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. 1983 Dec;345:329–351. doi: 10.1113/jphysiol.1983.sp014981

Ionic currents of solitary horizontal cells isolated from goldfish retina.

M Tachibana
PMCID: PMC1193800  PMID: 6420548

Abstract

Solitary horizontal cells, dissociated from papain-treated goldfish retinas, produce action potentials and show a non-linear current-voltage relationship. Underlying ion-conductance mechanisms were analysed by a single-micro-electrode voltage-clamp technique. Pharmacological and ion-substitution experiments revealed that ionic currents could be separated into at least four voltage-dependent currents: a Ca current and three types of K currents. The Ca current was activated by membrane depolarization beyond -45 mV, reached a maximal value near 0 mV, and became smaller at more positive potentials. By extrapolation, the reversal potential was estimated to be approximately +50 mV. The Ca current was inactivated by accumulation of intracellular Ca ions but not by membrane depolarization. Co ions (4mM) blocked this current. The first type of K current showed anomalous (inward-going) rectification near the resting potential (congruent to -60 mV). Hyperpolarization from the resting level produced a large, almost steady inward current, while depolarization evoked only a small, steady outward current. The current-voltage relationship revealed a shallow negative resistance region at membrane potentials beyond -50 mV. The current was blocked by Cs (10 mM) or Ba (1 mM) ions. The second type of K current (the transient outward current) was activated by membrane depolarization beyond -25 mV. The peak amplitude increased almost exponentially as the membrane was depolarized. During steady depolarization this current decayed exponentially (time constant congruent to 500 ms at +20 mV). The current was inactivated by conditioning depolarization (greater than 10 s) beyond -30 mV and blocked by 4-aminopyridine (10 mM). The third type of K current was the maintained outward current which was activated by membrane depolarization beyond -20 mV, increased to a steady level in a few hundred milliseconds, and showed little inactivation. The amplitude increased as the membrane was depolarized. The current was blocked by tetraethylammonium ions (20 mM). A Ca-mediated K current was not detected. Action potentials and the non-linear current-voltage relationship of solitary horizontal cells can be explained qualitatively by the combination of the four ionic currents.

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  1. Anctil M., Ali M. A., Couillard P. Isolated retinal cells of some lower vertebrates. Rev Can Biol. 1973 Jun;32(2):107–119. [PubMed] [Google Scholar]
  2. Bader C. R., Bertrand D., Schwartz E. A. Voltage-activated and calcium-activated currents studied in solitary rod inner segments from the salamander retina. J Physiol. 1982 Oct;331:253–284. doi: 10.1113/jphysiol.1982.sp014372. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bader C. R., MacLeish P. R., Schwartz E. A. Responses to light of solitary rod photoreceptors isolated from tiger salamander retina. Proc Natl Acad Sci U S A. 1978 Jul;75(7):3507–3511. doi: 10.1073/pnas.75.7.3507. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bader C. R., Macleish P. R., Schwartz E. A. A voltage-clamp study of the light response in solitary rods of the tiger salamander. J Physiol. 1979 Nov;296:1–26. doi: 10.1113/jphysiol.1979.sp012988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Baylor D. A., Fuortes M. G. Electrical responses of single cones in the retina of the turtle. J Physiol. 1970 Mar;207(1):77–92. doi: 10.1113/jphysiol.1970.sp009049. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Baylor D. A., Fuortes M. G., O'Bryan P. M. Receptive fields of cones in the retina of the turtle. J Physiol. 1971 Apr;214(2):265–294. doi: 10.1113/jphysiol.1971.sp009432. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Bray D. Surface movements during the growth of single explanted neurons. Proc Natl Acad Sci U S A. 1970 Apr;65(4):905–910. doi: 10.1073/pnas.65.4.905. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Brehm P., Eckert R. Calcium entry leads to inactivation of calcium channel in Paramecium. Science. 1978 Dec 15;202(4373):1203–1206. doi: 10.1126/science.103199. [DOI] [PubMed] [Google Scholar]
