Abstract
1. A three electrode voltage-clamp was used to investigate membrane currents in the skeletal muscle fibres of the stick insect, Carausius morosus. Contraction was blocked by hypertonic solutions. 2. Membrane currents elicited by step depolarizations consisted of an inward current, an early outward current and a delayed outward current. 3. The reversal potential of the delayed outward current did not change when SO4(2-) was substituted for Cl-, but shifted by 14.1 mV when [K]0 was increased from 20 mM to 40 mM in SO4(2-) solution, suggesting that the delayed current is carried by K+. Both early and delayed outward currents were substantially reduced by 120 mM-tetraethylammonium (TEA) ions. 4. The small size of the shift in the reversal potential of the delayed outward current with increased pulse duration suggests that the delayed current measured flows mainly across the surface membrane. 5. Increasing [Ca]o made the apparent reversal potential for the inward current (120 mM-TEA Ringer) more positive and increased the size of the maximum inward current. However, Ca-currents showed saturation with increasing [Ca]o, indicating that there is a site to which Ca ions bind during their passage through the membrane. The dissociation constant of this site was 7.3 mM at 0 mV and was voltage-dependent. 6. Inward currents were blocked by 1 mM-La3+ or Cd2+, or by substitution of Co2+ or Ni2+ for Mg2+. Strontium and barium were able to permeate the channel but Na+ and Mg2+ appear impermeant. 7. As expected from the low intracellular Ca concentration, the instantaneous current-voltage relation of the Ca current rectified strongly in the inward direction. 8. Both constant field theory and the simplest, single site, Eyring rate theory model predict the rectification of the instantaneous current-voltage relation. The rate theory model also predicts saturation of the Ca current with [Ca]o.
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- Adams D. J., Gage P. W. Characteristics of sodium and calcium conductance changes produced by membrane depolarization in an Aplysia neurone. J Physiol. 1979 Apr;289:143–161. doi: 10.1113/jphysiol.1979.sp012729. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Adrian R. H., Chandler W. K., Hodgkin A. L. Voltage clamp experiments in striated muscle fibres. J Physiol. 1970 Jul;208(3):607–644. doi: 10.1113/jphysiol.1970.sp009139. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- 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]
- Almers W. Potassium conductance changes in skeletal muscle and the potassium concentration in the transverse tubules. J Physiol. 1972 Aug;225(1):33–56. doi: 10.1113/jphysiol.1972.sp009928. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Armstrong C. M. Currents associated with the ionic gating structures in nerve membrane. Ann N Y Acad Sci. 1975 Dec 30;264:265–277. doi: 10.1111/j.1749-6632.1975.tb31488.x. [DOI] [PubMed] [Google Scholar]
- Armstrong C. M. Ionic pores, gates, and gating currents. Q Rev Biophys. 1974 May;7(2):179–210. doi: 10.1017/s0033583500001402. [DOI] [PubMed] [Google Scholar]
- Ascher P., Marty A., Neild T. O. Life time and elementary conductance of the channels mediating the excitatory effects of acetylcholine in Aplysia neurones. J Physiol. 1978 May;278:177–206. doi: 10.1113/jphysiol.1978.sp012299. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ashcroft F. M., Standen N. B., Stanfield P. R. Calcium currents in insect muscle [proceedings]. J Physiol. 1979 Jun;291:51P–52P. [PubMed] [Google Scholar]
- 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]
