Abstract
1. Two transient outward currents were identified in large pyramidal neurones from layer V of cat sensorimotor cortex ('Betz cells') using an in vitro brain slice preparation and single-microelectrode voltage clamp. Properties of the currents deduced from voltage-clamp measurements were reflected in neuronal responses during constant current stimulation. 2. Both transient outward currents rose rapidly after a step depolarization, but their subsequent time course differed greatly. The fast-transient current decayed within 20 ms, while the slow-transient current took greater than 10 s to decay. Raised extracellular potassium reduced current amplitude. Both currents were present in cadmium-containing or calcium-free perfusate. 3. Tetraethylammonium had little effect on the slow-transient current at a concentration of 1 mM, but the fast-transient current was reduced by 60%. 4-Aminopyridine had little effect on the fast-transient current over the range 20 microM-2 mM, but these concentrations reduced the slow-transient current and altered its time course. 4. Both transient currents were evoked by depolarizations below action potential threshold. The fast-transient current was evoked by a 7 mV smaller depolarization than the slow-transient current, but its chord conductance increased less steeply with depolarization. 5. Voltage-dependent inactivation of the fast-transient was steeper than that of the slow-transient current (4 vs. 7 mV per e-fold change), and half-inactivation occurred at a less negative potential (-59 vs. -65 mV). The activation and inactivation characteristics of each current overlapped, however, implying the existence of a steady 'window current' extending over a range of approximately 14 mV beginning negative to action potential threshold. 6. The fast-transient current displayed a clear voltage dependence of both its activation and inactivation kinetics, whereas the slow-transient current did not. Recovery of either current from inactivation took about 1 s near -70 mV. The recovery of the slow-transient current became faster with hyperpolarization. 7. The contribution of each transient current to repolarization of the action potential was assessed from pharmacological responses. Blockade of calcium influx had little or no effect on the rate of action potential repolarization, whereas the selective reduction of either transient current caused significant slowing of repolarization. 8. We conclude that Betz cells possess at least two transient potassium currents, each a member of the rapidly expanding family of voltage-gated potassium currents that have been identified in various cell types.(ABSTRACT TRUNCATED AT 400 WORDS)
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Selected References
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- Aldrich R. W., Jr, Getting P. A., Thompson S. H. Inactivation of delayed outward current in molluscan neurone somata. J Physiol. 1979 Jun;291:507–530. doi: 10.1113/jphysiol.1979.sp012828. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Alkon D. L., Shoukimas J. J., Heldman E. Calcium-mediated decrease of a voltage-dependent potassium current. Biophys J. 1982 Dec;40(3):245–250. doi: 10.1016/S0006-3495(82)84479-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bourque C. W. Transient calcium-dependent potassium current in magnocellular neurosecretory cells of the rat supraoptic nucleus. J Physiol. 1988 Mar;397:331–347. doi: 10.1113/jphysiol.1988.sp017004. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Callewaert G., Vereecke J., Carmeliet E. Existence of a calcium-dependent potassium channel in the membrane of cow cardiac Purkinje cells. Pflugers Arch. 1986 Apr;406(4):424–426. doi: 10.1007/BF00590947. [DOI] [PubMed] [Google Scholar]
