Abstract
The transient potassium current, IK(t), of enzymatically dissociated rat olfactory receptor neurons was studied using patch-clamp techniques. Upon depolarization from negative holding potentials, IK(t) activated rapidly and then inactivated with a time course described by the sum of two exponential components with time constants of 22.4 and 143 ms. Single-channel analysis revealed a further small component with a time constant of several seconds. Steady-state inactivation was complete at -20 mV and completely removed at -80 mV (midpoint -45 mV). Activation was significant at -40 mV and appeared to reach a maximum conductance at +40 mV (midpoint -13 mV). Deactivation was described by the sum of two voltage-dependent exponential components. Recovery from inactivation was extraordinarily slow (50 s at -100 mV) and the underlying processes appeared complex. IK(t) was reduced by 4- aminopyridine and tetraethylammonium applied externally. Increasing the external K+ concentration ([K+]o) from 5 to 25 mM partially removed IK(t) inactivation, usually without affecting activation kinetics. The elevated [K+]o also hyperpolarized the steady-state inactivation curve by 9 mV and significantly depolarized the voltage dependence of activation. Single transient K+ channels, with conductances of 17 and 26 pS, were observed in excised patches and often appeared to be localized into large clusters. These channels were similar to IK(t) in their kinetic, pharmacological, and voltage-dependent properties and their inactivation was also subject to modulation by [K+]o. The properties of IK(t) imply a role in action potential repolarization and suggest it may also be important in modulating spike parameters during neuronal burst firing. A simple method is also presented to correct for errors in the measurement of whole-cell resistance (Ro) that can result when patch-clamping very small cells. The analysis revealed a mean corrected Ro of 26 G omega for these cells.
Full Text
The Full Text of this article is available as a PDF (1.6 MB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Akasu T., Tokimasa T. Potassium currents in submucous neurones of guinea-pig caecum and their synaptic modification. J Physiol. 1989 Sep;416:571–588. doi: 10.1113/jphysiol.1989.sp017778. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Barrett J. N., Magleby K. L., Pallotta B. S. Properties of single calcium-activated potassium channels in cultured rat muscle. J Physiol. 1982 Oct;331:211–230. doi: 10.1113/jphysiol.1982.sp014370. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Barry P. H., Quartararo N. PNSCROLL, a software package for graphical interactive analysis of single channel patch clamp currents and other binary file records: under mouse control. Comput Biol Med. 1990;20(3):193–204. doi: 10.1016/0010-4825(90)90005-a. [DOI] [PubMed] [Google Scholar]
- Benndorf K., Markwardt F., Nilius B. Two types of transient outward currents in cardiac ventricular cells of mice. Pflugers Arch. 1987 Aug;409(6):641–643. doi: 10.1007/BF00584667. [DOI] [PubMed] [Google Scholar]
- Cahalan M. D., Chandy K. G., DeCoursey T. E., Gupta S. A voltage-gated potassium channel in human T lymphocytes. J Physiol. 1985 Jan;358:197–237. doi: 10.1113/jphysiol.1985.sp015548. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Cassell J. F., McLachlan E. M. The effect of a transient outward current (IA) on synaptic potentials in sympathetic ganglion cells of the guinea-pig. J Physiol. 1986 May;374:273–288. doi: 10.1113/jphysiol.1986.sp016079. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Clark R. B., Giles W. R., Imaizumi Y. Properties of the transient outward current in rabbit atrial cells. J Physiol. 1988 Nov;405:147–168. doi: 10.1113/jphysiol.1988.sp017326. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Connor J. A., Stevens C. F. Prediction of repetitive firing behaviour from voltage clamp data on an isolated neurone soma. J Physiol. 1971 Feb;213(1):31–53. doi: 10.1113/jphysiol.1971.sp009366. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Cooper E., Shrier A. Inactivation of A currents and A channels on rat nodose neurons in culture. J Gen Physiol. 1989 Nov;94(5):881–910. doi: 10.1085/jgp.94.5.881. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Cooper E., Shrier A. Single-channel analysis of fast transient potassium currents from rat nodose neurones. J Physiol. 1985 Dec;369:199–208. doi: 10.1113/jphysiol.1985.sp015896. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Daut J. Modulation of the excitatory synaptic response by fast transient K+ current in snail neurones. Nat New Biol. 1973 Dec 19;246(155):193–196. doi: 10.1038/newbio246193a0. [DOI] [PubMed] [Google Scholar]
- Deutsch C., Krause D., Lee S. C. Voltage-gated potassium conductance in human T lymphocytes stimulated with phorbol ester. J Physiol. 1986 Mar;372:405–423. doi: 10.1113/jphysiol.1986.sp016016. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Eng D. L., Kocsis J. D. Activity-dependent changes in extracellular potassium and excitability in turtle olfactory nerve. J Neurophysiol. 1987 Mar;57(3):740–754. doi: 10.1152/jn.1987.57.3.740. [DOI] [PubMed] [Google Scholar]