- Ashley C. C., Ridgway E. B. On the relationships between membrane potential, calcium transient and tension in single barnacle muscle fibres. J Physiol. 1970 Jul;209(1):105–130. doi: 10.1113/jphysiol.1970.sp009158. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Baker P. F., Hodgkin A. L., Ridgway E. B. Depolarization and calcium entry in squid giant axons. J Physiol. 1971 Nov;218(3):709–755. doi: 10.1113/jphysiol.1971.sp009641. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Baker P. F., Rink T. J. Catecholamine release from bovine adrenal medulla in response to maintained depolarization. J Physiol. 1975 Dec;253(2):593–620. doi: 10.1113/jphysiol.1975.sp011209. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Beeler G. W., Jr, Reuter H. The relation between membrane potential, membrane currents and activation of contraction in ventricular myocardial fibres. J Physiol. 1970 Mar;207(1):211–229. doi: 10.1113/jphysiol.1970.sp009057. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Brandt B. L., Hagiwara S., Kidokoro Y., Miyazaki S. Action potentials in the rat chromaffin cell and effects of acetylcholine. J Physiol. 1976 Dec;263(3):417–439. doi: 10.1113/jphysiol.1976.sp011638. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Caputo C., Fernandez de Bolaños P. Membrane potential, contractile activation and relaxation rates in voltage clamped short muscle fibres of the frog. J Physiol. 1979 Apr;289:175–189. doi: 10.1113/jphysiol.1979.sp012731. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Eckert R. Bioelectric control of ciliary activity. Science. 1972 May 5;176(4034):473–481. doi: 10.1126/science.176.4034.473. [DOI] [PubMed] [Google Scholar]
- Endo M. Calcium release from the sarcoplasmic reticulum. Physiol Rev. 1977 Jan;57(1):71–108. doi: 10.1152/physrev.1977.57.1.71. [DOI] [PubMed] [Google Scholar]
- FATT P., GINSBORG B. L. The ionic requirements for the production of action potentials in crustacean muscle fibres. J Physiol. 1958 Aug 6;142(3):516–543. doi: 10.1113/jphysiol.1958.sp006034. [DOI] [PMC free article] [PubMed] [Google Scholar]
- FRANKENHAEUSER B., HODGKIN A. L. The action of calcium on the electrical properties of squid axons. J Physiol. 1957 Jul 11;137(2):218–244. doi: 10.1113/jphysiol.1957.sp005808. [DOI] [PMC free article] [PubMed] [Google Scholar]
- FRANKENHAEUSER B., HODGKIN A. L. The after-effects of impulses in the giant nerve fibres of Loligo. J Physiol. 1956 Feb 28;131(2):341–376. doi: 10.1113/jphysiol.1956.sp005467. [DOI] [PMC free article] [PubMed] [Google Scholar]
- FRANKENHAEUSER B. Sodium permeability in toad nerve and in squid nerve. J Physiol. 1960 Jun;152:159–166. doi: 10.1113/jphysiol.1960.sp006477. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fukuda J., Furuyama S., Kawa K. Calcium dependent action potentials in skeletal muscle fibres of a beetle larva, Xylotrupes dichotomus. J Insect Physiol. 1977;23(3):367–374. doi: 10.1016/0022-1910(77)90275-x. [DOI] [PubMed] [Google Scholar]
- Goldman D. E. POTENTIAL, IMPEDANCE, AND RECTIFICATION IN MEMBRANES. J Gen Physiol. 1943 Sep 20;27(1):37–60. doi: 10.1085/jgp.27.1.37. [DOI] [PMC free article] [PubMed] [Google Scholar]
- HAGIWARA S., NAKA K. I. THE INITIATION OF SPIKE POTENTIAL IN BARNACLE MUSCLE FIBERS UNDER LOW INTRACELLULAR CA++. J Gen Physiol. 1964 Sep;48:141–162. doi: 10.1085/jgp.48.1.141. [DOI] [PMC free article] [PubMed] [Google Scholar]
- HODGKIN A. L., KATZ B. The effect of sodium ions on the electrical activity of giant axon of the squid. J Physiol. 1949 Mar 1;108(1):37–77. doi: 10.1113/jphysiol.1949.sp004310. [DOI] [PMC free article] [PubMed] [Google Scholar]
- HOWARTH J. V. The behaviour of frog muscle in hypertonic solutions. J Physiol. 1958 Nov 10;144(1):167–175. doi: 10.1113/jphysiol.1958.sp006093. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hagiwara S. Ca spike. Adv Biophys. 1973;4:71–102. [PubMed] [Google Scholar]