- Christie M. J., Adelman J. P., Douglass J., North R. A. Expression of a cloned rat brain potassium channel in Xenopus oocytes. Science. 1989 Apr 14;244(4901):221–224. doi: 10.1126/science.2539643. [DOI] [PubMed] [Google Scholar]
- Connor J. A., Stevens C. F. Voltage clamp studies of a transient outward membrane current in gastropod neural somata. J Physiol. 1971 Feb;213(1):21–30. doi: 10.1113/jphysiol.1971.sp009365. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Constanti A., Sim J. A. Calcium-dependent potassium conductance in guinea-pig olfactory cortex neurones in vitro. J Physiol. 1987 Jun;387:173–194. doi: 10.1113/jphysiol.1987.sp016569. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Dekin M. S., Getting P. A. In vitro characterization of neurons in the ventral part of the nucleus tractus solitarius. II. Ionic basis for repetitive firing patterns. J Neurophysiol. 1987 Jul;58(1):215–229. doi: 10.1152/jn.1987.58.1.215. [DOI] [PubMed] [Google Scholar]
- Foehring R. C., Schwindt P. C., Crill W. E. Norepinephrine selectively reduces slow Ca2+- and Na+-mediated K+ currents in cat neocortical neurons. J Neurophysiol. 1989 Feb;61(2):245–256. doi: 10.1152/jn.1989.61.2.245. [DOI] [PubMed] [Google Scholar]
- Galvan M., Sedlmeir C. Outward currents in voltage-clamped rat sympathetic neurones. J Physiol. 1984 Nov;356:115–133. doi: 10.1113/jphysiol.1984.sp015456. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gestrelius S., Grampp W. Kinetics of the TEA and 4-AP sensitive K+ current in the slowly adapting lobster stretch receptor neurone. Acta Physiol Scand. 1983 Jun;118(2):125–134. doi: 10.1111/j.1748-1716.1983.tb07252.x. [DOI] [PubMed] [Google Scholar]
- Gustafsson B., Galvan M., Grafe P., Wigström H. A transient outward current in a mammalian central neurone blocked by 4-aminopyridine. Nature. 1982 Sep 16;299(5880):252–254. doi: 10.1038/299252a0. [DOI] [PubMed] [Google Scholar]
- HAGIWARA S., KUSANO K., SAITO N. Membrane changes of Onchidium nerve cell in potassium-rich media. J Physiol. 1961 Mar;155:470–489. doi: 10.1113/jphysiol.1961.sp006640. [DOI] [PMC free article] [PubMed] [Google Scholar]
- HODGKIN A. L., HUXLEY A. F. A quantitative description of membrane current and its application to conduction and excitation in nerve. J Physiol. 1952 Aug;117(4):500–544. doi: 10.1113/jphysiol.1952.sp004764. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hermann A., Gorman A. L. Effects of 4-aminopyridine on potassium currents in a molluscan neuron. J Gen Physiol. 1981 Jul;78(1):63–86. doi: 10.1085/jgp.78.1.63. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Iverson L. E., Tanouye M. A., Lester H. A., Davidson N., Rudy B. A-type potassium channels expressed from Shaker locus cDNA. Proc Natl Acad Sci U S A. 1988 Aug;85(15):5723–5727. doi: 10.1073/pnas.85.15.5723. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Junge D. Calcium dependence of A-currents in perfused Aplysia neurons. Brain Res. 1985 Nov 4;346(2):294–300. doi: 10.1016/0006-8993(85)90863-7. [DOI] [PubMed] [Google Scholar]
- Kasai H., Kameyama M., Yamaguchi K., Fukuda J. Single transient K channels in mammalian sensory neurons. Biophys J. 1986 Jun;49(6):1243–1247. doi: 10.1016/S0006-3495(86)83754-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lancaster B., Nicoll R. A. Properties of two calcium-activated hyperpolarizations in rat hippocampal neurones. J Physiol. 1987 Aug;389:187–203. doi: 10.1113/jphysiol.1987.sp016653. [DOI] [PMC free article] [PubMed] [Google Scholar]
