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.

Electrical coupling underlies high-frequency oscillations in the hippocampus in vitro

Abstract

Coherent oscillations, in which ensembles of neurons fire in a repeated and synchronous manner, are thought to be important in higher brain functions. In the hippocampus, these discharges are categorized according to their frequency as theta (4–10 Hz)1, gamma (20–80 Hz)2 and high-frequency (200 Hz)3,4,5 discharges, and they occur in relation to different behavioural states. The synaptic bases of theta and gamma rhythms have been extensively studied6,7 but the cellular bases for high-frequency oscillations are not understood. Here we report that high-frequency network oscillations are present in rat brain slices in vitro, occurring as a brief series of repetitive population spikes at 150–200 Hz in all hippocampal principal cell layers. Moreover, this synchronous activity is not mediated through the more commonly studied modes of chemical synaptic transmission, but is in fact a result of direct electrotonic coupling of neurons, most likely through gap-junctional connections. Thus high-frequency oscillations synchronize the activity of electrically coupled subsets of principal neurons within the well-documented synaptic network of the hippocampus.

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

Figure 1: High-frequency oscillations in CA3.
Figure 2: High-frequency oscillations do not depend on synaptic transmission.
Figure 3: Gap-junctional coupling and high-frequency oscillations.
Figure 4: Cellular activity during high-frequency oscillations.

Similar content being viewed by others

References

  1. Vanderwolf, C. H. Hippocampal electrical activity and voluntary movement in the rat. Electroencephalogr. Clin. Neurophysiol. 26, 407–418 (1969).

    Article  CAS  Google Scholar 

  2. Stumpf, C. The fast component in the electrical activity of rabbit's hippocampus. Electroencephalogr. Clin. Neurophysiol. 18, 477–486 (1965).

    Article  CAS  Google Scholar 

  3. Chrobak, J. J. & Buzsáki, G. High-frequency oscillations in the output network of the hippocampal-entorhinal axis of the freely behaving rat. J. Neurosci. 16, 3056–3066 (1996).

    Article  CAS  Google Scholar 

  4. Ylinen, A. et al. Sharp wave-associated high-frequency oscillation (200 Hz) in the intact hippocampus: network and intracellular mechanisms. J. Neurosci. 15, 30–46 (1995).

    Article  CAS  Google Scholar 

  5. Buzsáki, G., Horváth, Z., Urioste, R., Hetke, J. & Wise, K. High-frequency network oscillation in the hippocampus. Science 256, 1025–1027 (1992).

    Article  ADS  Google Scholar 

  6. Cobb, S. R., Buhl, E. H., Halasy, K., Paulsen, O. & Somogyi, P. Synchronization of neuronal activity in hippocampus by individual GABAergic interneurons. Nature 378, 612–615 (1995).

    Article  Google Scholar 

  7. Whittington, M. A., Traub, R. D. & Jefferys, J. G. R. Synchronized oscillations in interneuron networks driven by metabotropic glutamate receptor activation. Nature 373, 612–615 (1995).

    Article  ADS  CAS  Google Scholar 

  8. Jefferys, J. G. R. & Haas, H. L. Synchronized bursting of CA1 pyramidal cells in the absence of synaptic transmission. Nature 300, 448–450 (1982).

    Article  ADS  CAS  Google Scholar 

  9. Taylor, C. P. & Dudek, F. E. Synchronous neural afterdischarges in rat hippocampal slices without active chemical synapses. Science 218, 810–812 (1982).

    Article  ADS  CAS  Google Scholar 

  10. Valiante, T. A., Perez-Velazquez, J. L., Jahromi, S. S. & Carlen, P. L. Coupling potentials in A1 neurons during calcium-free-induced field burst activity. J. Neurosci. 15, 6946–6956 (1995).

    Article  CAS  Google Scholar 

  11. Leslie, J., Nolan, M. F., Logan, S. D. & Spanswick, D. Actions of carbenoxolone on rat sympathetic preganglionic neurones in vitro. J. Physiol. (Lond.) 506P, 146 (1998).

    Google Scholar 

  12. Thomas, R. C. Experimental displacement of intracellular pH and the mechanism of its subsequent recovery. J. Physiol. (Lond.) 354, 3–22 (1984).

    Article  Google Scholar 

  13. Spray, D. C., Harris, A. L. & Bennett, M. V. L. Gap junctional conductance is a simple and sensitive function of intracellular pH. Science 211, 712–715 (1981).

    Article  ADS  CAS  Google Scholar 

  14. Spencer, W. A. & Kandel, E. R. Electrophysiology of hippocampal neurons. IV. Fast prepotentials. J. Neurophysiol. 24, 272–285 (1961).