  9. Burkhardt D. A. Responses and receptive-field organization of cones in perch retinas. J Neurophysiol. 1977 Jan;40(1):53–62. doi: 10.1152/jn.1977.40.1.53. [DOI] [PubMed] [Google Scholar]
  10. Byerly L., Hagiwara S. Calcium currents in internally perfused nerve cell bodies of Limnea stagnalis. J Physiol. 1982 Jan;322:503–528. doi: 10.1113/jphysiol.1982.sp014052. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Byzov A. L., Trifonov J. A. The response to electric stimulation of horizontal cells in the carp retina. Vision Res. 1968 Jul;8(7):817–822. doi: 10.1016/0042-6989(68)90132-6. [DOI] [PubMed] [Google Scholar]
  12. Byzov A. L., Trifonov Y. A., Chailahian L. M., Golubtzov K. W. Amplification of graded potentials in horizontal cells of the retina. Vision Res. 1977 Feb;17(2):265–273. doi: 10.1016/0042-6989(77)90090-6. [DOI] [PubMed] [Google Scholar]
  13. Colburn T. R., Schwartz E. A. Linear voltage control of current passed through a micropipette with variable resistance. Med Biol Eng. 1972 Jul;10(4):504–509. doi: 10.1007/BF02474198. [DOI] [PubMed] [Google Scholar]
  14. Connor J. A., Stevens C. F. Voltage clamp studies of a transient outward membrane current in gastropod neural somata. J Physiol. 1971 Feb;213(1):21–30. doi: 10.1113/jphysiol.1971.sp009365. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Doroshenko P. A., Tsyndrenko A. Ia. Deistvie vnutrikletochnogo kal'tsiia na kal'tsievyi vkhodiashchii tok. Neirofiziologiia. 1978;10(2):203–205. [PubMed] [Google Scholar]
  16. Dowling J. E., Brown J. E., Major D. Synapses of horizontal cells in rabbit and cat retinas. Science. 1966 Sep 30;153(3744):1639–1641. doi: 10.1126/science.153.3744.1639. [DOI] [PubMed] [Google Scholar]
  17. Dowling J. E., Werblin F. S. Organization of retina of the mudpuppy, Necturus maculosus. I. Synaptic structure. J Neurophysiol. 1969 May;32(3):315–338. doi: 10.1152/jn.1969.32.3.315. [DOI] [PubMed] [Google Scholar]
  18. Drujan B. D., Svaetichin G. Characterization of different classes of isolated retinal cells. Vision Res. 1972 Nov;12(11):1777–1784. doi: 10.1016/0042-6989(72)90068-5. [DOI] [PubMed] [Google Scholar]
  19. Ehinger B., Falck B., Laties A. M. Adrenergic neurons in teleost retina. Z Zellforsch Mikrosk Anat. 1969 May 23;97(2):285–297. doi: 10.1007/BF00344763. [DOI] [PubMed] [Google Scholar]
  20. Fain G. L., Lisman J. E. Membrane conductances of photoreceptors. Prog Biophys Mol Biol. 1981;37(2):91–147. doi: 10.1016/0079-6107(82)90021-9. [DOI] [PubMed] [Google Scholar]
  21. HODGKIN A. L., HOROWICZ P. The influence of potassium and chloride ions on the membrane potential of single muscle fibres. J Physiol. 1959 Oct;148:127–160. doi: 10.1113/jphysiol.1959.sp006278. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Hagiwara S., Byerly L. Calcium channel. Annu Rev Neurosci. 1981;4:69–125. doi: 10.1146/annurev.ne.04.030181.000441. [DOI] [PubMed] [Google Scholar]
  23. Hagiwara S., Fukuda J., Eaton D. C. Membrane currents carried by Ca, Sr, and Ba in barnacle muscle fiber during voltage clamp. J Gen Physiol. 1974 May;63(5):564–578. doi: 10.1085/jgp.63.5.564. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Hagiwara S., Miyazaki S., Rosenthal N. P. Potassium current and the effect of cesium on this current during anomalous rectification of the egg cell membrane of a starfish. J Gen Physiol. 1976 Jun;67(6):621–638. doi: 10.1085/jgp.67.6.621. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Hagiwara S., Nakajima S. Differences in Na and Ca spikes as examined by application of tetrodotoxin, procaine, and manganese ions. J Gen Physiol. 1966 Mar;49(4):793–806. doi: 10.1085/jgp.49.4.793. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Hagiwara S., Takahashi K. The anomalous rectification and cation selectivity of the membrane of a starfish egg cell. J Membr Biol. 1974;18(1):61–80. doi: 10.1007/BF01870103. [DOI] [PubMed] [Google Scholar]
