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. 1989 Feb 1;93(2):343–364. doi: 10.1085/jgp.93.2.343

Receptor Ca current and Ca-gated K current in tonic electroreceptors of the marine catfish Plotosus

PMCID: PMC2216209  PMID: 2703820

Abstract

The tonic electroreceptors of the marine catfish Plotosus consist of a cluster of ampullae of sensory epithelia, each of which is an isolated receptor unit that is attached to the distant skin with only a long duct. The single-cell layered sensory epithelium has pear-shaped receptor cells interspersed with thin processes of supporting cells. The apical border of the receptor cells is joined to the supporting cells with junctional complexes. Single ampullae were excised and electrically isolated by an air gap. Receptor responses were recorded as epithelial current under voltage clamp, and postsynaptic potentials (PSP) were recorded externally from the afferent nerve in the presence of tetrodotoxin. The ampulla showed a DC potential of -19.2 +/- 6.5 mV (mean +/- SD, n = 18), and an input resistance of 697 +/- 263 K omega (n = 21). Positive voltage steps evoked inward currents with two peaks and a positive dip, associated with PSPs. The apical membrane proved to be inactive. The inward current was ascribed to Ca current, and the positive dip to Ca-gated transient K current, bot in the basal membrane of receptor cells. The Ca channels proved to have ionic selectivity in the order of Sr2+ greater than Ca2+ greater than Ba2+, and presumably they also passed outward current nonselectively. Double-pulse experiments further revealed a current-dependent inactivation for a part of the Ca current.