- MacDermott A. B., Weight F. F. Action potential repolarization may involve a transient, Ca2+-sensitive outward current in a vertebrate neurone. Nature. 1982 Nov 11;300(5888):185–188. doi: 10.1038/300185a0. [DOI] [PubMed] [Google Scholar]
- Mayer M. L., Sugiyama K. A modulatory action of divalent cations on transient outward current in cultured rat sensory neurones. J Physiol. 1988 Feb;396:417–433. doi: 10.1113/jphysiol.1988.sp016970. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Meves H., Pichon Y. The effect of internal and external 4-aminopyridine on the potassium currents in intracellularly perfused squid giant axons. J Physiol. 1977 Jun;268(2):511–532. doi: 10.1113/jphysiol.1977.sp011869. [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]
- Penner R., Petersen M., Pierau F. K., Dreyer F. Dendrotoxin: a selective blocker of a non-inactivating potassium current in guinea-pig dorsal root ganglion neurones. Pflugers Arch. 1986 Oct;407(4):365–369. doi: 10.1007/BF00652619. [DOI] [PubMed] [Google Scholar]
- Quandt F. N. Three kinetically distinct potassium channels in mouse neuroblastoma cells. J Physiol. 1988 Jan;395:401–418. doi: 10.1113/jphysiol.1988.sp016926. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ruben P., Thompson S. Rapid recovery from K current inactivation on membrane hyperpolarization in molluscan neurons. J Gen Physiol. 1984 Dec;84(6):861–875. doi: 10.1085/jgp.84.6.861. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rudy B. Diversity and ubiquity of K channels. Neuroscience. 1988 Jun;25(3):729–749. doi: 10.1016/0306-4522(88)90033-4. [DOI] [PubMed] [Google Scholar]
- Rudy B., Hoger J. H., Lester H. A., Davidson N. At least two mRNA species contribute to the properties of rat brain A-type potassium channels expressed in Xenopus oocytes. Neuron. 1988 Oct;1(8):649–658. doi: 10.1016/0896-6273(88)90164-x. [DOI] [PubMed] [Google Scholar]
- Salkoff L. Drosophila mutants reveal two components of fast outward current. Nature. 1983 Mar 17;302(5905):249–251. doi: 10.1038/302249a0. [DOI] [PubMed] [Google Scholar]
- Schwindt P. C., Spain W. J., Crill W. E. Long-lasting reduction of excitability by a sodium-dependent potassium current in cat neocortical neurons. J Neurophysiol. 1989 Feb;61(2):233–244. doi: 10.1152/jn.1989.61.2.233. [DOI] [PubMed] [Google Scholar]
- Schwindt P. C., Spain W. J., Foehring R. C., Chubb M. C., Crill W. E. Slow conductances in neurons from cat sensorimotor cortex in vitro and their role in slow excitability changes. J Neurophysiol. 1988 Feb;59(2):450–467. doi: 10.1152/jn.1988.59.2.450. [DOI] [PubMed] [Google Scholar]
- Schwindt P. C., Spain W. J., Foehring R. C., Stafstrom C. E., Chubb M. C., Crill W. E. Multiple potassium conductances and their functions in neurons from cat sensorimotor cortex in vitro. J Neurophysiol. 1988 Feb;59(2):424–449. doi: 10.1152/jn.1988.59.2.424. [DOI] [PubMed] [Google Scholar]
- Siegelbaum S. A., Tsien R. W. Calcium-activated transient outward current in calf cardiac Purkinje fibres. J Physiol. 1980 Feb;299:485–506. doi: 10.1113/jphysiol.1980.sp013138. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Solc C. K., Zagotta W. N., Aldrich R. W. Single-channel and genetic analyses reveal two distinct A-type potassium channels in Drosophila. Science. 1987 May 29;236(4805):1094–1098. doi: 10.1126/science.2437657. [DOI] [PubMed] [Google Scholar]
- Spain W. J., Schwindt P. C., Crill W. E. Anomalous rectification in neurons from cat sensorimotor cortex in vitro. J Neurophysiol. 1987 May;57(5):1555–1576. doi: 10.1152/jn.1987.57.5.1555. [DOI] [PubMed] [Google Scholar]
