Abstract
Electrical resonance in vertebrate hair cells shapes receptor potentials and tunes each cell to a narrow band of frequencies. We have investigated the contribution of a potassium-selective inward rectifier (IR) to electrical resonance, isolating outward current carried by IR from other ionic currents active in the physiological voltage range (-75 to -30 mV) using a combination of potassium and calcium channel antagonists. IR expression is tightly regulated in the turtle's auditory epithelium, as revealed by the observation that its size declines systematically with resonant frequency. A critical feature of IR is the rapid inhibition produced by depolarization, which results in a negative slope in the steady-state current-voltage relation in the vicinity of the resting potential (-50 mV). The increasing block of outward current produced by depolarization is functionally equivalent to activating an inward current, suggesting that IR provides positive feedback and, in hair cells, serves an electrical function ordinarily reserved for voltage-dependent sodium and calcium currents. Additional support for this idea comes from the observation that superfusion with cesium selectively reduces IR and eliminates resonance in cells tuned to low frequencies and degrades resonant quality in cells tuned to more than 50 Hz.
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Selected References
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- Abeloff M. D., Rosen S. T., Luk G. D., Baylin S. B., Zeltzman M., Sjoerdsma A. Phase II trials of alpha-difluoromethylornithine, an inhibitor of polyamine synthesis, in advanced small cell lung cancer and colon cancer. Cancer Treat Rep. 1986 Jul;70(7):843–845. [PubMed] [Google Scholar]
- Art J. J., Fettiplace R., Fuchs P. A. Synaptic hyperpolarization and inhibition of turtle cochlear hair cells. J Physiol. 1984 Nov;356:525–550. doi: 10.1113/jphysiol.1984.sp015481. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Art J. J., Fettiplace R. Variation of membrane properties in hair cells isolated from the turtle cochlea. J Physiol. 1987 Apr;385:207–242. doi: 10.1113/jphysiol.1987.sp016492. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Art J. J., Fettiplace R., Wu Y. C. The effects of low calcium on the voltage-dependent conductances involved in tuning of turtle hair cells. J Physiol. 1993 Oct;470:109–126. doi: 10.1113/jphysiol.1993.sp019850. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Art J. J., Wu Y. C., Fettiplace R. The calcium-activated potassium channels of turtle hair cells. J Gen Physiol. 1995 Jan;105(1):49–72. doi: 10.1085/jgp.105.1.49. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bauer C. K., Meyerhof W., Schwarz J. R. An inward-rectifying K+ current in clonal rat pituitary cells and its modulation by thyrotrophin-releasing hormone. J Physiol. 1990 Oct;429:169–189. doi: 10.1113/jphysiol.1990.sp018250. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- 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]
- Fakler B., Brändle U., Glowatzki E., Weidemann S., Zenner H. P., Ruppersberg J. P. Strong voltage-dependent inward rectification of inward rectifier K+ channels is caused by intracellular spermine. Cell. 1995 Jan 13;80(1):149–154. doi: 10.1016/0092-8674(95)90459-x. [DOI] [PubMed] [Google Scholar]
- Farkas R. H., Nakajima S., Nakajima Y. Neurotensin excites basal forebrain cholinergic neurons: ionic and signal-transduction mechanisms. Proc Natl Acad Sci U S A. 1994 Mar 29;91(7):2853–2857. doi: 10.1073/pnas.91.7.2853. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fettiplace R., Crawford A. C. The origin of tuning in turtle cochlear hair cells. Hear Res. 1980 Jun;2(3-4):447–454. doi: 10.1016/0378-5955(80)90081-7. [DOI] [PubMed] [Google Scholar]
- Ficker E., Taglialatela M., Wible B. A., Henley C. M., Brown A. M. Spermine and spermidine as gating molecules for inward rectifier K+ channels. Science. 1994 Nov 11;266(5187):1068–1072. doi: 10.1126/science.7973666. [DOI] [PubMed] [Google Scholar]
- 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]
- 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]
- Hamill O. P., Marty A., Neher E., Sakmann B., Sigworth F. J. Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflugers Arch. 1981 Aug;391(2):85–100. doi: 10.1007/BF00656997. [DOI] [PubMed] [Google Scholar]
