Skip to main content
PMC home page
The Journal of Physiology logoLink to The Journal of Physiology
. 1984 Apr;349:227–247. doi: 10.1113/jphysiol.1984.sp015154

Ionic basis for the electro-responsiveness and oscillatory properties of guinea-pig thalamic neurones in vitro.

H Jahnsen, R Llinás
PMCID: PMC1199335  PMID: 6737293

Abstract

The ionic requirements for electro-responsiveness in thalamic neurones were studied using in vitro slice preparations of the guinea-pig diencephalon. Analysis of the current-voltage relationship in these neurones revealed delayed and anomalous rectification. Substitution of Na+ with choline in the bath or addition of tetrodotoxin (TTX) abolished the fast spikes and the plateau potentials, described in the accompanying paper. Ca2+ conductance blockage with Co2+, Cd2+ or Mn2+, or replacement of Ca2+ by Mg2+ abolished the low-threshold spikes (l.t.s.). Substitution with Ba2+ did not significantly increase the duration of the l.t.s., suggesting that under normal conditions the falling phase of this response is brought about by inactivation of the Ca2+ conductance. The after-hyperpolarization (a.h.p.) following fast spikes was markedly reduced in amplitude and duration by bath application of Cd2+, Co2+ or Mn2+, indicating that a large component of this response is generated by a Ca2+-dependent K+ conductance (gK[Ca]). Following hyperpolarizing current pulses, the membrane potential showed a delayed return to base line. This delay is produced by a transient K+ conductance as it can be modified by changing the drive force for K+. Presumptive intra-dendritic recording demonstrated high-threshold Ca2+ spikes (h.t.s.s.) which activate a gK[Ca]. Such h.t.s.s. were also seen at the somatic level when K+ conductance was blocked with 4-aminopyridine. It is proposed that the intrinsic biophysical properties of thalamic neurones allow them to serve as relay systems and as single cell oscillators at two distinct frequencies, 9-10 and 5-6 Hz. These frequencies coincide with the alpha and theta rhythms of the e.e.g. and, in the latter case, with the frequency of Parkinson's tremor.