- Firestein S., Werblin F. S. Gated currents in isolated olfactory receptor neurons of the larval tiger salamander. Proc Natl Acad Sci U S A. 1987 Sep;84(17):6292–6296. doi: 10.1073/pnas.84.17.6292. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Florio S. K., Westbrook C. D., Vasko M. R., Bauer R. J., Kenyon J. L. Transient potassium currents in avian sensory neurons. J Neurophysiol. 1990 Apr;63(4):725–737. doi: 10.1152/jn.1990.63.4.725. [DOI] [PubMed] [Google Scholar]
- Frings S., Lindemann B. Odorant response of isolated olfactory receptor cells is blocked by amiloride. J Membr Biol. 1988 Nov;105(3):233–243. doi: 10.1007/BF01871000. [DOI] [PubMed] [Google Scholar]
- Getchell T. V. Functional properties of vertebrate olfactory receptor neurons. Physiol Rev. 1986 Jul;66(3):772–818. doi: 10.1152/physrev.1986.66.3.772. [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]
- 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]
- 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]
- Hoshi T., Aldrich R. W. Voltage-dependent K+ currents and underlying single K+ channels in pheochromocytoma cells. J Gen Physiol. 1988 Jan;91(1):73–106. doi: 10.1085/jgp.91.1.73. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Joshi H., Getchell M. L., Zielinski B., Getchell T. V. Spectrophotometric determination of cation concentrations in olfactory mucus. Neurosci Lett. 1987 Dec 4;82(3):321–326. doi: 10.1016/0304-3940(87)90276-x. [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]
- Kawa K. Transient outward currents and changes of their gating properties after cell activation in thrombocytes of the newt. J Physiol. 1987 Apr;385:189–205. doi: 10.1113/jphysiol.1987.sp016491. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kostyuk P. G., Krishtal O. A., Pidoplichko V. I. Effect of internal fluoride and phosphate on membrane currents during intracellular dialysis of nerve cells. Nature. 1975 Oct 23;257(5528):691–693. doi: 10.1038/257691a0. [DOI] [PubMed] [Google Scholar]
- Lynch J. W., Barry P. H. Action potentials initiated by single channels opening in a small neuron (rat olfactory receptor). Biophys J. 1989 Apr;55(4):755–768. doi: 10.1016/S0006-3495(89)82874-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lynch J. W., Barry P. H., Quartararo N. A temperature and solution control system for the measurement of single channel currents in excised membrane patches. Pflugers Arch. 1988 Aug;412(3):322–327. doi: 10.1007/BF00582515. [DOI] [PubMed] [Google Scholar]
- Marty A., Neher E. Potassium channels in cultured bovine adrenal chromaffin cells. J Physiol. 1985 Oct;367:117–141. doi: 10.1113/jphysiol.1985.sp015817. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Maue R. A., Dionne V. E. Patch-clamp studies of isolated mouse olfactory receptor neurons. J Gen Physiol. 1987 Jul;90(1):95–125. doi: 10.1085/jgp.90.1.95. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Maue R. A., Dionne V. E. Preparation of isolated mouse olfactory receptor neurons. Pflugers Arch. 1987 Jul;409(3):244–250. doi: 10.1007/BF00583472. [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]
- McClintock T. S., Ache B. W. Ionic currents and ion channels of lobster olfactory receptor neurons. J Gen Physiol. 1989 Dec;94(6):1085–1099. doi: 10.1085/jgp.94.6.1085. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Oxford G. S., Wagoner P. K. The inactivating K+ current in GH3 pituitary cells and its modification by chemical reagents. J Physiol. 1989 Mar;410:587–612. doi: 10.1113/jphysiol.1989.sp017550. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pixley S. K., Pun R. Y. Cultured rat olfactory neurons are excitable and respond to odors. Brain Res Dev Brain Res. 1990 Apr 1;53(1):125–130. doi: 10.1016/0165-3806(90)90132-i. [DOI] [PubMed] [Google Scholar]
- Premack B. A., Thompson S., Coombs-Hahn J. Clustered distribution and variability in kinetics of transient K channels in molluscan neuron cell bodies. J Neurosci. 1989 Nov;9(11):4089–4099. doi: 10.1523/JNEUROSCI.09-11-04089.1989. [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]
- Röper J., Schwarz J. R. Heterogeneous distribution of fast and slow potassium channels in myelinated rat nerve fibres. J Physiol. 1989 Sep;416:93–110. doi: 10.1113/jphysiol.1989.sp017751. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Salkoff L., Wyman R. Facilitation of membrane electrical excitability in Drosophila. Proc Natl Acad Sci U S A. 1980 Oct;77(10):6216–6220. doi: 10.1073/pnas.77.10.6216. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Schild D. Whole-cell currents in olfactory receptor cells of Xenopus laevis. Exp Brain Res. 1989;78(2):223–232. doi: 10.1007/BF00228894. [DOI] [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]
- Taylor P. S. Selectivity and patch measurements of A-current channels in Helix aspersa neurones. J Physiol. 1987 Jul;388:437–447. doi: 10.1113/jphysiol.1987.sp016623. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Trotier D. A patch-clamp analysis of membrane currents in salamander olfactory receptor cells. Pflugers Arch. 1986 Dec;407(6):589–595. doi: 10.1007/BF00582636. [DOI] [PubMed] [Google Scholar]