Skip to main content
SpringerLink
Log in

Separation of ionic currents in the somatic membrane of frog sensory neurons

  • Articles
  • Published:
The Journal of Membrane Biology Aims and scope Submit manuscript

Summary

Electrical properties of isolated frog primary afferent neurons were examined by suction pipette technique, which combines internal perfusion with current or voltage clamp using a switching circuit with a single electrode. When K+ in the external and internal solutions was totally replaced with Cs+, extremely prolonged Ca spikes, lasting for 5 to 10 sec, and Na spikes, having a short plateau phase of 10 to 15 msec, were observed in Na+-free and Ca2+-free solutions, respectively. Under voltage clamp, Ca2+ current (I Ca) appeared at around −30 mV and maximum peak current was elicited at about 0 mV. With increasing test pulses to the positive side,I Ca became smaller and flattened but did not reverse. Increases of [Ca] o induced a hyperbolic increase ofI Ca and also shifted itsI-V curve along the voltage axis to the more positive direction. Internal perfusion of F− blockedI Ca time-dependently. The Ca channel was permeable to foreign divalent cations in the sequence ofI Ca>I Ba>I Sr≫I Mn>I Zn. Organic Ca-blockers equally depressed the divalent cation currents dose- and time-dependently without shifting theI-V relationships, while inorganic blockers suppressed these currents dose-dependently and the inhibition appeared much stronger in the order ofI Ba=I Sr>I Ca>I Mn=I Zn.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Adams, D.J., Gage, P.W. 1979. Characteristics of sodium and calcium conductance change produced by membrane depolarization in anAplysia neurone.J. Physiol. (London) 289:143–161

    Google Scholar 

  • Adams, D.J., Gage, P.W. 1980. Divalent ion current and the delayed potassium conductance in anAplysia neurone.J. Physiol. (London) 304:297–313

    Google Scholar 

  • Ahmed, Z., Connor, J.A. 1979. Measurement of calcium influx under voltage clamp in molluscan neurones using the metallochrome dye arsenazo III.J. Physiol. (London) 286:61–82

    Google Scholar 

  • Akaike, N., Brown, A.M., Dahl, G., Higashi, H. Isenberg, G., Tsuda, Y., Yatani, A. 1983a. Voltage-dependent activation of potassium current inHelix neurons by endogenous cellular calcium.J. Physiol. (London) 334:309–324

    Google Scholar 

  • Akaike, N., Brown, A.M., Nishi, K., Tsuda, Y., 1981a. Actions of verapamil, diltiazem and other divalent cations on the calcium-current ofHelix neurones.Br. J. Pharmacol 74:87–95

    PubMed  Google Scholar 

  • Akaike, N., Fishman, H.M., Lee, K.S., Moore, L.E., Brown, A.M. 1978a. The units of calcium conduction inHelix neurones.Nature (London) 274:379–381

    Google Scholar 

  • Akaike, N., Ito, H., Nishi, K., Oyama, Y. 1982. Further analysis of inhibitory effects of propranolol and local anaesthetics on the calcium current inHelix neurones.Br. J. Pharmacol 76:37–43

    PubMed  Google Scholar 

  • Akaike, N., Lee, K.S., Brown, A.M. 1978b. The calcium current ofHelix neuron.J. Gen. Physiol. 71:509–531

    PubMed  Google Scholar 

  • Akaike, N., Nishi, K., Oyama, Y. 1981b. Inhibitory effects of propranolol on the calcium current ofHelix neurones.Br. J. Pharmacol 73:431–434

    PubMed  Google Scholar 

  • Akaike, N., Nishi, K., Oyama, Y. 1981c. The manganese current ofHelix neuron.In: The Mechanism of Gated Calcium Transport across Biological Membranes. S.T. Ohnishi and M. Endo, editors. pp. 111–117. Academic Press, Honolulu

    Google Scholar 

  • Akaike, N., Nishi, K., Oyama, Y. 1983b. Characteristics of manganese current and its comparison with currents carried by other divalent cations in snail soma membranes.J. Membrane Biol. 76:287–295

    Google Scholar 

  • Bayer, R., Kaufmann, R., Mannhold, R. 1975. Inotropic and electrophysiological actions of verapamil and D-600 in mammalian myocardium. II. Pattern of inotropic effects of the optical isomers.Naunyn-Schmiedebergs Arch. Pharmacol 290:69–80

