones. J Physiol 431: 291–318PubMedGoogle Scholar
  43. 43.
    Wollmuth LP (1995) Multiple ion binding sites in Ih channels of rod photoreceptors from tiger salamanders. Pflügers Arch 430: 34–43PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Tokyo 2003

Authors and Affiliations

  • Ei-ichi Miyachi
    • 1
  • Fusao Kawai
    • 1
  1. 1.Department of PhysiologyFujita Health University School of MedicineToyoake, AichiJapan

Personalised recommendations