  27. Hagiwara S., Yoshida S., Yoshii M. Transient and delayed potassium currents in the egg cell membrane of the coelenterate, Renilla koellikeri. J Physiol. 1981 Sep;318:123–141. doi: 10.1113/jphysiol.1981.sp013854. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Hagiwara S., Yoshii M. Effects of internal potassium and sodium on the anomalous rectification of the starfish egg as examined by internal perfusion. J Physiol. 1979 Jul;292:251–265. doi: 10.1113/jphysiol.1979.sp012849. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Hille B. Ionic selectivity of Na and K channels of nerve membranes. Membranes. 1975;3:255–323. [PubMed] [Google Scholar]
  30. Johnston D., Lam D. M. Regenerative and passive membrane properties of isolated horizontal cells from a teleost retina. Nature. 1981 Jul 30;292(5822):451–454. doi: 10.1038/292451a0. [DOI] [PubMed] [Google Scholar]
  31. Kaneko A. Electrical connexions between horizontal cells in the dogfish retina. J Physiol. 1971 Feb;213(1):95–105. doi: 10.1113/jphysiol.1971.sp009370. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Kaneko A., Shimazaki H. Effects of external ions on the synaptic transmission from photorecptors to horizontal cells in the carp retina. J Physiol. 1975 Nov;252(2):509–522. doi: 10.1113/jphysiol.1975.sp011155. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Kostyuk P. G., Krishtal O. A. Effects of calcium and calcium-chelating agents on the inward and outward current in the membrane of mollusc neurones. J Physiol. 1977 Sep;270(3):569–580. doi: 10.1113/jphysiol.1977.sp011969. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Kostyuk P. G., Krishtal O. A., Shakhovalov Y. A. Separation of sodium and calcium currents in the somatic membrane of mollusc neurones. J Physiol. 1977 Sep;270(3):545–568. doi: 10.1113/jphysiol.1977.sp011968. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Lam D. M. Biosynthesis of acetylcholine in turtle photoreceptors. Proc Natl Acad Sci U S A. 1972 Jul;69(7):1987–1991. doi: 10.1073/pnas.69.7.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Lam D. M., Steinman L. The uptake of ( - 3 H) aminobutyric acid in the goldfish retina. Proc Natl Acad Sci U S A. 1971 Nov;68(11):2777–2781. doi: 10.1073/pnas.68.11.2777. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Lam D. M., Su Y. Y., Swain L., Marc R. E., Brandon C., Wu J. Y. Immunocytochemical localisation of L-glutamic acid decarboxylase in the goldfish retina. Nature. 1979 Apr 5;278(5704):565–567. doi: 10.1038/278565a0. [DOI] [PubMed] [Google Scholar]
  38. MACNICHOL E. J., SVAETICHIN G. Electric responses from the isolated retinas of fishes. Am J Ophthalmol. 1958 Sep;46(3 Pt 2):26–46. doi: 10.1016/0002-9394(58)90053-9. [DOI] [PubMed] [Google Scholar]
  39. Marc R. E., Stell W. K., Bok D., Lam D. M. GABA-ergic pathways in the goldfish retina. J Comp Neurol. 1978 Nov 15;182(2):221–244. doi: 10.1002/cne.901820204. [DOI] [PubMed] [Google Scholar]
  40. Meech R. W., Standen N. B. Potassium activation in Helix aspersa neurones under voltage clamp: a component mediated by calcium influx. J Physiol. 1975 Jul;249(2):211–239. doi: 10.1113/jphysiol.1975.sp011012. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Meech R. W. The sensitivity of Helix aspersa neurones to injected calcium ions. J Physiol. 1974 Mar;237(2):259–277. doi: 10.1113/jphysiol.1974.sp010481. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Miyazaki S. I., Ohmori H., Sasaki S. Potassium rectifications of the starfish oocyte membrane and their changes during oocyte maturation. J Physiol. 1975 Mar;246(1):55–78. doi: 10.1113/jphysiol.1975.sp010880. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Naka K. I., Rushton W. A. The generation and spread of S-potentials in fish (Cyprinidae). J Physiol. 1967 Sep;192(2):437–461. doi: 10.1113/jphysiol.1967.sp008308. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Naka K. I. The horizontal cells. Vision Res. 1972 Apr;12(4):573–588. doi: 10.1016/0042-6989(72)90153-8. [DOI] [PubMed] [Google Scholar]
  45. Naka K. Functional organization of catfish retina. J Neurophysiol. 1977 Jan;40(1):26–43. doi: 10.1152/jn.1977.40.1.26. [DOI] [PubMed] [Google Scholar]