    Article  CAS  Google Scholar 

  15. Traub, R. D., Jefferys, J. G. R., Miles, R., Whittington, M. A. & Tóth, K. Abranching dendritic model of a rodent CA3 pyramidal neurone. J. Physiol. (Lond.) 481, 79–95 (1994).

    Article  CAS  Google Scholar 

  16. Jefferys, J. G. R. Influence of electric fields on the excitability of granule cells in guinea-pig hippocampal slices. J. Physiol. (Lond.) 319, 143–152 (1981).

    Article  CAS  Google Scholar 

  17. Rash, J. et al. Grid-mapped freeze-fracture analysis of gap junctions in gray and white matter of adult rat central nervous system, with evidence for a “pan-glial syncytium” that is not coupled to neurons. J. Comp. Neurol. 388, 265–292 (1997).

    Article  CAS  Google Scholar 

  18. Church, J. & Baimbridge, K. G. Exposure to high-pH medium increases the incidence and extent of dye coupling between rat hippocampal CA1 pyramidal neurons in vitro. J. Neurosci. 11, 3289–3295 (1991).

    Article  CAS  Google Scholar 

  19. MacVicar, B. A. & Dudeck, F. E. Electrotonic coupling between pyramidal cells: a direct demonstration in rat hippocampal slices. Science 213, 782–785 (1981).

    Article  ADS  CAS  Google Scholar 

  20. Simbürger, E., Stang, A., Kremer, M. & Dermietzel, R. Expression of connexin 43 in adult rodent brain. Histochem. Cell Biol. 107, 127–137 (1997).

    Article  Google Scholar 

  21. MacVicar, B. A. & Jahnsen, H. Uncoupling of CA3 pyramidal neurons by propionate. Brain Res. 330, 141–145 (1985).

    Article  CAS  Google Scholar 

  22. Perez-Velazquez, J. L., Valiante, T. A. & Carlen, P. L. Modulation of gap junctional mechanisms during calcium-free induced field burst activity: a possible role for electrotonic coupling in epileptogenesis. J. Neurosci. 14, 4308–4317 (1994).

    Article  CAS  Google Scholar 

  23. Patrylo, P. R., Kuhn, A. J., Schweitzer, J. S. & Dudeck, F. E. Multiple-unit recordings during slow field-potential shifts in low-[Ca2+]0solutions in rat hippocampal and cortical slices. Neuroscience 74, 107–118 (1996).

    Article  CAS  Google Scholar 

  24. Traub, R. D. Model of synchronized population bursts in electrically coupled interneurons containing active dendritic conductances. J. Comp. Neurosci. 2, 283–289 (1995).

    Article  CAS  Google Scholar 

  25. Strata, F. et al. Pacemaker current in dye-coupled hilar interneurons contributes to the generation of giant GABAergic potentials in developing hippocampus. J. Neurosci. 17, 1435–1446 (1997).

    Article  CAS  Google Scholar 

  26. Logan, S. D., Pickering, A. E., Gibson, I. C., Nolan, M. F. & Spanswick, D. Electrotonic coupling between rat sympathetic preganglionic neurones in vitro. J. Physiol. (Lond.) 495, 491–502 (1996).

    Article  CAS  Google Scholar 

  27. Llinás, R., Baker, R. & Sotelo, C. Electrotonic coupling between neurons in cat inferior olive. J. Neurophysiol. 37, 560–571 (1974).

    Article  Google Scholar 

  28. Vaney, D. I. The coupling pattern of axon-bearing horizontal cells in the mammalian retina. Proc. R. Soc. Lond. B 252, 93–101 (1993).

    Article  ADS  CAS  Google Scholar 

  29. Pinault, D. Backpropagation of action potentials generated at ectopic axonal loci: hypothesis that axon terminals integrate local environmental signals. Brain Res. Brain Res. Rev. 21, 42–92 (1995).

    Article  CAS  Google Scholar 

  30. Hamill, O. P., Marty, A., Neher, E., Sakmann, B. & Sigworth, F. J. Improved patch-clamp techniques for high-resolution recording from cells and cell-free membrane patches. Pflügers Arch. 391, 85–81 (1981).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by a Training grant from the European Commission (toA.D.) and by the Wellcome Trust. R.D.T. is a Wellcome Principal Research Fellow. We thank U.Heinemann, H.-J. Gabriel, S. Gabriel and U. Endermann for discussions.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to A. Draguhn.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Draguhn, A., Traub, R., Schmitz, D. et al. Electrical coupling underlies high-frequency oscillations in the hippocampus in vitro. Nature 394, 189–192 (1998). https://doi.org/10.1038/28184

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/28184

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