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Selected References

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  1. Akaike N., Lee K. S., Brown A. M. The calcium current of Helix neuron. J Gen Physiol. 1978 May;71(5):509–531. doi: 10.1085/jgp.71.5.509. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Almers W., Fink R., Palade P. T. Calcium depletion in frog muscle tubules: the decline of calcium current under maintained depolarization. J Physiol. 1981 Mar;312:177–207. doi: 10.1113/jphysiol.1981.sp013623. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Ashcroft F. M., Stanfield P. R. Calcium dependence of the inactivation of calcium currents in skeletal muscle fibers of an insect. Science. 1981 Jul 10;213(4504):224–226. doi: 10.1126/science.213.4504.224. [DOI] [PubMed] [Google Scholar]
  4. Bosher S. K., Warren R. L. Very low calcium content of cochlear endolymph, an extracellular fluid. Nature. 1978 Jun 1;273(5661):377–378. doi: 10.1038/273377a0. [DOI] [PubMed] [Google Scholar]
  5. 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]
  6. Brehm P., Eckert R., Tillotson D. Calcium-mediated inactivation of calcium current in Paramecium. J Physiol. 1980 Sep;306:193–203. doi: 10.1113/jphysiol.1980.sp013391. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Brown A. M., Morimoto K., Tsuda Y., wilson D. L. Calcium current-dependent and voltage-dependent inactivation of calcium channels in Helix aspersa. J Physiol. 1981 Nov;320:193–218. doi: 10.1113/jphysiol.1981.sp013944. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Bullock T. H. Electroreception. Annu Rev Neurosci. 1982;5:121–170. doi: 10.1146/annurev.ne.05.030182.001005. [DOI] [PubMed] [Google Scholar]
  9. Byerly L., Chase P. B., Stimers J. R. Permeation and interaction of divalent cations in calcium channels of snail neurons. J Gen Physiol. 1985 Apr;85(4):491–518. doi: 10.1085/jgp.85.4.491. [DOI] [PMC free article] [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. Clusin W. T., Bennett M. V. Calcium-activated conductance in skate electroreceptors: current clamp experiments. J Gen Physiol. 1977 Feb;69(2):121–143. doi: 10.1085/jgp.69.2.121. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Clusin W. T., Bennett M. V. Calcium-activated conductance in skate electroreceptors: voltage clamp experiments. J Gen Physiol. 1977 Feb;69(2):145–182. doi: 10.1085/jgp.69.2.145. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Clusin W. T., Bennett M. V. The ionic basis of oscillatory responses of skate electroreceptors. J Gen Physiol. 1979 Jun;73(6):703–723. doi: 10.1085/jgp.73.6.703. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Clusin W. T., Bennett M. V. The oscillatory responses of skate electroreceptors to small voltage stimuli. J Gen Physiol. 1979 Jun;73(6):685–702. doi: 10.1085/jgp.73.6.685. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Corey D. P., Hudspeth A. J. Ionic basis of the receptor potential in a vertebrate hair cell. Nature. 1979 Oct 25;281(5733):675–677. doi: 10.1038/281675a0. [DOI] [PubMed] [Google Scholar]
  16. Crawford A. C., Fettiplace R. An electrical tuning mechanism in turtle cochlear hair cells. J Physiol. 1981 Mar;312:377–412. doi: 10.1113/jphysiol.1981.sp013634. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Davis H. A model for transducer action in the cochlea. Cold Spring Harb Symp Quant Biol. 1965;30:181–190. doi: 10.1101/sqb.1965.030.01.020. [DOI] [PubMed] [Google Scholar]
  18. Eckert R., Tillotson D. L. Calcium-mediated inactivation of the calcium conductance in caesium-loaded giant neurones of Aplysia californica. J Physiol. 1981 May;314:265–280. doi: 10.1113/jphysiol.1981.sp013706. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Fain G. L., Quandt F. N., Gerschenfeld H. M. Calcium-dependent regenerative responses in rods. Nature. 1977 Oct 20;269(5630):707–710. doi: 10.1038/269707a0. [DOI] [PubMed] [Google Scholar]
  20. Fenwick E. M., Marty A., Neher E. Sodium and calcium channels in bovine chromaffin cells. J Physiol. 1982 Oct;331:599–635. doi: 10.1113/jphysiol.1982.sp014394. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Fleckenstein A. Specific pharmacology of calcium in myocardium, cardiac pacemakers, and vascular smooth muscle. Annu Rev Pharmacol Toxicol. 1977;17:149–166. doi: 10.1146/annurev.pa.17.040177.001053. [DOI] [PubMed] [Google Scholar]
  22. Fox A. P., Krasne S. Two calcium currents in Neanthes arenaceodentatus egg cell membranes. J Physiol. 1984 Nov;356:491–505. doi: 10.1113/jphysiol.1984.sp015479. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Fukushima Y., Hagiwara S. Currents carried by monovalent cations through calcium channels in mouse neoplastic B lymphocytes. J Physiol. 1985 Jan;358:255–284. doi: 10.1113/jphysiol.1985.sp015550. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. HAMA K. SOME OBSERVATIONS ON THE FINE STRUCTURE OF THE LATERAL LINE ORGAN OF THE JAPANESE SEA EEL LYNCOZYMBA NYSTROMI. J Cell Biol. 1965 Feb;24:193–210. doi: 10.1083/jcb.24.2.193. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. 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]
  26. 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]
  27. Hama K. A study on the fine structure of the saccular macula of the gold fish. Z Zellforsch Mikrosk Anat. 1969;94(2):155–171. doi: 10.1007/BF00339353. [DOI] [PubMed] [Google Scholar]
