GluR5 kainate receptor activation in interneurons increases tonic inhibition of pyramidal cells

Nature Neuroscience

Volumn 1, Issue 6, 1998, Pages 470-478

  Cossart, Rosa ^a   Esclapez, Monique ^a   Hirsch, June C ^a   Bernard, Christophe ^a   Ben Ari, Yehezkel ^a  

^a Hôpital de Port Royal ^*  (France)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID RECEPTOR STIMULATING AGENT; GLUR5 KAINATE RECEPTOR; KAINIC ACID; KAINIC ACID RECEPTOR;

ANIMAL; ARTICLE; DRUG EFFECT; EXCITATORY POSTSYNAPTIC POTENTIAL; INTERNEURON; METABOLISM; NERVE CELL INHIBITION; PHYSIOLOGY; PYRAMIDAL NERVE CELL; RAT; ULTRASTRUCTURE; WISTAR RAT;

ANIMALS; EXCITATORY AMINO ACID AGONISTS; EXCITATORY POSTSYNAPTIC POTENTIALS; INTERNEURONS; KAINIC ACID; NEURAL INHIBITION; PYRAMIDAL CELLS; RATS; RATS, WISTAR; RECEPTORS, KAINIC ACID;

EID: 0032176966     PISSN: 10976256     EISSN: None     Source Type: Journal    
DOI: 10.1038/2185     Document Type: Article

References (38)

