Skip to main content
The Journal of Physiology logoLink to The Journal of Physiology
. 1996 Sep 15;495(Pt 3):665–679. doi: 10.1113/jphysiol.1996.sp021624

Inwardly rectifying currents in hair cells and supporting cells in the goldfish sacculus.

I Sugihara 1, T Furukawa 1
PMCID: PMC1160773  PMID: 8887774

Abstract

1. Inwardly rectifying ionic currents were studied using patch-clamp recording methods in oscillatory-type and spike-type hair cells and supporting cells dissociated from the goldfish sacculus. These cells had different types of inwardly rectifying currents. The biophysical properties of these currents were investigated. 2. A unique potassium current (Isc) was the sole ionic current recognized in supporting cells. Isc was active throughout the membrane potential range between +30 and -170 mV, but showed weak inward rectification and no inactivation. 3. In spike-type hair cells, inwardly rectifying current (Ik1) was selectively permeable to K+ (K+:Na+ permeability ratio, 1:0.0021). Ik1 could underlie the high negative resting potential of these hair cells because it is partially active at this potential. The strong inward rectification of Ik1 contributed to the low negative plateau potential seen in spike-type hair cells. 4. In oscillatory-type hair cells, hyperpolarization-activated potassium-sodium current (Ih), which had properties similar to that in photoreceptor and other neurons, was present instead of inwardly rectifying K+ current. 5. In the cell-attached and inside-out modes with 125 microM external K+ ([K+]o), IK1 channel had a unitary conductance of 27 pS and showed inactivation with increasing hyperpolarization. Putative Ih and Iso single channels had unitary conductances of 7 and 61 pS, respectively, in the cell-attached mode with 125 microM Ko+.