- Spain W. J., Schwindt P. C., Crill W. E. Post-inhibitory excitation and inhibition in layer V pyramidal neurones from cat sensorimotor cortex. J Physiol. 1991 Mar;434:609–626. doi: 10.1113/jphysiol.1991.sp018489. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Stafstrom C. E., Schwindt P. C., Chubb M. C., Crill W. E. Properties of persistent sodium conductance and calcium conductance of layer V neurons from cat sensorimotor cortex in vitro. J Neurophysiol. 1985 Jan;53(1):153–170. doi: 10.1152/jn.1985.53.1.153. [DOI] [PubMed] [Google Scholar]
- Stafstrom C. E., Schwindt P. C., Crill W. E. Repetitive firing in layer V neurons from cat neocortex in vitro. J Neurophysiol. 1984 Aug;52(2):264–277. doi: 10.1152/jn.1984.52.2.264. [DOI] [PubMed] [Google Scholar]
- Stafstrom C. E., Schwindt P. C., Flatman J. A., Crill W. E. Properties of subthreshold response and action potential recorded in layer V neurons from cat sensorimotor cortex in vitro. J Neurophysiol. 1984 Aug;52(2):244–263. doi: 10.1152/jn.1984.52.2.244. [DOI] [PubMed] [Google Scholar]
- Stansfeld C. E., Marsh S. J., Halliwell J. V., Brown D. A. 4-Aminopyridine and dendrotoxin induce repetitive firing in rat visceral sensory neurones by blocking a slowly inactivating outward current. Neurosci Lett. 1986 Mar 14;64(3):299–304. doi: 10.1016/0304-3940(86)90345-9. [DOI] [PubMed] [Google Scholar]
- Storm J. F. Action potential repolarization and a fast after-hyperpolarization in rat hippocampal pyramidal cells. J Physiol. 1987 Apr;385:733–759. doi: 10.1113/jphysiol.1987.sp016517. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Storm J. F. Temporal integration by a slowly inactivating K+ current in hippocampal neurons. Nature. 1988 Nov 24;336(6197):379–381. doi: 10.1038/336379a0. [DOI] [PubMed] [Google Scholar]
- Thompson S. Aminopyridine block of transient potassium current. J Gen Physiol. 1982 Jul;80(1):1–18. doi: 10.1085/jgp.80.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tsuda Y., Oyama Y., Carpenter D. O., Akaike N. Effects of Ca2+ on the transient outward current of single isolated Helix central neurones. Br J Pharmacol. 1988 Oct;95(2):526–530. doi: 10.1111/j.1476-5381.1988.tb11673.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ulbricht W., Wagner H. H. Block of potassium channels of the nodal membrane by 4-aminopyridine and its partial removal on depolarization. Pflugers Arch. 1976 Nov 30;367(1):77–87. doi: 10.1007/BF00583659. [DOI] [PubMed] [Google Scholar]
- Woody C. D., Baranyi A., Szente M. B., Gruen E., Holmes W., Nenov V., Strecker G. J. An aminopyridine-sensitive, early outward current recorded in vivo in neurons of the precruciate cortex of cats using single-electrode voltage-clamp techniques. Brain Res. 1989 Feb 20;480(1-2):72–81. doi: 10.1016/0006-8993(89)91568-0. [DOI] [PubMed] [Google Scholar]
- Yeh J. Z., Oxford G. S., Wu C. H., Narahashi T. Interactions of aminopyridines with potassium channels of squid axon membranes. Biophys J. 1976 Jan;16(1):77–81. doi: 10.1016/S0006-3495(76)85663-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Zbicz K. L., Weight F. F. Transient voltage and calcium-dependent outward currents in hippocampal CA3 pyramidal neurons. J Neurophysiol. 1985 Apr;53(4):1038–1058. doi: 10.1152/jn.1985.53.4.1038. [DOI] [PubMed] [Google Scholar]
- Zona C., Pirrone G., Avoli M., Dichter M. Delayed and fast transient potassium currents in rat neocortical neurons in cell culture. Neurosci Lett. 1988 Dec 5;94(3):285–290. doi: 10.1016/0304-3940(88)90032-8. [DOI] [PubMed] [Google Scholar]