- 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]
- Hagiwara S., Ozawa S., Sand O. Voltage clamp analysis of two inward current mechanisms in the egg cell membrane of a starfish. J Gen Physiol. 1975 May;65(5):617–644. doi: 10.1085/jgp.65.5.617. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hagiwara S., Takahashi K. Surface density of calcium ions and calcium spikes in the barnacle muscle fiber membrane. J Gen Physiol. 1967 Jan;50(3):583–601. doi: 10.1085/jgp.50.3.583. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Heistracher P., Hunt C. C. The relation of membrane changes ot contraction in twitch muscle fibres. J Physiol. 1969 May;201(3):589–611. doi: 10.1113/jphysiol.1969.sp008774. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hencek M., Zachar J. Calcium currents and conductances in the msucle membrane of the crayfish. J Physiol. 1977 Jun;268(1):51–71. doi: 10.1113/jphysiol.1977.sp011846. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hencek M., Zachar J., Zacharová D. Membrane currents in a calcium type muscle membrane under voltage clamp. Physiol Bohemoslov. 1978;27(5):457–466. [PubMed] [Google Scholar]
- Hille B. Ionic selectivity, saturation, and block in sodium channels. A four-barrier model. J Gen Physiol. 1975 Nov;66(5):535–560. doi: 10.1085/jgp.66.5.535. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Johnson E. A., Lieberman M. Heart: excitation and contraction. Annu Rev Physiol. 1971;33:479–532. doi: 10.1146/annurev.ph.33.030171.002403. [DOI] [PubMed] [Google Scholar]
- Kass R. S., Siegelbaum S. A., Tsien R. W. Three-micro-electrode voltage clamp experiments in calf cardiac Purkinje fibres: is slow inward current adequately measured? J Physiol. 1979 May;290(2):201–225. doi: 10.1113/jphysiol.1979.sp012768. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Keynes R. D., Bezanilla F., Taylor R. E., Rojas E. The rate of action of tetrodotoxin on sodium conductance in the squid giant axon. Philos Trans R Soc Lond B Biol Sci. 1975 Jun 10;270(908):365–375. doi: 10.1098/rstb.1975.0016. [DOI] [PubMed] [Google Scholar]
- Keynes R. D., Rojas E. Kinetics and steady-state properties of the charged system controlling sodium conductance in the squid giant axon. J Physiol. 1974 Jun;239(2):393–434. doi: 10.1113/jphysiol.1974.sp010575. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Keynes R. D., Rojas E., Taylor R. E., Vergara J. Calcium and potassium systems of a giant barnacle muscle fibre under membrane potential control. J Physiol. 1973 Mar;229(2):409–455. doi: 10.1113/jphysiol.1973.sp010146. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kostyuk P. G. Calcium ionic channels in electrically excitable membrane. Neuroscience. 1980;5(6):945–959. doi: 10.1016/0306-4522(80)90178-5. [DOI] [PubMed] [Google Scholar]
- 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]
- Krishtal O. A., Pidoplichko V. I., Shakhovalov Y. A. Conductance of the calcium channel in the membrane of snail neurones. J Physiol. 1981 Jan;310:423–434. doi: 10.1113/jphysiol.1981.sp013558. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Llinás R., Hess R. Tetrodotoxin-resistant dendritic spikes in avian Purkinje cells. Proc Natl Acad Sci U S A. 1976 Jul;73(7):2520–2523. doi: 10.1073/pnas.73.7.2520. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- 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]
- Meves H. The ionic requirements for the production of action potentials in helix pomatia neurones. Pflugers Arch. 1968;304(3):215–241. doi: 10.1007/BF00592126. [DOI] [PubMed] [Google Scholar]
