Skip to main content
Log in

Two components of Ca-dependent potassium current in identified neurones ofAplysia californica

  • Excitable Tissues and Central Nervous Physiology
  • Published:
Pflügers Archiv Aims and scope Submit manuscript

    We’re sorry, something doesn't seem to be working properly.

    Please try refreshing the page. If that doesn't work, please contact support so we can address the problem.

Abstract

Outward tail currents measured inAplysia neurones after termination of depolarizing voltage-clamp pulses consist of rapidly decaying voltage-dependent K currents and slow tail currents of much slower time course. The rapidly decaying voltage-dependent tail currents were blocked with aminopyridines, and measurements of the slow tail currents were made following decay of any residual rapid tail currents. The slow tail current exhibited two components of differing sensitivity to externally applied tetraethylammonium (TEA) ions. In some neurones of the abdominal ganglion (L-2, L-4), virtually all of the slow tail current was resistant to blockage by TEA, while in others (L-3, L-6) 80% or more of the slow tail current was blocked by low TEA concentrations (K D<1 mM), the remaining slow tail current being resistant to TEA. This TEA-resistant slow tail current was identified as a K current because it reversed near the K equilibrium potential (E K), the reversal potential was shifted by changes in the external K concentration, and it could be blocked by injection of Cs+. It was abolished by replacement of external Ca2+ by Co2+ or Ba2+, by addition of Cd2+, or by injection of EGTA, and thus determined to be a Ca-dependent current. Intracellular injection of TEA or external application of aminopyridine or apamine had little or no effect on the TEA-resistant slow tail current. Quinidine reduced the TEA-sensitive, but not the TEA-resistant current. Both the TEA-sensitive and the TEA-resistant components of the slow tail current exhibited similar time courses of decay. Thus, neurones ofAplysia appear to contain different proportions of two classes of Ca-dependent K channels that differ in their sensitivity to certain channel blocking agents.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Adams WB, Levitan IB (1981) Ionic dependence and charge carriers of the currents underlying bursting inAplysia neuron R15. Soc Neurosci Abstr 5:239

    Google Scholar 

  • Aldrich RW, Getting PA, Thompson SH (1979) Inactivation of delayed outward current in molluscan neurone somata. J Physiol 291:507–530

    Google Scholar 

  • Atwater I, Dawson CM, Ribalet B, Rojas E (1979) Potassium permeability activated by intracellular calcium ion concentration in the pancreatic β cell. J Physiol 288:575–588

    Google Scholar 

  • Barish ME, Thompson SH (1983) Calcium buffering and slow recovery kinetics of calcium-dependent outward current in molluscan neurones. J Physiol 337:201–219

    Google Scholar 

  • Barrett EF, Barrett JN (1976) Separation of two voltage-sensitive potassium currents, and demonstration of a tetrodotoxin-resistant calcium current in frog motoneurones. J Physiol 255:737–774

    Google Scholar 

  • Barrett JN, Magleby KL, Pallotta BS (1982) Properties of single Ca-activated potassium channels in cultured rat muscle. J Physiol 331:211–230

    Google Scholar 

  • Brehm P, Eckert R (1978) Calcium entry leads to inactivation of calcium channel inParamecium. Science NY 202:1203–1206

    Google Scholar 

  • Burgess GM, Claret M, Jenkinson DM (1981) Effects of quinine and apamin on the calcium-dependent potassium permeability of mammalian hepatocytes and red cells. J Physiol 317:67–90

    Google Scholar 

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

    Google Scholar 

  • Chad J, Eckert R, Ewald D (1984) Kinetics of Ca-dependent inactivation of calcium current in neurones ofAplysia californica. J Physiol 347:279–300

    Google Scholar 

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

    Google Scholar 

  • Deitmer JW, Eckert R (1984) Different sensitivity to TEA reveals two components of Ca-dependent K current inAplysia neurones. Pflügers Arch Suppl 400:R40

    Google Scholar 

  • Doroshenko PA, Kostyuk PG, Tsyndrenko AY (1979) Investigation of the TEA-resistant outward current in the somatic membrane of perfused nerve cells. Neirofiziologiya 11:460–468 [translated in Neurophysiology 11:341–348 (1980)]

    Google Scholar 

  • Eckert R, Ewald D (1983) Calcium tail currents in voltage-clamped intact nerve cell bodies ofAplysia californica. J Physiol 345:533–548

    Google Scholar 

  • Eckert R, Tillotson D (1981) Calcium-mediated inactivation of the calcium conductance in caesium-loaded giant neurones ofAplysia californica. J Physiol 314:265–280

    Google Scholar 

  • Gardos G (1959) The role of calcium in the potassium permeability of human erythrocytes. Acta Physiol Acad Sci Hung 15:121–125

    Google Scholar 

  • Groman ALF, Hermann A (1982) Quantitative differences in the currents of bursting and beating molluscan pace-maker neurones. J Physiol 333:681–699

    Google Scholar 

  • Gorman ALF, Hermann A, Thomas MV (1981) Intracellular calcium and the control of neuronal pace-maker activity. Fedn Proc 40:2233–2239

    Google Scholar 

  • Gorman ALF, Thomas MV (1980) Potassium conductance and internal calcium accumulation in a molluscan neurone. J Physiol 308:287–313

    Google Scholar 

  • Gorman ALF, Woolum JC (1981) Time dependence of the calcium-activated potassium current. Biophys J 36:297–302

    Google Scholar 

  • Gorman ALF, Woolum JC, Cornwall MC (1982) Selectivity of the Ca2+-activated and light dependent K+ channels for monovalent cations. Biophys J 38:319–322