1. Siegel, S.J. et al. Distribution of the excitatory amino acid receptor subunits GluR2(4) in monkey hippocampus and colocalization with subunits GluR5-7 and NMDAR1. J. Neurosci. 15, 2707-2719 (1995).
2. Huntley, G.W. et al. Selective distribution of kainate receptor subunit immunoreactivity in monkey neocortex revealed by a monoclonal antibody that recognizes glutamate receptor subunits GluR5/6/7. J. Neurosci. 13, 2965-2981 (1993).
3. Good, P.F., Huntley, G.W., Rogers, S.W., Heinemann, S.F. & Morrison, J.H. Organization and quantitative analysis of kainate receptor subunit GluR5-7 immunoreactivity in monkey hippocampus. Brain Res. 624, 347-353 (1993).
4. Bahn, S., Volk, B. & Wisden, W. Kainate receptor gene expression in the developing rat brain. J. Neurosci. 14, 5525-5547 (1994).
5. Bettler, B. et al. Cloning of a novel glutamate receptor subunit, GluR5: expression in the nervous system during development. Neuron 5, 583-595 (1990).
6. Lerma, J., Morales, M., Vicente, M.A. & Herreras, O. Glutamate receptors of the kainate type and synaptic transmission. Trends. Neurosci. 20, 9-12 (1997).
7. Ben-Ari, Y. Limbic seizure and brain damage produced by kainic acid: mechanisms and relevance to human temporal lobe epilepsy. Neuroscience 14, 375-403 (1985).
8. Nadler, J. Kainic acid as a tool for the study of temporal lobe epilepsy. Life Sci. 29, 2031-2042 (1981).
9. Ben-Ari, Y. & Gho, M. Long-lasting modification of the synaptic properties of rat CA3 hippocampal neurones induced by kainic acid. J. Physiol. (Lond.) 404, 365-384 (1988).
10. Westbrook, G.L. & Lothman, E.W. Cellular and synaptic basis of kainic acid-induced hippocampal epileptiform activity. Brain Res. 273, 97-109 (1983).
11. Robinson, J.H. & Deadwyler, S.A. Kainic acid produces depolarization of CA3 pyramidal cells in the vitro hippocampal slice. Brain Res. 221, 117-127 (1981).
12. Gaiarsa, J.L., Beaudoin, M. & Ben-Ari, Y. Effect of neonatal degranulation on the morphological development of rat CA3 pyramidal neurons: Inductive role of mossy fibers on the formation of thorny excrescences. J. Comp. Neurol. 321, 612-625 (1992).
13. Gaiarsa, J.-L., Zagrean, L. & Ben-Ari, Y. Neonatal irradiation prevents the formation of hippocampal mossy fibers and the epileptic action of kainate on rat CA3 pyramidal neurons. J. Neurophysiol 71, 204-215 (1994).
14. Represa, A. & Ben-Ari, Y. Kindling is associated with the formation of novel mossy fibre synapses in the CA3 region. Exp. Brain Res. 92, 69-78 (1992).
15. Mulle, C. et al. Altered synaptic physiology and reduced susceptibility to kainate-induced seizures in GluR6-deficient mice. Nature 392, 601-604 (1998).
16. Castillo, P.E., Malenka, R.C. & Nicoll, R.A. Kainate receptors mediate a slow postsynaptic current in hippocampal CA3 neurons. Nature 388, 182-186 (1997).
17. Vignes, M. & Collingridge, G.L. The synaptic activation of kainate receptors. Nature 388, 179-182 (1997).
18. Fisher, R.S. & Alger, B.E. Electrophysiological mechanisms of kainic acid-induced epileptiform activity in the rat hippocampal slice. J. Neurosci. 4, 1312-1323 (1984).
19. Rodriguez-Moreno, A., Herreras, O. & Lerma, J. Kainate receptors presynaptically downregulate GABAergic inhibition in the rat hippocampus. Neuron 19, 893-901 (1997).
20. Clarke, V.R. et al. A hippocampal GluR5 kainate receptor regulating inhibitory synaptic transmission. Nature 389, 599-603 (1997).
21. Freund, T.F. & Buzsaki, G. Interneurons of the hippocampus. Hippocampus 6, 347-470 (1996).
22. B-activated K+ conductance by kainate and quisqualate in rat CA3 hippocampal pyramidal neurones. Pflugers Arch. 415, 471-478 (1990).
23. Congar, P., Leinekugel, X., Ben-Ari, Y. & Crepel, V. A long-lasting calcium-activated nonselective cationic current is generated by synaptic stimulation or exogeneous activation of group I metabotropic glutamate receptors in CA1 pyramidal neurons. J. Neurosci. 17, 5366-5379 (1997).
24. Vida, I., Halasy, K., Szinyei, C., Somogyi, P. & Buhl, E.H. Unitary IPSPs evoked by interneurons at the stratum radiatum-stratum lacunosum-moleculare border in the CA1 area of the rat hippocampus in vitro. J. Physiol. (Lond.) 506, 755-773 (1998).
25. Poncer, J.C., Shinozaki, H. & Miles, R. Dual modulation of synaptic inhibition by distinct metabotropic glutamate receptors in the rat hippocampus. J. Physiol. (Lond). 485, 121-134 (1995).
26. Frazier, C.J. et al. Acetylcholine activates an alpha-bungarotoxin-sensitive nicotinic current in rat hippocampal interneurons, but not pyramidal cells. J. Neurosci. 18, 1187-1195 (1998).
27. Bergles, D.E., Doze, V.A., Madison, D.V. & Smith, S.J. Excitatory actions of norepinephrine on multiple classes of hippocampal CA1 interneurons. J. Neurosci. 16, 572-585 (1996).
28. Kondo, S. & Marty, A. Differential effects of noradrenaline on evoked, spontaneous and miniature IPSCs in rat cerebellar stellate cells. J. Physiol. (Lond.) 509, 233-243 (1998).
29. Radnikow, G. & Misgeld, U. Dopamine D1 receptors facilitate GABAA synaptic currents in the rat substantia nigra pars reticulata. J. Neurosci. 18, 2009-2016 (1998).
30. Miller, K.K., Hoffer, A., Svoboda, K.R. & Lupica, C.R. Cholecystokinin increases GABA release by inhibiting a resting K+ conductance in hippocampal interneurons. J. Neurosci. 17, 4994-5003 (1997).
31. Wang, H.L., Li, A. & Wu, T. Vasoactive intestinal polypeptide enhances the GABAergic synaptic transmission in cultured hippocampal neurons. Brain Res. 746, 294-300 (1997).
32. Batchelor, A.M., Madge, D.J. & Garthwaite, J. Synaptic activation of metabotropic glutamate receptors in the parallel fibre-Purkinje cell pathway in rat cerebellar slices. Neuroscience 63, 911-915 (1994).
33. Rodriquez-Moreno, A. & Lerma, J. Kainate receptor modulation of GABA release involves a metabotropic function. Neuron 20, 1211-1218 (1998).
34. Lerma, J. Kainate reveals its targets. Neuron 19, 1155-1158 (1997).
35. Kondo, S. & Marty, A. Synaptic currents at individual connections among stellate cells in rat cerebellar slices. J. Physiol. (Lond.) 509, 221-232 (1998).
36. Häusser, M. & Clark, B.A. Tonic synaptic inhibition modulates neuronal output pattern and spatiotemporal synaptic integration. Neuron 19, 665-678 (1997).
37. Houser, C.R. & Esclapez, M. Vulnerability and plasticity of the GABA system in the pilocarpine model of spontaneous recurrent seizures. Epilepsy Res. 26, 207-218 (1996).
38. Esclapez, M., Hirsch, J. C., Khazipov, R., Ben-Ari, Y. & Bernard, C. Operative GABAergic inhibition in hippocampal CA1 pyramidal neurons in experimental epilepsy. Proc. Natl. Acad. Sci. USA 94, 12151-12156 (1997).