  46. Neher E. Two fast transient current components during voltage clamp on snail neurons. J Gen Physiol. 1971 Jul;58(1):36–53. doi: 10.1085/jgp.58.1.36. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Norton A. L., Spekreijse H., Wolbarsht M. L., Wagner H. G. Receptive field organization of the S-potential. Science. 1968 May 31;160(3831):1021–1022. doi: 10.1126/science.160.3831.1021. [DOI] [PubMed] [Google Scholar]
  48. O'Lague P. H., Potter D. D., Furshpan E. J. Studies on rat sympathetic neurons developing in cell culture. I. Growth characteristics and electrophysiological properties. Dev Biol. 1978 Dec;67(2):384–403. doi: 10.1016/0012-1606(78)90208-7. [DOI] [PubMed] [Google Scholar]
  49. Pinto L. H., Pak W. L. Light-induced changes in photoreceptor membrane resistance and potential in Gecko retinas. I. Preparations treated to reduce lateral interactions. J Gen Physiol. 1974 Jul;64(1):26–48. doi: 10.1085/jgp.64.1.26. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Pinto L. H., Pak W. L. Light-induced changes in photoreceptor membrane resistance and potential in Gecko retinas. II. Preparations with active lateral interactions. J Gen Physiol. 1974 Jul;64(1):49–69. doi: 10.1085/jgp.64.1.49. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Plant T. D., Standen N. B. Calcium current inactivation in identified neurones of Helix aspersa. J Physiol. 1981 Dec;321:273–285. doi: 10.1113/jphysiol.1981.sp013983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Schwartz E. A. Calcium-independent release of GABA from isolated horizontal cells of the toad retina. J Physiol. 1982 Feb;323:211–227. doi: 10.1113/jphysiol.1982.sp014069. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. TOMITA T. Electrical activity in the vertebrate retina. J Opt Soc Am. 1963 Jan;53:49–57. doi: 10.1364/josa.53.000049. [DOI] [PubMed] [Google Scholar]
  54. Tachibana M. Membrane properties of solitary horizontal cells isolated from goldfish retina. J Physiol. 1981 Dec;321:141–161. doi: 10.1113/jphysiol.1981.sp013976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Takahashi K., Yoshii M. Effects of internal free calcium upon the sodium and calcium channels in the tunicate egg analysed by the internal perfusion technique. J Physiol. 1978 Jun;279:519–549. doi: 10.1113/jphysiol.1978.sp012360. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Thompson S. H. Three pharmacologically distinct potassium channels in molluscan neurones. J Physiol. 1977 Feb;265(2):465–488. doi: 10.1113/jphysiol.1977.sp011725. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Tillotson D. Inactivation of Ca conductance dependent on entry of Ca ions in molluscan neurons. Proc Natl Acad Sci U S A. 1979 Mar;76(3):1497–1500. doi: 10.1073/pnas.76.3.1497. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Toyoda J., Kujiraoka T. Analyses of bipolar cell responses elicited by polarization of horizontal cells. J Gen Physiol. 1982 Jan;79(1):131–145. doi: 10.1085/jgp.79.1.131. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Trifonov I. U. Izuchenie sinapticheskoi peredachi mezhdu fotoretseptorom i gorizontal'noi kletkoi pri pomoshchi élektricheskikh razdrazhenii setchatki. Biofizika. 1968 Sep-Oct;13(5):809–817. [PubMed] [Google Scholar]
  60. Werblin F. S., Dowling J. E. Organization of the retina of the mudpuppy, Necturus maculosus. II. Intracellular recording. J Neurophysiol. 1969 May;32(3):339–355. doi: 10.1152/jn.1969.32.3.339. [DOI] [PubMed] [Google Scholar]
  61. Wilson W. A., Goldner M. M. Voltage clamping with a single microelectrode. J Neurobiol. 1975 Jul;6(4):411–422. doi: 10.1002/neu.480060406. [DOI] [PubMed] [Google Scholar]
  62. Witkovsky P., Dowling J. E. Synaptic relationships in the plexiform layers of carp retina. Z Zellforsch Mikrosk Anat. 1969;100(1):60–82. doi: 10.1007/BF00343821. [DOI] [PubMed] [Google Scholar]
  63. Yamada E., Ishikawa T. The fine structure of the horizontal cells in some vertebrate retinae. Cold Spring Harb Symp Quant Biol. 1965;30:383–392. doi: 10.1101/sqb.1965.030.01.038. [DOI] [PubMed] [Google Scholar]

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