    Google Scholar 

  • Habermann E (1972) Bee and wasp venoms. Science NY 177:314–322

    Google Scholar 

  • Hagiwara S (1975) Ca-dependent action potential. In: Eisenman G (ed) Membranes, vol 3. Marcell Dekker, New York

    Google Scholar 

  • Hagiwara S, Saito N (1959) Voltage-current relations in nerve cell membrane ofOnchidium verruculatum. J physiol 148:161–179

    Google Scholar 

  • Hermann A, Gorman ALF (1978) Blockage of the Ca2+-induced K+ current by TEA in molluscan bursting pacemaker neurons. Biophys J 21:52a

    Google Scholar 

  • Hermann A, Gorman ALF (1979a) External and internal effects of tetraethylammonium on voltage-dependent and Ca-dependent K+ current components in molluscan pacemaker neurons. Neurosci Lett 12:87–92

    Google Scholar 

  • Hermann A Gorman ALF (1979b) Blockade of voltage-dependent and Ca2+-dependent K+ currents by internal Ba2+ in molluscan pacemaker neurons. Experientia 35:229–231

    Google Scholar 

  • Hermann A, Gorman ALF (1981a) Effects of 4-aminopyridine on potassium currents in a molluscan neuron. J Gen Physiol 78:63–86

    Google Scholar 

  • Hermann A, Gorman ALF (1981b) Effects of tetraethylammonium on potassium currents in a molluscan neuron. J Gen Physiol 78:87–110

    Google Scholar 

  • Hermann A, Gorman ALF (1984) Action of quinidine on ionic currents of molluscan pacemaker neurons. J Gen Physiol 83:919–940

    Google Scholar 

  • Johnston D (1980) Voltage, temperature and ionic dependence of the slow outward current inAplysia burst-firing neurones. J Physiol 289:145–157

    Google Scholar 

  • Junge D, Stephens CL (1973) Cyclic variation of potassium conductance in a burst-generating neurone inAplysia. J Physiol 235:155–181

    Google Scholar 

  • Kostyuk PG, Krishtal OA, Pidoplichko VI (1975) Effect of internal fluoride and phosphate on membrane currents during intracellular dialysis of nerve cells. Nature (Lond) 257:691–693

    Google Scholar 

  • Kostyuk PG, Krishtal OA, Shakhovalov YA (1977) Separation of sodium and calcium currents in the membrane of mollusc neurones. J Physiol 270:545–568

    Google Scholar 

  • Kramer RH, Zucker RS (1983) Inactivation of persistant inward current mediates post-burst hyperpolarization inAplysia bursting pacemaker neurons. Soc Neurosci Abstr 9:510

    Google Scholar 

  • Latorre R, Vergara C, Hidalgo C (1982) Reconstitution in planar lipid bilayers of a Ca2+-dependent K+ channel from transverse tubule membranes isolated from rabbit skeletal muscle. Proc Natl Acad Sci USA 79:805–809

    Google Scholar 

  • Lew VL, Ferreira HG (1978) Calcium transport and the properties of a calcium-activated potassium channel in red blood cell membranes. Curr Top Membr Trans. 10:218–278

    Google Scholar 

  • Lewis RS, Hudspeth AJ (1983) Voltage- and ion-dependent conductances in solitary vertebrate hair cells. Nature (Lond) 304:538–541

    Google Scholar 

  • Lux HD, Hofmeier G (1979) The voltage dependence of the Ca mediated K current [I K(Ca)] in Helix neurons. Neurosci Lett (Suppl) 3:582

    Google Scholar 

  • Lux HD, Neher E, Marty A (1981) Single channel activity associated with the calcium dependent outward current in Helix pomatia. Pflügers Arch 389:293–295

    Google Scholar 

  • Meech RW (1972) Intracellular calcium injection causes increased potassium conductance inAplysia nerve cells. Comp Biochem Physyiol 42A:493–499

    Google Scholar 

  • Meech RW (1978) Calcium-dependent potassium activation in nervous tissues. Ann Rev Biophys Bioeng 7:1–18

    Google Scholar 

  • Meech RW, Standen NB (1975) Potassium activation in Helix neurones under voltage clamp: a component mediated by calcium influx. J Physiol (Lond) 249:211–239

    Google Scholar 

  • Meech RW, Strumwasser F (1970) Intracellular calcium injection activates potassium conductance inAplysia nerve cells. Fedn Proc 29:234

    Google Scholar 

  • Moolenaar WH, Spector F (1979) The calcium current and the activation of a slow potassium conductance in voltage-clamped mouse neuroblastoma cells. J Physiol 292:307–323

    Google Scholar 

  • Neher E (1971) Two fast transient current components during voltage clamp on snail neurons. J Gen Physiol 58:36–53

    Google Scholar 

  • Smith SJ (1980) Ca++ regulation in gastropod nerve cell bodies. In: Koester J, Byrne JH (eds) Molluscan nerve cells: from biophysics to behavior. Cold Spring Harbor Laboratory, Cold Spring Harbor

    Google Scholar 

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

    Google Scholar 

  • Standen NB (1981) Ca channel inactivation by intracellular Ca injection intoHelix neurones. Nature (Lond) 293:158–159

    Google Scholar 

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

    Google Scholar 

  • Whittam R (1968) Control of membrane permeability to potassium in red blood cells. Nature (Lond) 219:610

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Deitmer, J.W., Eckert, R. Two components of Ca-dependent potassium current in identified neurones ofAplysia californica . Pflugers Arch. 403, 353–359 (1985). https://doi.org/10.1007/BF00589246

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00589246

Key words

Navigation