- Meves H., Vogel W. Calcium inward currents in internally perfused giant axons. J Physiol. 1973 Nov;235(1):225–265. doi: 10.1113/jphysiol.1973.sp010386. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mounier Y., Vassort G. Evidence for a transient potassium membrane current dependent on calcium influx in crab muscle fibre. J Physiol. 1975 Oct;251(3):609–625. doi: 10.1113/jphysiol.1975.sp011111. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mounier Y., Vassort G. Initial and delayed membrane currents in crab muscle fibre under voltage-clamp conditions. J Physiol. 1975 Oct;251(3):589–608. doi: 10.1113/jphysiol.1975.sp011110. [DOI] [PMC free article] [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]
- 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]
- Okamoto H., Takahashi K., Yoshii M. Two components of the calcium current in the egg cell membrane of the tunicate. J Physiol. 1976 Feb;255(2):527–561. doi: 10.1113/jphysiol.1976.sp011294. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Peachey L. D. The sarcoplasmic reticulum and transverse tubules of the frog's sartorius. J Cell Biol. 1965 Jun;25(3 Suppl):209–231. doi: 10.1083/jcb.25.3.209. [DOI] [PubMed] [Google Scholar]
- Reuter H., Scholz H. A study of the ion selectivity and the kinetic properties of the calcium dependent slow inward current in mammalian cardiac muscle. J Physiol. 1977 Jan;264(1):17–47. doi: 10.1113/jphysiol.1977.sp011656. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ritchie J. M. Binding of tetrodotoxin and saxitoxin to sodium channels. Philos Trans R Soc Lond B Biol Sci. 1975 Jun 10;270(908):319–336. doi: 10.1098/rstb.1975.0012. [DOI] [PubMed] [Google Scholar]
- Salkoff L., Wyman R. Outward currents in developing Drosophila flight muscle. Science. 1981 Apr 24;212(4493):461–463. doi: 10.1126/science.6259736. [DOI] [PubMed] [Google Scholar]
- Siri L. N., Sánchez J. A., Stefani E. Effect of glycerol treatment on the calcium current of frog skeletal muscle. J Physiol. 1980 Aug;305:87–96. doi: 10.1113/jphysiol.1980.sp013351. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Standen N. B. Voltage-clamp studies of the calcium inward current in an identified snail neurone: comparison with the sodium inward current. J Physiol. 1975 Jul;249(2):253–268. doi: 10.1113/jphysiol.1975.sp011014. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Stanfield P. R., Ashcroft F. M., Plant T. D. Gating of a muscle K+ channel and its dependence on the permeating ion species. Nature. 1981 Feb 5;289(5797):509–511. doi: 10.1038/289509a0. [DOI] [PubMed] [Google Scholar]
- Stanfield P. R. The effect of the tetraethylammonium ion on the delayed currents of frog skeletal muscle. J Physiol. 1970 Jul;209(1):209–229. doi: 10.1113/jphysiol.1970.sp009163. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Stanfield P. R. The effect of zinc ions on the gating of the delayed potassium conductance of frog sartorius muscle. J Physiol. 1975 Oct;251(3):711–735. doi: 10.1113/jphysiol.1975.sp011118. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- 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]
- Tomita T. Electrophysiology of mammalian smooth muscle. Prog Biophys Mol Biol. 1975;30(2-3):185–203. doi: 10.1016/0079-6107(76)90009-2. [DOI] [PubMed] [Google Scholar]
- Van Helden D., Hamill O. P., Gage P. W. Permeant cations alter endplate channel characteristics. Nature. 1977 Oct 20;269(5630):711–713. doi: 10.1038/269711a0. [DOI] [PubMed] [Google Scholar]
- WEIDMANN S. The electrical constants of Purkinje fibres. J Physiol. 1952 Nov;118(3):348–360. doi: 10.1113/jphysiol.1952.sp004799. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Washio H. The ionic requirements for the initiation of action potentials in insect muscle fibers. J Gen Physiol. 1972 Feb;59(2):121–134. doi: 10.1085/jgp.59.2.121. [DOI] [PMC free article] [PubMed] [Google Scholar]