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Synchronized oscillations in interneuron networks driven by metabotropic glutamate receptor activation

Abstract

PARTIALLY synchronous 40-Hz oscillations of cortical neurons have been implicated in cognitive function. Specifically, coherence of these oscillations between different parts of the cortex may provide conjunctive properties1,2 to solve the 'binding problem' associating features detected by the cortex into unified perceived objects. Here we report an emergent 40-Hz oscillation in networks of inhibitory neurons connected by synapses using GABAA (γ-aminobutyric acid) receptors in slices of rat hippocampus and neocortex. These network inhibitory postsynaptic potential oscillations occur in response to the activation of metabotropic glutamate receptors. The oscillations can entrain pyramidal cell discharges. The oscillation frequency is determined both by the net excitation of interneurons and by the kinetics of the inhibitory postsynaptic potentials between them. We propose that interneuron network oscillations, in conjunction with intrinsic membrane resonances and long-loop (such as thalamocortical) interactions, contribute to 40-Hz rhythms in vivo.

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References

  1. Llinás, R. R., Grace, A. A. & Yarom, Y. Proc. natn. Acad. Sci. U.S.A 88, 897–901 (1991).

    Article  ADS  Google Scholar 

  2. Gray, C. M. J. comp. Neurosci. 1, 11–38 (1994).

    Article  CAS  Google Scholar 

  3. Miles, R. & Poncer, J.-C. J. Physiol., Lond. 463, 461–473 (1993).

    Article  CAS  Google Scholar 

  4. Davies, C. H., Davies, S. N. & Collingridge, G. L. J. Physiol., Lond. 424, 513–531 (1990).

    Article  CAS  Google Scholar 

  5. Thompson, S. M. & Gähwiler, B. H. J. Neurophysiol. 61, 501–511 (1989).

    Article  CAS  Google Scholar 

  6. Davies, S. N. & Collingridge, G. L. Proc. R. Soc. B236, 373–384 (1989).

    Article  ADS  CAS  Google Scholar 

  7. Ropert, N., Miles, R. & Korn, H. J. Physiol., Lond. 428, 707–722 (1990).

    Article  CAS  Google Scholar 

  8. Katsumaru, H., Kosaka, T., Heizmann, C. W. & Hama, K. Expl Brain Res. 72, 363–370 (1988).

    CAS  Google Scholar 

  9. Michelson, H. B. & Wong, R. K. S. J. Physiol., Lond. 477, 35–45 (1994).

    Article  CAS  Google Scholar 

  10. Bashir, Z. I. et al. Nature 363, 347–350 (1993).

    Article  ADS  CAS  Google Scholar 

  11. Gray, C. M., König, P., Engel, A. K. & Singer, W. Nature 338, 334–337 (1989).

    Article  ADS  CAS  Google Scholar 

  12. Gray, C. M. & Singer, W. Proc. natn. Acad. Sci. U.S.A. 86, 1698–1702 (1989).

    Article  ADS  CAS  Google Scholar 

  13. Engel, A. K., König, P., Gray, C. M. & Singer, W. Eur. J. Neurosci. 2, 588–606 (1990).

    Article  Google Scholar 

  14. Engel, A. K., Kreiter, A. K., König, P. & Singer, W. Proc. natn. Acad. Sci. U.S.A. 88, 6048–6052 (1991).

    Article  ADS  CAS  Google Scholar 

  15. Engel, A. K., König, P., Kreiter, A. K. & Singer, W. Science 252, 1177–1179 (1991).

    Article  ADS  CAS  Google Scholar 

  16. Engel, A. K., König, P. & Singer, W. Proc. natn. Acad. Sci. U.S.A. 88, 9136–9140 (1991).

    Article  ADS  CAS  Google Scholar 

  17. Llinás, R. & Ribary, U. Proc. natn. Acad. Sci. U.S.A. 90, 2078–2081 (1993).

    Article  ADS  Google Scholar 

  18. Ribary, U. et al. Proc. natn. Acad. Sci. U.S.A. 88, 11037–11041 (1991).

    Article  ADS  CAS  Google Scholar 

  19. Soltesz, I. & Deschênes, M. J. Neurophysiol. 70, 97–116 (1993).

    Article  CAS  Google Scholar 

  20. Adrian, E. D. Electroencephalogr. clin. Neurophysiol. 2, 377–388 (1950).

    Article  CAS  Google Scholar 

  21. Bressler, S. L. & Freeman, W. J. Electroencephalogr. clin. Neurophysiol. 50, 19–24 (1980).

    Article  CAS  Google Scholar 

  22. Nuñez, A., Amzica, F. & Steriade, M. Neuroscience 51, 7–10 (1992).

    Article  Google Scholar 

  23. Steriade, M., Curro Dossi, R. & Contreras, D. Neuroscience 56, 1–9 (1993).

    Article  CAS  Google Scholar 

  24. Eeckman, F. H. & Freeman, W. J. Brain Res. 528, 238–244 (1990).

    Article  CAS  Google Scholar 

  25. Lytton, W. W. & Sejnowski, T. J. J. Neurophysiol. 66, 1059–1078 (1991).

    Article  CAS  Google Scholar 

  26. Buhl, E. M., Halasy, K. & Somogyi, P. Nature 368, 823–828 (1994).

    Article  ADS  CAS  Google Scholar 

  27. McBain, C. J., DiChiara, T. J. & Kauer, J. A. J. Neurosci. 14, 4433–4445 (1994).

    Article  CAS  Google Scholar 

  28. Gulyás, A. I. et al. Nature 366, 683–687 (1993).

    Article  ADS  Google Scholar 

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Whittington, M., Traub, R. & Jefferys, J. Synchronized oscillations in interneuron networks driven by metabotropic glutamate receptor activation. Nature 373, 612–615 (1995). https://doi.org/10.1038/373612a0

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