- Henley C. M., 3rd, Gerhardt H. J., Schacht J. Inhibition of inner ear ornithine decarboxylase by neomycin in-vitro. Brain Res Bull. 1987 Dec;19(6):695–698. doi: 10.1016/0361-9230(87)90056-6. [DOI] [PubMed] [Google Scholar]
- Hille B., Schwarz W. Potassium channels as multi-ion single-file pores. J Gen Physiol. 1978 Oct;72(4):409–442. doi: 10.1085/jgp.72.4.409. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Hudspeth A. J., Lewis R. S. A model for electrical resonance and frequency tuning in saccular hair cells of the bull-frog, Rana catesbeiana. J Physiol. 1988 Jun;400:275–297. doi: 10.1113/jphysiol.1988.sp017120. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Inoue M., Imanaga I. G protein-mediated inhibition of inwardly rectifying K+ channels in guinea pig chromaffin cells. Am J Physiol. 1993 Oct;265(4 Pt 1):C946–C956. doi: 10.1152/ajpcell.1993.265.4.C946. [DOI] [PubMed] [Google Scholar]
- Krishtal O. A., Pidoplichko V. I. A receptor for protons in the nerve cell membrane. Neuroscience. 1980;5(12):2325–2327. doi: 10.1016/0306-4522(80)90149-9. [DOI] [PubMed] [Google Scholar]
- Kubo Y., Baldwin T. J., Jan Y. N., Jan L. Y. Primary structure and functional expression of a mouse inward rectifier potassium channel. Nature. 1993 Mar 11;362(6416):127–133. doi: 10.1038/362127a0. [DOI] [PubMed] [Google Scholar]
- 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]
- 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]
- Matsuda H. Open-state substructure of inwardly rectifying potassium channels revealed by magnesium block in guinea-pig heart cells. J Physiol. 1988 Mar;397:237–258. doi: 10.1113/jphysiol.1988.sp016998. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Navaratnam D. S., Escobar L., Covarrubias M., Oberholtzer J. C. Permeation properties and differential expression across the auditory receptor epithelium of an inward rectifier K+ channel cloned from the chick inner ear. J Biol Chem. 1995 Aug 18;270(33):19238–19245. doi: 10.1074/jbc.270.33.19238. [DOI] [PubMed] [Google Scholar]
- Neher E., Lux H. D. Rapid changes of potassium concentration at the outer surface of exposed single neurons during membrane current flow. J Gen Physiol. 1973 Mar;61(3):385–399. doi: 10.1085/jgp.61.3.385. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- 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]
- 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]
- Penington N. J., Kelly J. S., Fox A. P. Whole-cell recordings of inwardly rectifying K+ currents activated by 5-HT1A receptors on dorsal raphe neurones of the adult rat. J Physiol. 1993 Sep;469:387–405. doi: 10.1113/jphysiol.1993.sp019819. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Salzer S. J., Mattox D. E., Brownell W. E. Cochlear damage and increased threshold in alpha-difluoromethylornithine (DFMO) treated guinea pigs. Hear Res. 1990 Jun;46(1-2):101–112. doi: 10.1016/0378-5955(90)90143-d. [DOI] [PubMed] [Google Scholar]
- Sanguinetti M. C., Kass R. S. Photoalteration of calcium channel blockade in the cardiac Purkinje fiber. Biophys J. 1984 May;45(5):873–880. doi: 10.1016/S0006-3495(84)84233-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Schweitzer L., Casseday J. H., Sjoerdsma A., McCann P. P., Bartolome J. V. Identification of polyamines in the cochlea of the rat and their potential role in hearing. Brain Res Bull. 1986 Feb;16(2):215–218. doi: 10.1016/0361-9230(86)90035-3. [DOI] [PubMed] [Google Scholar]
- 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]
- Vandenberg C. A. Inward rectification of a potassium channel in cardiac ventricular cells depends on internal magnesium ions. Proc Natl Acad Sci U S A. 1987 Apr;84(8):2560–2564. doi: 10.1073/pnas.84.8.2560. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Woodhull A. M. Ionic blockage of sodium channels in nerve. J Gen Physiol. 1973 Jun;61(6):687–708. doi: 10.1085/jgp.61.6.687. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wu Y. C., Art J. J., Goodman M. B., Fettiplace R. A kinetic description of the calcium-activated potassium channel and its application to electrical tuning of hair cells. Prog Biophys Mol Biol. 1995;63(2):131–158. doi: 10.1016/0079-6107(95)00002-5. [DOI] [PubMed] [Google Scholar]
- Yamaguchi K., Nakajima Y., Nakajima S., Stanfield P. R. Modulation of inwardly rectifying channels by substance P in cholinergic neurones from rat brain in culture. J Physiol. 1990 Jul;426:499–520. doi: 10.1113/jphysiol.1990.sp018151. [DOI] [PMC free article] [PubMed] [Google Scholar]