Full text

PDF
229

Selected References

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

  1. ANDERSEN P., BROOKS C. M., ECCLES J. C., SEARS T. A. THE VENTRO-BASAL NUCLEUS OF THE THALAMUS: POTENTIAL FIELDS, SYNAPTIC TRANSMISSION AND EXCITABILITY OF BOTH PRESYNAPTIC AND POST-SYNAPTIC COMPONENTS. J Physiol. 1964 Nov;174:348–369. doi: 10.1113/jphysiol.1964.sp007492. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. ANDERSEN P., SEARS T. A. THE ROLE OF INHIBITION IN THE PHASING OF SPONTANEOUS THALAMO-CORTICAL DISCHARGE. J Physiol. 1964 Oct;173:459–480. doi: 10.1113/jphysiol.1964.sp007468. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Armstrong C. M., Swenson R. P., Jr, Taylor S. R. Block of squid axon K channels by internally and externally applied barium ions. J Gen Physiol. 1982 Nov;80(5):663–682. doi: 10.1085/jgp.80.5.663. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Blankenship J. E., Kuno M. Analysis of spontaneous subthreshold activity in spinal motoneurons of the cat. J Neurophysiol. 1968 Mar;31(2):195–209. doi: 10.1152/jn.1968.31.2.195. [DOI] [PubMed] [Google Scholar]
  5. Blankenship J. E. Tetrodotoxin: from poison to powerful tool. Perspect Biol Med. 1976 Summer;19(4):509–526. doi: 10.1353/pbm.1976.0071. [DOI] [PubMed] [Google Scholar]
  6. 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]
  7. Eaton D. C., Brodwick M. S. Effects of barium on the potassium conductance of squid axon. J Gen Physiol. 1980 Jun;75(6):727–750. doi: 10.1085/jgp.75.6.727. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Eckert R., Lux H. D. A voltage-sensitive persistent calcium conductance in neuronal somata of Helix. J Physiol. 1976 Jan;254(1):129–151. doi: 10.1113/jphysiol.1976.sp011225. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. 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]
  10. 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]
  11. 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]
  12. Hagiwara S. Ca spike. Adv Biophys. 1973;4:71–102. [PubMed] [Google Scholar]
  13. 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]
  14. Hotson J. R., Prince D. A. A calcium-activated hyperpolarization follows repetitive firing in hippocampal neurons. J Neurophysiol. 1980 Feb;43(2):409–419. doi: 10.1152/jn.1980.43.2.409. [DOI] [PubMed] [Google Scholar]
  15. Jahnsen H., Llinás R. Electrophysiological properties of guinea-pig thalamic neurones: an in vitro study. J Physiol. 1984 Apr;349:205–226. doi: 10.1113/jphysiol.1984.sp015153. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Llinás R., Hess R. Tetrodotoxin-resistant dendritic spikes in avian Purkinje cells. Proc Natl Acad Sci U S A. 1976 Jul;73(7):2520–2523. doi: 10.1073/pnas.73.7.2520. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Llinás R., Jahnsen H. Electrophysiology of mammalian thalamic neurones in vitro. Nature. 1982 Jun 3;297(5865):406–408. doi: 10.1038/297406a0. [DOI] [PubMed] [Google Scholar]
  18. Llinás R., Sugimori M. Electrophysiological properties of in vitro Purkinje cell dendrites in mammalian cerebellar slices. J Physiol. 1980 Aug;305:197–213. doi: 10.1113/jphysiol.1980.sp013358. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Llinás R., Sugimori M. Electrophysiological properties of in vitro Purkinje cell somata in mammalian cerebellar slices. J Physiol. 1980 Aug;305:171–195. doi: 10.1113/jphysiol.1980.sp013357. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Llinás R., Walton K., Bohr V. Synaptic transmission in squid giant synapse after potassium conductance blockage with external 3- and 4-aminopyridine. Biophys J. 1976 Jan;16(1):83–86. doi: 10.1016/S0006-3495(76)85664-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Llinás R., Yarom Y. Electrophysiology of mammalian inferior olivary neurones in vitro. Different types of voltage-dependent ionic conductances. J Physiol. 1981 Jun;315:549–567. doi: 10.1113/jphysiol.1981.sp013763. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Llinás R., Yarom Y. Properties and distribution of ionic conductances generating electroresponsiveness of mammalian inferior olivary neurones in vitro. J Physiol. 1981 Jun;315:569–584. doi: 10.1113/jphysiol.1981.sp013764. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Matteson D. R., Armstrong C. M. Evidence for a population of sleepy sodium channels in squid axon at low temperature. J Gen Physiol. 1982 May;79(5):739–758. doi: 10.1085/jgp.79.5.739. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. 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]
  25. Murase K., Randić M. Electrophysiological properties of rat spinal dorsal horn neurones in vitro: calcium-dependent action potentials. J Physiol. 1983 Jan;334:141–153. doi: 10.1113/jphysiol.1983.sp014485. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. 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]
  27. Pelhate M., Pichon Y. Proceedings: Selective inhibition of potassium current in the giant axon of the cockroach. J Physiol. 1974 Oct;242(2):90P–91P. [PubMed] [Google Scholar]
  28. Ritchie J. M., Rogart R. B. The binding of saxitoxin and tetrodotoxin to excitable tissue. Rev Physiol Biochem Pharmacol. 1977;79:1–50. doi: 10.1007/BFb0037088. [DOI] [PubMed] [Google Scholar]
  29. Schwartzkroin P. A., Slawsky M. Probable calcium spikes in hippocampal neurons. Brain Res. 1977 Oct 21;135(1):157–161. doi: 10.1016/0006-8993(77)91060-5. [DOI] [PubMed] [Google Scholar]
  30. Stafstrom C. E., Schwindt P. C., Crill W. E. Negative slope conductance due to a persistent subthreshold sodium current in cat neocortical neurons in vitro. Brain Res. 1982 Mar 18;236(1):221–226. doi: 10.1016/0006-8993(82)90050-6. [DOI] [PubMed] [Google Scholar]
  31. WERMAN R., GRUNDFEST H. Graded and all-or-none electrogenesis in arthropod muscle. II. The effects of alkali-earth and onium ions on lobster muscle fibers. J Gen Physiol. 1961 May;44:997–1027. doi: 10.1085/jgp.44.5.997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Wong R. K., Prince D. A. Participation of calcium spikes during intrinsic burst firing in hippocampal neurons. Brain Res. 1978 Dec 29;159(2):385–390. doi: 10.1016/0006-8993(78)90544-9. [DOI] [PubMed] [Google Scholar]
  33. Yeh J. Z., Oxford G. S., Wu C. H., Narahashi T. Dynamics of aminopyridine block of potassium channels in squid axon membrane. J Gen Physiol. 1976 Nov;68(5):519–535. doi: 10.1085/jgp.68.5.519. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from The Journal of Physiology are provided here courtesy of The Physiological Society

RESOURCES