  28. Hudspeth A. J. Extracellular current flow and the site of transduction by vertebrate hair cells. J Neurosci. 1982 Jan;2(1):1–10. doi: 10.1523/JNEUROSCI.02-01-00001.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Hudspeth A. J., Jacobs R. Stereocilia mediate transduction in vertebrate hair cells (auditory system/cilium/vestibular system). Proc Natl Acad Sci U S A. 1979 Mar;76(3):1506–1509. doi: 10.1073/pnas.76.3.1506. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Hudspeth A. J. The cellular basis of hearing: the biophysics of hair cells. Science. 1985 Nov 15;230(4727):745–752. doi: 10.1126/science.2414845. [DOI] [PubMed] [Google Scholar]
  31. Katz B., Miledi R. Tetrodotoxin-resistant electric activity in presynaptic terminals. J Physiol. 1969 Aug;203(2):459–487. doi: 10.1113/jphysiol.1969.sp008875. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. 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]
  33. Kusano K. Influence of ionic environment on the relationship between pre- and postsynaptic potentials. J Neurobiol. 1970;1(4):435–437. doi: 10.1002/neu.480010407. [DOI] [PubMed] [Google Scholar]
  34. Lee K. S., Tsien R. W. Mechanism of calcium channel blockade by verapamil, D600, diltiazem and nitrendipine in single dialysed heart cells. Nature. 1983 Apr 28;302(5911):790–794. doi: 10.1038/302790a0. [DOI] [PubMed] [Google Scholar]
  35. Lee K. S., Tsien R. W. Reversal of current through calcium channels in dialysed single heart cells. Nature. 1982 Jun 10;297(5866):498–501. doi: 10.1038/297498a0. [DOI] [PubMed] [Google Scholar]
  36. Lewis R. S., Hudspeth A. J. Voltage- and ion-dependent conductances in solitary vertebrate hair cells. Nature. 1983 Aug 11;304(5926):538–541. doi: 10.1038/304538a0. [DOI] [PubMed] [Google Scholar]
  37. Lissmann H. W., Mullinger A. M. Organization of ampullary electric receptors in Gymnotidae (Pisces). Proc R Soc Lond B Biol Sci. 1968 Mar 26;169(1017):345–378. doi: 10.1098/rspb.1968.0015. [DOI] [PubMed] [Google Scholar]
  38. McGlone F. P., Russell I. J., Sand O. Measurement of calcium ion concentrations in the lateral line cupulae of Xenopus laevis. J Exp Biol. 1979 Dec;83:123–130. doi: 10.1242/jeb.83.1.123. [DOI] [PubMed] [Google Scholar]
  39. Meech R. W. Calcium-dependent potassium activation in nervous tissues. Annu Rev Biophys Bioeng. 1978;7:1–18. doi: 10.1146/annurev.bb.07.060178.000245. [DOI] [PubMed] [Google Scholar]
  40. Mentrard D., Vassort G., Fischmeister R. Calcium-mediated inactivation of the calcium conductance in cesium-loaded frog heart cells. J Gen Physiol. 1984 Jan;83(1):105–131. doi: 10.1085/jgp.83.1.105. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Naitoh Y., Eckert R. Ionic mechanisms controlling behavioral responses of paramecium to mechanical stimulation. Science. 1969 May 23;164(3882):963–965. doi: 10.1126/science.164.3882.963. [DOI] [PubMed] [Google Scholar]
  42. Obara S., Bennett M. V. Mode of operation of ampullae of Lorenzini of the skate, Raja. J Gen Physiol. 1972 Nov;60(5):534–557. doi: 10.1085/jgp.60.5.534. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Obara S., Sugawara Y. Contribution of Ca to the electroreceptor mechanism in Plotosus ampullae. J Physiol (Paris) 1979;75(4):335–340. [PubMed] [Google Scholar]
  44. Ohmori H. Mechano-electrical transduction currents in isolated vestibular hair cells of the chick. J Physiol. 1985 Feb;359:189–217. doi: 10.1113/jphysiol.1985.sp015581. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Ohmori H. Mechanoelectrical transducer has discrete conductances in the chick vestibular hair cell. Proc Natl Acad Sci U S A. 1984 Mar;81(6):1888–1891. doi: 10.1073/pnas.81.6.1888. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Ohmori H. Studies of ionic currents in the isolated vestibular hair cell of the chick. J Physiol. 1984 May;350:561–581. doi: 10.1113/jphysiol.1984.sp015218. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. 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]
  48. Ross W. N., Stuart A. E. Voltage sensitive calcium channels in the presynaptic terminals of a decrementally conducting photoreceptor. J Physiol. 1978 Jan;274:173–191. doi: 10.1113/jphysiol.1978.sp012142. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Russell I. J., Sellick P. M. Measurement of potassium and chloride ion concentrations in the cupulae of the lateral lines of Xenopus laevis. J Physiol. 1976 May;257(1):245–255. doi: 10.1113/jphysiol.1976.sp011366. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Sugawara Y., Obara S. Damped oscillation in the ampullary electroreceptors of Plotosus involves Ca-activated transient K conductance in the basal membrane of receptor cells. Brain Res. 1984 Jun 4;302(1):171–175. doi: 10.1016/0006-8993(84)91296-4. [DOI] [PubMed] [Google Scholar]
  51. Sugawara Y., Obara S. Ionic currents in the sensory epithelium examined in isolated electroreceptors of Plotosus under simulated in situ conditions. Brain Res. 1984 Jun 4;302(1):176–179. doi: 10.1016/0006-8993(84)91297-6. [DOI] [PubMed] [Google Scholar]
  52. 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]
  53. Zipser B., Bennett M. V. Tetrodotoxin resistant electrically excitable responses of receptor cells. Brain Res. 1973 Nov 9;62(1):253–259. doi: 10.1016/0006-8993(73)90637-9. [DOI] [PubMed] [Google Scholar]

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