Skip to main content
NCBI home page
The Journal of Physiology logoLink to The Journal of Physiology
. 1997 Dec 15;505(Pt 3):593–603. doi: 10.1111/j.1469-7793.1997.593ba.x

Functional differences in Na+ channel gating between fast-spiking interneurones and principal neurones of rat hippocampus.

M Martina 1, P Jonas 1
PMCID: PMC1160038  PMID: 9457638

Abstract

1. GABAergic interneurones differ from glutamatergic principal neurones in their ability to discharge high-frequency trains of action potentials without adaptation. To examine whether Na+ channel gating contributed to these differences, Na+ currents were recorded in nucleated patches from interneurones (dentate gyrus basket cells, BCs) and principal neurones (CA1 pyramidal cells, PCs) of rat hippocampal slices. 2. The voltage dependence of Na+ channel activation in BCs and PCs was similar. The slope factors of the activation curves, fitted with Boltzmann functions raised to the third power, were 11.5 and 11.8 mV, and the mid-point potentials were -25.1 and -23.9 mV, respectively. 3. Whereas the time course of Na+ channel activation (-30 to +40 mV) was similar, the deactivation kinetics (-100 to -40 mV) were faster in BCs than in PCs (tail current decay time constants, 0.13 and 0.20 ms, respectively, at -40 mV). 4. Na+ channels in BCs and PCs differed in the voltage dependence of inactivation. The slope factors of the steady-state inactivation curves fitted with Boltzmann functions were 6.7 and 10.7 mV, and the mid-point potentials were -58.3 and -62.9 mV, respectively. 5. The onset of Na+ channel inactivation at -55 mV was slower in BCs than in PCs; the inactivation time constants were 18.6 and 9.3 ms, respectively. At more positive potentials the differences in inactivation onset were smaller. 6. The time course of recovery of Na+ channels from inactivation induced by a 30 ms pulse was fast and mono-exponential (tau = 2.0 ms at -120 mV) in BCs, whereas it was slower and bi-exponential in PCs (tau 1 = 2.0 ms and tau 2 = 133 ms; amplitude contribution of the slow component, 15%). 7. We conclude that Na+ channels of BCs and PCs differ in gating properties that contribute to the characteristic action potential patterns of the two types of neurones.