Full text

PDF
665

Images in this article

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Barres B. A., Chun L. L., Corey D. P. Ion channel expression by white matter glia: I. Type 2 astrocytes and oligodendrocytes. Glia. 1988;1(1):10–30. doi: 10.1002/glia.440010104. [DOI] [PubMed] [Google Scholar]
  2. Carmeliet E. Induction and removal of inward-going rectification in sheep cardiac Purkinje fibres. J Physiol. 1982 Jun;327:285–308. doi: 10.1113/jphysiol.1982.sp014232. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. 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]
  4. ENGER P. S. IONIC COMPOSITION OF THE CRANIAL AND LABYRINTHINE FLUIDS AND SACCULAR D.C. POTENTIALS IN FISH. Comp Biochem Physiol. 1964 Jan;11:131–137. doi: 10.1016/0010-406x(64)90100-8. [DOI] [PubMed] [Google Scholar]
  5. Fuchs P. A., Evans M. G. Potassium currents in hair cells isolated from the cochlea of the chick. J Physiol. 1990 Oct;429:529–551. doi: 10.1113/jphysiol.1990.sp018271. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Fuchs P. A., Murrow B. W. Cholinergic inhibition of short (outer) hair cells of the chick's cochlea. J Neurosci. 1992 Mar;12(3):800–809. doi: 10.1523/JNEUROSCI.12-03-00800.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Furukawa T., Ishii Y. Neurophysiological studies on hearing in goldfish. J Neurophysiol. 1967 Nov;30(6):1377–1403. doi: 10.1152/jn.1967.30.6.1377. [DOI] [PubMed] [Google Scholar]
  8. Furukawa T. Slow depolarizing response from supporting cells in the goldfish saccule. J Physiol. 1985 Sep;366:107–117. doi: 10.1113/jphysiol.1985.sp015787. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. 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]
  10. Hama K., Saito K. Gap junctions between the supporting cells in some acoustico-vestibular receptors. J Neurocytol. 1977 Feb;6(1):1–12. doi: 10.1007/BF01175410. [DOI] [PubMed] [Google Scholar]
  11. Hestrin S. The properties and function of inward rectification in rod photoreceptors of the tiger salamander. J Physiol. 1987 Sep;390:319–333. doi: 10.1113/jphysiol.1987.sp016703. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Holt J. R., Eatock R. A. Inwardly rectifying currents of saccular hair cells from the leopard frog. J Neurophysiol. 1995 Apr;73(4):1484–1502. doi: 10.1152/jn.1995.73.4.1484. [DOI] [PubMed] [Google Scholar]
  13. Hudspeth A. J., Corey D. P. Sensitivity, polarity, and conductance change in the response of vertebrate hair cells to controlled mechanical stimuli. Proc Natl Acad Sci U S A. 1977 Jun;74(6):2407–2411. doi: 10.1073/pnas.74.6.2407. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Kakei M., Noma A. Adenosine-5'-triphosphate-sensitive single potassium channel in the atrioventricular node cell of the rabbit heart. J Physiol. 1984 Jul;352:265–284. doi: 10.1113/jphysiol.1984.sp015290. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Koumi S., Sato R., Hayakawa H. Modulation of voltage-dependent inactivation of the inwardly rectifying K+ channel by chloramine-T. Eur J Pharmacol. 1994 Jun 13;258(3):281–284. doi: 10.1016/0014-2999(94)90493-6. [DOI] [PubMed] [Google Scholar]
  16. Lopatin A. N., Makhina E. N., Nichols C. G. Potassium channel block by cytoplasmic polyamines as the mechanism of intrinsic rectification. Nature. 1994 Nov 24;372(6504):366–369. doi: 10.1038/372366a0. [DOI] [PubMed] [Google Scholar]
  17. Matsuda H., Saigusa A., Irisawa H. Ohmic conductance through the inwardly rectifying K channel and blocking by internal Mg2+. Nature. 1987 Jan 8;325(7000):156–159. doi: 10.1038/325156a0. [DOI] [PubMed] [Google Scholar]
  18. Matsuura S., Ikeda K., Furukawa T. Effects of Na + , K + , and ouabain on microphonic potentials of the goldfish inner ear. Jpn J Physiol. 1971 Oct;21(5):563–578. doi: 10.2170/jjphysiol.21.563. [DOI] [PubMed] [Google Scholar]
  19. McCormick D. A., Pape H. C. Properties of a hyperpolarization-activated cation current and its role in rhythmic oscillation in thalamic relay neurones. J Physiol. 1990 Dec;431:291–318. doi: 10.1113/jphysiol.1990.sp018331. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Mroz E. A., Nissim K. R., Lechene C. Rapid resting ion fluxes in goldfish hair cells are balanced by (Na+,K+)-ATPase. Hear Res. 1993 Oct;70(1):22–30. doi: 10.1016/0378-5955(93)90049-7. [DOI] [PubMed] [Google Scholar]
  21. Newman E. A. Inward-rectifying potassium channels in retinal glial (Müller) cells. J Neurosci. 1993 Aug;13(8):3333–3345. doi: 10.1523/JNEUROSCI.13-08-03333.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Newman E. A. Membrane physiology of retinal glial (Müller) cells. J Neurosci. 1985 Aug;5(8):2225–2239. doi: 10.1523/JNEUROSCI.05-08-02225.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Nichols C. G., Ho K., Hebert S. Mg(2+)-dependent inward rectification of ROMK1 potassium channels expressed in Xenopus oocytes. J Physiol. 1994 May 1;476(3):399–409. doi: 10.1113/jphysiol.1994.sp020141. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Oesterle E. C., Dallos P. Intracellular recordings from supporting cells in the guinea pig cochlea: DC potentials. J Neurophysiol. 1990 Aug;64(2):617–636. doi: 10.1152/jn.1990.64.2.617. [DOI] [PubMed] [Google Scholar]
  25. Ohmori H. Inactivation kinetics and steady-state current noise in the anomalous rectifier of tunicate egg cell membranes. J Physiol. 1978 Aug;281:77–99. doi: 10.1113/jphysiol.1978.sp012410. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. 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]
  27. Orkand R. K., Nicholls J. G., Kuffler S. W. Effect of nerve impulses on the membrane potential of glial cells in the central nervous system of amphibia. J Neurophysiol. 1966 Jul;29(4):788–806. doi: 10.1152/jn.1966.29.4.788. [DOI] [PubMed] [Google Scholar]
  28. Ransom C. B., Sontheimer H. Biophysical and pharmacological characterization of inwardly rectifying K+ currents in rat spinal cord astrocytes. J Neurophysiol. 1995 Jan;73(1):333–346. doi: 10.1152/jn.1995.73.1.333. [DOI] [PubMed] [Google Scholar]
  29. Sakmann B., Trube G. Voltage-dependent inactivation of inward-rectifying single-channel currents in the guinea-pig heart cell membrane. J Physiol. 1984 Feb;347:659–683. doi: 10.1113/jphysiol.1984.sp015089. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Santos-Sacchi J., Dallos P. Intercellular communication in the supporting cells of the organ of Corti. Hear Res. 1983 Mar;9(3):317–326. doi: 10.1016/0378-5955(83)90034-5. [DOI] [PubMed] [Google Scholar]
  31. Santos-Sacchi J. Isolated supporting cells from the organ of Corti: some whole cell electrical characteristics and estimates of gap junctional conductance. Hear Res. 1991 Mar;52(1):89–98. doi: 10.1016/0378-5955(91)90190-k. [DOI] [PubMed] [Google Scholar]
  32. Shigemoto T., Ohmori H. Muscarinic receptor hyperpolarizes cochlear hair cells of chick by activating Ca(2+)-activated K+ channels. J Physiol. 1991 Oct;442:669–690. doi: 10.1113/jphysiol.1991.sp018814. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Standen N. B., Stanfield P. R. Potassium depletion and sodium block of potassium currents under hyperpolarization in frog sartorius muscle. J Physiol. 1979 Sep;294:497–520. doi: 10.1113/jphysiol.1979.sp012943. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Stelling J. W., Jacob T. J. The inward rectifier K+ current underlies oscillatory membrane potential behaviour in bovine pigmented ciliary epithelial cells. J Physiol. 1992 Dec;458:439–456. doi: 10.1113/jphysiol.1992.sp019426. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Sugihara I. Calcium-activated potassium channels in goldfish hair cells. J Physiol. 1994 May 1;476(3):373–390. doi: 10.1113/jphysiol.1994.sp020139. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Sugihara I., Furukawa T. Morphological and functional aspects of two different types of hair cells in the goldfish sacculus. J Neurophysiol. 1989 Dec;62(6):1330–1343. doi: 10.1152/jn.1989.62.6.1330. [DOI] [PubMed] [Google Scholar]
  37. Sugihara I., Furukawa T. Potassium currents underlying the oscillatory response in hair cells of the goldfish sacculus. J Physiol. 1995 Dec 1;489(Pt 2):443–453. doi: 10.1113/jphysiol.1995.sp021064. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Sugihara I., Furukawa T. Quickly flickering inwardly rectifying K channels in goldfish hair cell membrane. Neurosci Res. 1986 Feb;3(3):261–267. doi: 10.1016/0168-0102(86)90009-x. [DOI] [PubMed] [Google Scholar]
  39. Taglialatela M., Wible B. A., Caporaso R., Brown A. M. Specification of pore properties by the carboxyl terminus of inwardly rectifying K+ channels. Science. 1994 May 6;264(5160):844–847. doi: 10.1126/science.8171340. [DOI] [PubMed] [Google Scholar]

Articles from The Journal of Physiology are provided here courtesy of The Physiological Society

RESOURCES