Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Noradrenaline and serotonin selectively modulate thalamic burst firing by enhancing a hyperpolarization-activated cation current

Abstract

NEURONS in many regions of the mammalian nervous system generate action potentials in two distinct modes: rhythmic oscillations in which spikes cluster together in a cyclical manner, and single spike firing in which action potentials occur relatively independently of one another1,2. Which mode of action potential generation a neuron displays often varies with the behavioural state of the animal2,3. For example, the shift from slow-wave sleep to waking and attentiveness is associated with a change in thalamic neurons from rhythmic burst firing to repetitive single spike activity, and a greatly increased responsiveness to excitatory synaptic inputs1-3. This marked change in firing pattern and excitability is controlled in part by ascending noradrenergic and serotonergic inputs from the brainstem4-11, although the cellular mechanisms of this effect have remained largely unknown. Here we report that noradrenaline and serotonin enhance a mixed Na+/K+ current which is activated by hyperpolarization (Ih) and that this enhancement may be mediated by increases in intracellular concentration of cyclic AMP. This novel action of noradrenaline and serotonin reduces the ability of thalamic neurons to generate rhythmic burst firing and promotes a state of excitability that is conducive to the thalamocortical synaptic processing associated with cognition.

This is a preview of subscription content, access via your institution

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

Prices may be subject to local taxes which are calculated during checkout

References

  1. Steriade, M. & Deschênes, M. Brain Res. Rev. 8, 1–63 (1984).

    Article  Google Scholar 

  2. Steriade, M. & Llinás, R. R. Physiol. Rev. 68, 649–742 (1988).

    Article  CAS  Google Scholar 

  3. Hobson, J. A. & Steriade, M. in Handbook of Physiology Vol. IV 701–823 (Am. Physiol. Soc., 1987).

    Google Scholar 

  4. Jouvet, M. Ergeba. Biol. 64, 166–307 (1972).

    CAS  Google Scholar 

  5. Aston-Jones, G. & Bloom, F. E. J. Neurosci. 1, 876–886 (1981).

    Article  CAS  Google Scholar 

  6. Trulson, M. E. & Jacobs, B. L. Brain Res. 163, 135–150 (1979).

    Article  CAS  Google Scholar 

  7. Phillis, J. W., Tebécis, A. K. & York, D. H. J. Physiol., Lond. 190, 563–581 (1967).

    Article  CAS  Google Scholar 

  8. Kayama, Y. Vision Res. 25, 339–347 (1985).

    Article  CAS  Google Scholar 

  9. Rogawski, M. A. & Aghajanian, G. K. Nature 187, 731–734 (1980).

    Article  ADS  Google Scholar 

  10. Nakai, Y. & Takaroi, S. Brain Res. 1, 47–60 (1974).

    Article  Google Scholar 

  11. Yoshida, M., Sasa, M. & Takaori, S. Brain Res. 290, 95–105 (1984).

    Article  CAS  Google Scholar 

  12. Crunelli, V., Haby, M., Jassik-Gerschenfeld, D., Leresche, N. & Pirchio, M. J. Physiol., Lond. 399, 153–176 (1988).

    Article  CAS  Google Scholar 

  13. Pazos, A. & Palacios, J. M. Brain Res. 346, 205–230 (1985).

    Article  CAS  Google Scholar 

  14. Pazos, A., Cortes, R. & Palacios, J. M. Brain Res. 346, 231–249 (1985).

    Article  CAS  Google Scholar 

  15. Nicoll, R. A. Science 241, 545–551 (1988).

    Article  ADS  CAS  Google Scholar 

  16. Halliwell, J. V. & Adams, P. R. Brain Res. 250, 71–92 (1982).

    Article  CAS  Google Scholar 

  17. DiFrancesco, D. Prog. Biophys. molec. Biol. 46, 163–183 (1985).

    Article  CAS  Google Scholar 

  18. Crepel, F. & Penit-Soria, J. J. Physiol., Lond. 372, 1–23 (1986).

    Article  CAS  Google Scholar 

  19. Spain, W. J., Schwindt, P. C. & Crill, W. E. J. Neurophysiol. 57, 1555–1576 (1987).

    Article  CAS  Google Scholar 

  20. Yarom, Y. & Llinás, R. R. J. Neurosci. 7, 1166–1177 (1987).

    Article  CAS  Google Scholar 

  21. Lacey, M. G. & North, R. A. J. Physiol., Lond. 407, 18P (1988).

    Google Scholar 

  22. Madison, D. V., Malenka, R. C. & Nicoll, R. A. Nature 321, 695–697 (1986).

    Article  ADS  CAS  Google Scholar 

  23. Tsien, R. W. J. gen. Physiol. 64, 293–319 (1974).

    Article  CAS  Google Scholar 

  24. Brown, H. F., DiFrancesco, D. & Noble, S. J. Nature 280, 235–236 (1979).

    Article  ADS  CAS  Google Scholar 

  25. Hagiwara, N. & Irisawa, H. J. Physiol., Lond. 409, 121–141 (1989).

    Article  CAS  Google Scholar 

  26. Kupferman, I. A. Rev. Neurosci. 42, 629–641 (1980).

    Google Scholar 

  27. Thompson, S. M., Deisz, R. A. & Prince, D. A. Neurosci. Lett. 89, 49–54 (1988).

    Article  CAS  Google Scholar 

  28. McCormick, D. A. & Prince, D. A. J. Physiol., Lond. 392, 147–165 (1987).

    Article  CAS  Google Scholar 

  29. McCormick, D. A. & Prince, D. A. J. Neurophysiol. 59, 978–996 (1988).

    Article  CAS  Google Scholar 

  30. McCormick, D. A. & Pape, H.-C. Nature 334, 246–248 (1988).

    Article  ADS  CAS  Google Scholar 

  31. Livingstone, M. S. & Hubel, D. H. Nature 291, 554–561 (1981).

    Article  ADS  CAS  Google Scholar 

  32. Jahnsen, H. & Llinás, R. J. Physiol., Lond. 349, 205–226 (1984).

    Article  CAS  Google Scholar 

  33. Jahnsen, H. & Llinás, R. J. Physiol., Lond. 349, 227–247 (1984).

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Pape, HC., McCormick, D. Noradrenaline and serotonin selectively modulate thalamic burst firing by enhancing a hyperpolarization-activated cation current. Nature 340, 715–718 (1989). https://doi.org/10.1038/340715a0

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/340715a0

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing