A network of electrically coupled interneurons drives synchronized inhibition in neocortex (original) (raw)

References

  1. Holt, G. R., Softky, W. R., Koch, C. & Douglas, R. J. Comparison of discharge variability in vitro and in vivo in cat visual cortex neurons . J. Neurophysiol. 75, 1806– 1814 (1996).
    Article CAS Google Scholar
  2. Gray, C. M. The temporal correlation hypothesis of visual feature integration: still alive and well. Neuron 24, 31– 47 (1999).
    Article CAS Google Scholar
  3. deCharms, R. C. & Merzenich, M. M. Primary cortical representation of sounds by the coordination of action-potential timing. Nature 381, 610–613 (1996).
    Article CAS Google Scholar
  4. Donoghue, J. P., Sanes, J. N., Hatsopoulos, N. G. & Gaal, G. Neural discharge and local field potential oscillations in primate motor cortex during voluntary movements. J. Neurophysiol. 79, 159–173 (1998).
    Article CAS Google Scholar
  5. Azouz, R. & Gray, C. M. Cellular mechanisms contributing to response variability of cortical neurons in vivo. J. Neurosci. 19, 2209–2223 (1999).
    Article CAS Google Scholar
  6. Stevens, C. F. & Zador, A. M. Input synchrony and the irregular firing of cortical neurons. Nat. Neurosci. 1, 210–217 (1998).
    Article CAS Google Scholar
  7. Lampl, I., Reichova, I. & Ferster, D. Synchronous membrane potential fluctuations in neurons of the cat visual cortex. Neuron 22, 361 –374 (1999).
    Article CAS Google Scholar
  8. Steriade, M. Synchronized activities of coupled oscillators in the cerebral cortex and thalamus at different levels of vigilance. Cereb. Cortex 7, 583–604 (1997).
    Article CAS Google Scholar
  9. Fisahn, A., Pike, F. G., Buhl, E. H. & Paulsen, O. Cholinergic induction of network oscillations at 40 Hz in the hippocampus in vitro. Nature 394, 186–189 (1998).
    Article CAS Google Scholar
  10. Buzsaki, G. & Chrobak, J. J. Temporal structure in spatially organized neuronal ensembles: a role for interneuronal networks. Curr. Opin. Neurobiol. 5, 504–510 (1995).
    Article CAS Google Scholar
  11. Benardo, L. S. Recruitment of GABAergic inhibition and synchronization of inhibitory interneurons in rat neocortex. J. Neurophysiol. 77, 3134 –3144 (1997).
    Article CAS Google Scholar
  12. Zhang, Y. et al. Slow oscillations (≤1 Hz) mediated by GABAergic interneuronal networks in rat hippocampus. J. Neurosci. 18, 9256–9268 (1998).
    Article Google Scholar
  13. Whittington, M. A., Traub, R. D. & Jefferys, J. G. Synchronized oscillations in interneuron networks driven by metabotropic glutamate receptor activation. Nature 373, 612–615 (1995).
    Article CAS Google Scholar
  14. Traub, R. D., Jefferys, J. G. R. & Whittington, M. A. Fast Oscillations in Cortical Circuits (MIT Press, Cambridge, Massachusetts, 1999).
    Book Google Scholar
  15. Skinner, F. K., Zhang, L., Velazquez, J. L. & Carlen, P. L. Bursting in inhibitory interneuronal networks: A role for gap-junctional coupling . J. Neurophysiol. 81, 1274– 1283 (1999).
    Article CAS Google Scholar
  16. Kawaguchi, Y. & Kubota, Y. GABAergic cell subtypes and their synaptic connections in rat frontal cortex. Cereb. Cortex. 7, 476–486 (1997).
    Article CAS Google Scholar
  17. Somogyi, P., Tamas, G., Lujan, R. & Buhl, E. H. Salient features of synaptic organisation in the cerebral cortex. Brain Res. Rev. 26, 113–135 (1998).
    Article CAS Google Scholar
  18. Gibson, J. R., Beierlein, M. & Connors, B. W. Two networks of electrically coupled inhibitory neurons in neocortex. Nature, 402, 75– 79 (1999).
    Article CAS Google Scholar
  19. Galarreta, M. & Hestrin, S. A network of fast-spiking cells in the neocortex connected by electrical synapses. Nature 402, 72–75 (1999).
    Article CAS Google Scholar
  20. Tamás, G., Buhl, E. H., Lörincz, A. & Somogyi, P. Proximally targeted GABAergic synapses and gap junctions synchronize cortical interneurons. Nat. Neurosci. 3, 366– 371 (2000).
    Article Google Scholar
  21. Thomson, A. M. Activity-dependent properties of synaptic transmission at two classes of connections made by rat neocortical pyramidal axons in vitro. J. Physiol (Lond.) 502, 131–147 (1997).
    Article CAS Google Scholar
  22. Reyes, A. et al. Target-cell-specific facilitation and depression in neocortical circuits. Nat. Neurosci. 1, 279– 285 (1998).
