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. 1993 Dec;472:711–724. doi: 10.1113/jphysiol.1993.sp019968

Effects of membrane potential and muscarine on potassium M-channel kinetics in rat sympathetic neurones.

A A Selyanko 1, D A Brown 1
PMCID: PMC1160508  PMID: 8145167

Abstract

1. Using cell-attached patch pipettes, sustained activity of single potassium M-channels was recorded from dissociated rat superior cervical ganglion neurones. Previous results indicated that this activity, consisting of three main levels of open-channel conductance (congruent to 7, congruent to 12 and congruent to 19 pS) was activated by membrane depolarization and inhibited by muscarine added outside the patch. Consequently, a kinetic analysis was undertaken in order to identify M-channel states sensitive to muscarine and membrane potential. 2. Channel activity recorded at 30 mV positive to the resting membrane potential level (congruent to -60 mV) showed three shut and two open times. Mean shut times were: tau s1 = 8.0 +/- 2.2 ms; tau s2 = 71.3 +/- 8.6 ms and tau s3 = 740 +/- 220 ms. Mean open times were: tau o1 = 10.6 +/- 1.9 ms and tau o2 = 59.3 +/- 8.7 ms. When bursts of channel openings were determined as those including tau s1, two exponential components were evident in burst duration distributions (tau b1 = 11.0 +/- 0.9 ms and tau b2 = 80.4 +/- 11.0 ms). 3. Membrane hyperpolarization significantly lengthened all three shut times and shortened both open times. It also slightly enhanced the relative contribution of high-conductance channels and decreased the relative contribution of low-conductance channels to overall activity. 4. All three shut times of the M-channels were lengthened by 10 microM muscarine without significantly affecting their open times. 5. It is concluded that both open and shut states of the M-channel are voltage sensitive while only shut states are sensitive to muscarine.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Adams P. R., Brown D. A., Constanti A. M-currents and other potassium currents in bullfrog sympathetic neurones. J Physiol. 1982 Sep;330:537–572. doi: 10.1113/jphysiol.1982.sp014357. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Adams P. R., Brown D. A., Constanti A. Pharmacological inhibition of the M-current. J Physiol. 1982 Nov;332:223–262. doi: 10.1113/jphysiol.1982.sp014411. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Brown D. A., Adams P. R. Muscarinic suppression of a novel voltage-sensitive K+ current in a vertebrate neurone. Nature. 1980 Feb 14;283(5748):673–676. doi: 10.1038/283673a0. [DOI] [PubMed] [Google Scholar]
  4. Brown D. A. M currents. Ion Channels. 1988;1:55–94. doi: 10.1007/978-1-4615-7302-9_2. [DOI] [PubMed] [Google Scholar]
  5. Brown D. A., Marrion N. V., Smart T. G. On the transduction mechanism for muscarine-induced inhibition of M-current in cultured rat sympathetic neurones. J Physiol. 1989 Jun;413:469–488. doi: 10.1113/jphysiol.1989.sp017664. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Brown D. M-currents: an update. Trends Neurosci. 1988 Jul;11(7):294–299. doi: 10.1016/0166-2236(88)90089-6. [DOI] [PubMed] [Google Scholar]
  7. Colquhoun D., Sakmann B. Fast events in single-channel currents activated by acetylcholine and its analogues at the frog muscle end-plate. J Physiol. 1985 Dec;369:501–557. doi: 10.1113/jphysiol.1985.sp015912. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Constanti A., Brown D. A. M-Currents in voltage-clamped mammalian sympathetic neurones. Neurosci Lett. 1981 Jul 17;24(3):289–294. doi: 10.1016/0304-3940(81)90173-7. [DOI] [PubMed] [Google Scholar]
  9. Lopez H. S., Adams P. R. A G Protein Mediates the Inhibition of the Voltage-Dependent Potassium M Current by Muscarine, LHRH, Substance P and UTP in Bullfrog Sympathetic Neurons. Eur J Neurosci. 1989 Sep;1(5):529–542. doi: 10.1111/j.1460-9568.1989.tb00360.x. [DOI] [PubMed] [Google Scholar]
  10. Marrion N. V., Adams P. R., Gruner W. Multiple kinetic states underlying macroscopic M-currents in bullfrog sympathetic neurons. Proc Biol Sci. 1992 Jun 22;248(1323):207–214. doi: 10.1098/rspb.1992.0063. [DOI] [PubMed] [Google Scholar]
  11. Marrion N. V., Smart T. G., Brown D. A. Membrane currents in adult rat superior cervical ganglia in dissociated tissue culture. Neurosci Lett. 1987 Jun 1;77(1):55–60. doi: 10.1016/0304-3940(87)90606-9. [DOI] [PubMed] [Google Scholar]
  12. Neher E., Marty A., Fukuda K., Kubo T., Numa S. Intracellular calcium release mediated by two muscarinic receptor subtypes. FEBS Lett. 1988 Nov 21;240(1-2):88–94. doi: 10.1016/0014-5793(88)80345-4. [DOI] [PubMed] [Google Scholar]
  13. Owen D. G., Marsh S. J., Brown D. A. M-current noise and putative M-channels in cultured rat sympathetic ganglion cells. J Physiol. 1990 Dec;431:269–290. doi: 10.1113/jphysiol.1990.sp018330. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Pfaffinger P. Muscarine and t-LHRH suppress M-current by activating an IAP-insensitive G-protein. J Neurosci. 1988 Sep;8(9):3343–3353. doi: 10.1523/JNEUROSCI.08-09-03343.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Robbins J., Trouslard J., Marsh S. J., Brown D. A. Kinetic and pharmacological properties of the M-current in rodent neuroblastoma x glioma hybrid cells. J Physiol. 1992;451:159–185. doi: 10.1113/jphysiol.1992.sp019159. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Selyanko A. A., Stansfeld C. E., Brown D. A. Closure of potassium M-channels by muscarinic acetylcholine-receptor stimulants requires a diffusible messenger. Proc Biol Sci. 1992 Nov 23;250(1328):119–125. doi: 10.1098/rspb.1992.0139. [DOI] [PubMed] [Google Scholar]
  17. Stansfeld C. E., Marsh S. J., Gibb A. J., Brown D. A. Identification of M-channels in outside-out patches excised from sympathetic ganglion cells. Neuron. 1993 Apr;10(4):639–654. doi: 10.1016/0896-6273(93)90166-o. [DOI] [PubMed] [Google Scholar]

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