    PubMed  Google Scholar 

  • Brown, A.M., Morimoto, K., Tsuda, Y., Wilson, D. 1981. Calcium current-dependent and voltage-dependent inactivation of calcium channels inHelix aspersa.J. Physiol. (London) 320:193–218

    Google Scholar 

  • Byerly, L., Hagiwara, S. 1982. Calcium currents in internally perfused nerve cell bodies ofLimnea stagnalis.J. Physiol. (London) 322:503–528

    Google Scholar 

  • Connor, J.A. 1979. Calcium current in molluscan neurones: Measurement under conditions which maximize its visibility.J. Physiol. (London) 286:41–60

    Google Scholar 

  • Connor, J.A., Stevens, C.F. 1971. Voltage clamp studies of a transient outward membrane current in gastropod neural somata.J. Physiol. (London) 213:21–30

    Google Scholar 

  • Eckert, R., Lux, H.D. 1976. A voltage-sensitive persistent calcium conductance in neuronal somata ofHelix.J. Physiol. (London) 254:129–151

    Google Scholar 

  • Edwards, C. 1982. The selectivity of ion channels in nerve and muscle.Neuroscience 7:1335–1366

    PubMed  Google Scholar 

  • Fatt, P., Ginsborg, B.L. 1958. The ionic requirements for the production of action potentials in crustacean muscle fibers.J. Physiol. (London) 142:516–543

    Google Scholar 

  • Fenwick, E.M., Marty, A., Neher, E. 1981. Voltage clamp and single channel recording from bovine chromaffin cells.J. Physiol. (London) 319:100–101P

    Google Scholar 

  • Geduldig, D., Gruener, R. 1970. Voltage clamp of theAplysia giant neurone: Early sodium and calcium currents.J. Physiol. (London) 211:217–244

    Google Scholar 

  • Gorman, A.L.F., Thomas, M.V. 1978. Changes in the intracellular concentration of free calcium ions in a pace-maker neurone, measured with the metallochromic indicator dye arsenazo III.J. Physiol. (London) 275:357–376

    Google Scholar 

  • Gustafsson, B., Galvan, M., Grafe, P., Wigström, H. 1982. A transient outward current in a mammalian central neurone blocked by 4-aminopyridine.Nature (London) 299:252–254

    Google Scholar 

  • Hagiwara, S., Byerly, L. 1981. Calcium channel.Annu. Rev. Neurosci. 4:69–125

    PubMed  Google Scholar 

  • Hagiwara, S., Fukuda, J., Eaton, D. 1974. Membrane currents carried by Ca, Sr, and Ba in barnacle muscle fiber during voltage clamp.J. Gen. Physiol. 63:564–578

    Google Scholar 

  • Hagiwara, S., Takahashi, K. 1967. Surface density of calcium ions and calcium spikes in the barnacle muscle fiber membrane.J. Gen. Physiol. 50:583–601

    PubMed  Google Scholar 

  • Hattori, K., Akaike, N., Oomura, Y., Kuraoka, S. 1983. Separation of GABA-induced chloride current in the frog primary afferent neuron.Am. J. Physiol. (in press)

  • Hodgkin, A.L., Huxley, A.F. 1952. A quantitative description of membrane current and its application to conduction and excitation in nerve.J. Physiol. (London) 177:500–544

    Google Scholar 

  • Ito, M. 1957. The electrical activity of spinal ganglion cells investigated with intracellular microelectrodes.Jpn. J. Physiol. 7:297–323

    PubMed  Google Scholar 

  • Kawa, K. 1979. Zinc-dependent action potentials in giant neurons of the snailEuhadra quaestia.J. Membrane Biol. 49:325–344

    Google Scholar 

  • Kerkut, G.A., Walker, R.J., Lambert, J.D.C., Gayton, R.J., Loker, J.E. 1975. Mapping of nerve cells in the subaesophageal ganglia ofHelix aspersa.Comp. Biochem. Physiol. 50:1–25

    Google Scholar 

  • Kohlhardt, M., Bauer, B., Krause, H., Fleckenstein, A. 1972. A differentiation of the transmembrane Na and Ca channels in mammalian cardiac fibers by the use of specific inhibitors.Pfluegers Arch. ges. Physiol. 335:309–322

    Google Scholar 

  • Kohlhardt, M., Haastert, H.P., Krause, H. 1973. Evidence of non-specificity of the Ca channel in mammalian myocardial fibre membranes.Pfluegers Arch. ges. Physiol. 342:125–136

    Google Scholar 

  • Koketsu, K., Cerf, J.A., Nishi, S. 1959. Effect of quaternary ammonium ions on electrical activity of spinal ganglion cells in frog.J. Neurophysiol. 22:177–294