Full text

PDF
593

Selected References

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

  1. Alzheimer C., Schwindt P. C., Crill W. E. Modal gating of Na+ channels as a mechanism of persistent Na+ current in pyramidal neurons from rat and cat sensorimotor cortex. J Neurosci. 1993 Feb;13(2):660–673. doi: 10.1523/JNEUROSCI.13-02-00660.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Cantrell A. R., Ma J. Y., Scheuer T., Catterall W. A. Muscarinic modulation of sodium current by activation of protein kinase C in rat hippocampal neurons. Neuron. 1996 May;16(5):1019–1026. doi: 10.1016/s0896-6273(00)80125-7. [DOI] [PubMed] [Google Scholar]
  3. Connors B. W., Gutnick M. J. Intrinsic firing patterns of diverse neocortical neurons. Trends Neurosci. 1990 Mar;13(3):99–104. doi: 10.1016/0166-2236(90)90185-d. [DOI] [PubMed] [Google Scholar]
  4. Crill W. E. Persistent sodium current in mammalian central neurons. Annu Rev Physiol. 1996;58:349–362. doi: 10.1146/annurev.ph.58.030196.002025. [DOI] [PubMed] [Google Scholar]
  5. Du J., Zhang L., Weiser M., Rudy B., McBain C. J. Developmental expression and functional characterization of the potassium-channel subunit Kv3.1b in parvalbumin-containing interneurons of the rat hippocampus. J Neurosci. 1996 Jan 15;16(2):506–518. doi: 10.1523/JNEUROSCI.16-02-00506.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Fleidervish I. A., Friedman A., Gutnick M. J. Slow inactivation of Na+ current and slow cumulative spike adaptation in mouse and guinea-pig neocortical neurones in slices. J Physiol. 1996 May 15;493(Pt 1):83–97. doi: 10.1113/jphysiol.1996.sp021366. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Han Z. S., Buhl E. H., Lörinczi Z., Somogyi P. A high degree of spatial selectivity in the axonal and dendritic domains of physiologically identified local-circuit neurons in the dentate gyrus of the rat hippocampus. Eur J Neurosci. 1993 May 1;5(5):395–410. doi: 10.1111/j.1460-9568.1993.tb00507.x. [DOI] [PubMed] [Google Scholar]
  8. Howe J. R., Ritchie J. M. Multiple kinetic components of sodium channel inactivation in rabbit Schwann cells. J Physiol. 1992 Sep;455:529–566. doi: 10.1113/jphysiol.1992.sp019315. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Isom L. L., De Jongh K. S., Patton D. E., Reber B. F., Offord J., Charbonneau H., Walsh K., Goldin A. L., Catterall W. A. Primary structure and functional expression of the beta 1 subunit of the rat brain sodium channel. Science. 1992 May 8;256(5058):839–842. doi: 10.1126/science.1375395. [DOI] [PubMed] [Google Scholar]
  10. Johnston D., Magee J. C., Colbert C. M., Cristie B. R. Active properties of neuronal dendrites. Annu Rev Neurosci. 1996;19:165–186. doi: 10.1146/annurev.ne.19.030196.001121. [DOI] [PubMed] [Google Scholar]
  11. Joho R. H., Moorman J. R., VanDongen A. M., Kirsch G. E., Silberberg H., Schuster G., Brown A. M. Toxin and kinetic profile of rat brain type III sodium channels expressed in Xenopus oocytes. Brain Res Mol Brain Res. 1990 Feb;7(2):105–113. doi: 10.1016/0169-328x(90)90087-t. [DOI] [PubMed] [Google Scholar]
  12. Jonas P., Bräu M. E., Hermsteiner M., Vogel W. Single-channel recording in myelinated nerve fibers reveals one type of Na channel but different K channels. Proc Natl Acad Sci U S A. 1989 Sep;86(18):7238–7242. doi: 10.1073/pnas.86.18.7238. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Jonas P. Temperature dependence of gating current in myelinated nerve fibers. J Membr Biol. 1989 Dec;112(3):277–289. doi: 10.1007/BF01870958. [DOI] [PubMed] [Google Scholar]
  14. Lacaille J. C., Williams S. Membrane properties of interneurons in stratum oriens-alveus of the CA1 region of rat hippocampus in vitro. Neuroscience. 1990;36(2):349–359. doi: 10.1016/0306-4522(90)90431-3. [DOI] [PubMed] [Google Scholar]
  15. Madison D. V., Nicoll R. A. Control of the repetitive discharge of rat CA 1 pyramidal neurones in vitro. J Physiol. 1984 Sep;354:319–331. doi: 10.1113/jphysiol.1984.sp015378. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Mainen Z. F., Sejnowski T. J. Influence of dendritic structure on firing pattern in model neocortical neurons. Nature. 1996 Jul 25;382(6589):363–366. doi: 10.1038/382363a0. [DOI] [PubMed] [Google Scholar]
  17. Makita N., Bennett P. B., George A. L., Jr Molecular determinants of beta 1 subunit-induced gating modulation in voltage-dependent Na+ channels. J Neurosci. 1996 Nov 15;16(22):7117–7127. doi: 10.1523/JNEUROSCI.16-22-07117.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. McCormick D. A., Connors B. W., Lighthall J. W., Prince D. A. Comparative electrophysiology of pyramidal and sparsely spiny stellate neurons of the neocortex. J Neurophysiol. 1985 Oct;54(4):782–806. doi: 10.1152/jn.1985.54.4.782. [DOI] [PubMed] [Google Scholar]
  19. Safronov B. V., Vogel W. Single voltage-activated Na+ and K+ channels in the somata of rat motoneurones. J Physiol. 1995 Aug 15;487(1):91–106. doi: 10.1113/jphysiol.1995.sp020863. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Sah P., Gibb A. J., Gage P. W. The sodium current underlying action potentials in guinea pig hippocampal CA1 neurons. J Gen Physiol. 1988 Mar;91(3):373–398. doi: 10.1085/jgp.91.3.373. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Spruston N., Schiller Y., Stuart G., Sakmann B. Activity-dependent action potential invasion and calcium influx into hippocampal CA1 dendrites. Science. 1995 Apr 14;268(5208):297–300. doi: 10.1126/science.7716524. [DOI] [PubMed] [Google Scholar]
  22. 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]
  23. Stuart G. J., Dodt H. U., Sakmann B. Patch-clamp recordings from the soma and dendrites of neurons in brain slices using infrared video microscopy. Pflugers Arch. 1993 Jun;423(5-6):511–518. doi: 10.1007/BF00374949. [DOI] [PubMed] [Google Scholar]
  24. Terlau H., Shon K. J., Grilley M., Stocker M., Stühmer W., Olivera B. M. Strategy for rapid immobilization of prey by a fish-hunting marine snail. Nature. 1996 May 9;381(6578):148–151. doi: 10.1038/381148a0. [DOI] [PubMed] [Google Scholar]
  25. Traub R. D., Whittington M. A., Stanford I. M., Jefferys J. G. A mechanism for generation of long-range synchronous fast oscillations in the cortex. Nature. 1996 Oct 17;383(6601):621–624. doi: 10.1038/383621a0. [DOI] [PubMed] [Google Scholar]
  26. Warman E. N., Durand D. M., Yuen G. L. Reconstruction of hippocampal CA1 pyramidal cell electrophysiology by computer simulation. J Neurophysiol. 1994 Jun;71(6):2033–2045. doi: 10.1152/jn.1994.71.6.2033. [DOI] [PubMed] [Google Scholar]
  27. Zhang L., McBain C. J. Potassium conductances underlying repolarization and after-hyperpolarization in rat CA1 hippocampal interneurones. J Physiol. 1995 Nov 1;488(Pt 3):661–672. doi: 10.1113/jphysiol.1995.sp020998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Zhang L., McBain C. J. Voltage-gated potassium currents in stratum oriens-alveus inhibitory neurones of the rat CA1 hippocampus. J Physiol. 1995 Nov 1;488(Pt 3):647–660. doi: 10.1113/jphysiol.1995.sp020997. [DOI] [PMC free article] [PubMed] [Google Scholar]

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

RESOURCES