    Article CAS Google Scholar
  23. Kawaguchi, Y. Selective cholinergic modulation of cortical GABAergic cell subtypes. J. Neurophysiol. 78, 1743–1747 (1997).
    Article CAS Google Scholar
  24. Kawaguchi, Y. & Shindou, T. Noradrenergic excitation and inhibition of GABAergic cell types in rat frontal cortex. J. Neurosci. 18, 6963–6976 (1998).
    Article CAS Google Scholar
  25. Xiang, Z., Huguenard, J. R. & Prince, D. A. Cholinergic switching within neocortical inhibitory networks. Science 281, 985– 988 (1998).
    Article CAS Google Scholar
  26. Baude, A. et al. The metabotropic glutamate receptor (mGluR1 alpha) is concentrated at perisynaptic membrane of neuronal subpopulations as detected by immunogold reaction. Neuron 11, 771– 787 (1993).
    Article CAS Google Scholar
  27. Schoepp, D. D. & Conn, P. J. Metabotropic glutamate receptors in brain function and pathology. Trends Pharmacol. Sci. 14, 13–20 (1993).
    Article CAS Google Scholar
  28. Flint, A. C., Dammerman, R. S. & Kriegstein, A. R. Endogenous activation of metabotropic glutamate receptors in neocortical development causes neuronal calcium oscillations. Proc. Natl. Acad. Sci. USA 96, 12144– 12149 (1999).
    Article CAS Google Scholar
  29. Yuste, R., Peinado, A. & Katz, L. C. Neuronal domains in developing neocortex. Science 257, 665–669 (1992).
    Article CAS Google Scholar
  30. Kandler, K. & Katz, L. C. Coordination of neuronal activity in developing visual cortex by gap junction-mediated biochemical communication . J. Neurosci. 18, 1419– 1427 (1998).
    Article CAS Google Scholar
  31. Wang, X. J. & Rinzel, J. Spindle rhythmicity in the reticularis thalami nucleus: synchronization among mutually inhibitory neurons. Neuroscience 53, 899–904 (1993).
    Article CAS Google Scholar
  32. Van Vreeswijk, C., Abbott, L. F. & Ermentrout, G. B. When inhibition not excitation synchronizes neural firing. J. Comput. Neurosci. 1, 313– 321 (1994).
    Article CAS Google Scholar
  33. Buhl, E. H., Tamas, G. & Fisahn, A. Cholinergic activation and tonic excitation induce persistent gamma oscillations in mouse somatosensory cortex in vitro. J. Physiol. (Lond.) 513, 117–126 (1998).
    Article CAS Google Scholar
  34. Bennett, M. V. Gap junctions as electrical synapses. J. Neurocytol. 26, 349–366 (1997).
    Article CAS Google Scholar
  35. Manor, Y., Rinzel, J., Segev, I. & Yarom, Y. Low-amplitude oscillations in the inferior olive: a model based on electrical coupling of neurons with heterogeneous channel densities. J. Neurophysiol. 77 , 2736–2752 (1997).
    Article CAS Google Scholar
  36. Michelson, H. B. & Wong, R. K. Synchronization of inhibitory neurones in the guinea-pig hippocampus in vitro. J. Physiol. (Lond.) 477, 35–45 (1994).
    Article CAS Google Scholar
  37. Lytton, W. W. & Sejnowski, T. J. Simulations of cortical pyramidal neurons synchronized by inhibitory interneurons. J. Neurophysiol. 66, 1059–1079 (1991).
    Article CAS Google Scholar
  38. Cobb, S. R., Buhl, E. H., Halasy, K., Paulsen, O. & Somogyi, P. Synchronization of neuronal activity in hippocampus by individual GABAergic interneurons. Nature 378, 75–78 (1995).
    Article CAS Google Scholar
  39. Engel, A. K., Roelfsema, P. R., Fries, P., Brecht, M. & Singer, W. Role of the temporal domain for response selection and perceptual binding. Cereb. Cortex 7, 571–582 (1997).
    Article CAS Google Scholar
  40. Hatsopoulos, N. G., Ojakangas, C. L., Paninski, L. & Donoghue, J. P. Information about movement direction obtained from synchronous activity of motor cortical neurons. Proc. Natl. Acad. Sci. USA 95, 15706–15711 (1998).
    Article CAS Google Scholar
  41. Mainen, Z. F. & Sejnowski, T. J. Reliability of spike timing in neocortical neurons. Science 268, 1503 –1506 (1995).
    Article CAS Google Scholar
  42. Häusser, M. & Clark, B. A. Tonic synaptic inhibition modulates neuronal output pattern and spatiotemporal synaptic integration . Neuron 19, 665–678 (1997).
    Article Google Scholar
  43. Agmon, A. & Connors, B. W. Thalamocortical responses of mouse somatosensory (barrel) cortex in vitro. Neuroscience 41, 365–379 (1991).
    Article CAS Google Scholar

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