    PubMed  Google Scholar 

  • Koketsu, K., Koyama, I. 1962. Membrane responses of frog's spinal ganglion cells in calcium-free solutions.J. Physiol. (London) 163:1–12

    Google Scholar 

  • Kostyuk, P.G., Krishtal, O.A., Pidoplichko, V.I. 1975. Effect of internal fluoride and phosphate on membrane currents during intracellular dialysis of nerve cells.Nature (London) 257:691–693

    Google Scholar 

  • Kostyuk, P.G., Krishtal, O.A., Shakhovalov, Y.A. 1977. Separation of sodium and calcium currents in the somatic membrane of mollusc neurones.J. Physiol. (London) 270:545–568

    Google Scholar 

  • Lee, K.S., Akaike, N., Brown, A.M. 1978. Properties of internally perfused, voltage-clamped, isolated nerve cell bodies.J. Gen. Physiol. 71:489–507

    PubMed  Google Scholar 

  • Lee, K.S., Weeks, T.A., Kao, R.L., Akaike, N., Brown, A.M. 1979. Sodium current in single heart muscle cells.Nature (London) 278:269–271

    Google Scholar 

  • Magura, I.S. 1977. Long-lasting inward current in snail neurons in barium solutions in voltage-clamp conditions.J. Membrane Biol. 35:239–256

    Google Scholar 

  • Nishi, K., Akaike, N., Oyama, Y., Ito, H. 1983. Characteristics of calcium currents and actions of calcium-antagonists on calcium and potassium currents in theHelix neurons: Their specificity and potency.Cir. Res. (in press)

  • Nishi, S., Minota, S., Karczmar, A.G. 1974. Primary afferent neurones: The ionic mechanism of GABA-mediated depolarization.Neuropharmacology 13:215–219

    PubMed  Google Scholar 

  • Okamoto, H., Takahashi, K., Yamashita, N. 1977. Ionic currents through the membrane of the mammalian oocyte and their comparison with those in the tunicate and sea urchin.J. Physiol. (London) 267:465–495

    Google Scholar 

  • Okamoto, H., Takahashi, K., Yoshii, M. 1976. Membrane currents of the tunicate egg under the voltage-clamp condition.J. Physiol. (London) 254:607–638

    Google Scholar 

  • Oyama, Y., Nishi, K., Yatani, A., Akaike, N. 1982. Zinc current inHelix soma membrane.Comp. Biochem. Physiol. 72:403–410

    Google Scholar 

  • Reuter, H. 1973. Divalent cations as charge carriers in excitable membrane.Prog. Biophys. 26:1–43

    Google Scholar 

  • Satow, Y., Kung, C. 1979. Voltage sensitive Ca-channels and the transient inward current inParamecium tetraurelia.J. Exp. Biol. 78:149–161

    Google Scholar 

  • Shannon, R.D. 1976. Revised effective ionic radii and systematic studies of interatomic distances in halides and chalcogenides.Acta Cryst. 32:751–767

    Google Scholar 

  • Smith, S.J., Zucker, R.S. 1980. Aequorin response facilitation and intracellular calcium accumulation in molluscan neurones.J. Physiol. (London) 300:167–196

    Google Scholar 

  • Thompson, S.H. 1977. Three pharmacologically distinct potassium channels in molluscan neurones.J. Physiol. (London) 265:465–488

    Google Scholar 

  • Vereecke, J., Carmeliet, E. 1971. Sr action potentials in cardiac Purkinje fibres. I. Evidence for a regenerative increase in Sr conductance.Pfluegers Arch. ges. Physiol. 322:60–72

    Google Scholar 

  • Wilson, W.A., Goldner, M.M. 1975. Voltage clamping with a single microelectrode.J. Neurobiol. 6:411–422

    PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Physiology, Kyushu University Faculty of Dentistry, 812, Fukuoka, Japan

    S. Ishizuka

  2. Department of Physiology, Kyushu University Faculty of Medicine, 812, Fukuoka, Japan

    K. Hattori & N. Akaike

Authors
  1. S. Ishizuka
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. K. Hattori
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. N. Akaike
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ishizuka, S., Hattori, K. & Akaike, N. Separation of ionic currents in the somatic membrane of frog sensory neurons. J. Membrain Biol. 78, 19–28 (1984). https://doi.org/10.1007/BF01872528

Download citation

  • Received:

  • Revised:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01872528

Key Words

Search

Navigation