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The Journal of Neuroscience, October 27, 2004, 24(43):9658-9668; doi:10.1523/JNEUROSCI.2973-04.2004

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Cellular/Molecular
Distinct Roles for the Kainate Receptor Subunits GluR5 and GluR6 in Kainate-Induced Hippocampal Gamma Oscillations

André Fisahn,^1,5 Anis Contractor,² Roger D. Traub,³ Eberhard H. Buhl,^4,5 Stephen F. Heinemann,² and Chris J. McBain¹

¹Laboratory of Cellular and Synaptic Neurophysiology, National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, Maryland 20892, ²Molecular Neurobiology Laboratory, The Salk Institute, La Jolla, California 92037, ³State University of New York Health Science Center, Brooklyn, New York 11203, ⁴School of Biomedical Sciences, University of Leeds, Leeds LS2 9NQ, United Kingdom, and ⁵Medical Research Council Anatomical Neuropharmacology Unit, University of Oxford, Oxford OX1 3TH, United Kingdom

Kainate receptors (KARs) play an important role in synaptic physiology, plasticity, and pathological phenomena such as epilepsy. However, the physiological implications for neuronal networks of the distinct expression patterns of KAR subunits are unknown. Using KAR knock-out mice, we show that subunits glutamate receptor (GluR) 5 and GluR6 play distinct roles in kainate-induced gamma oscillations and epileptiform burst activity. Ablation of GluR5 leads to a higher susceptibility of the network to the oscillogenic and epileptogenic effects of kainate, whereas lack of GluR6 prevents kainate-induced gamma oscillations or epileptiform bursts. Based on experimental and simulated neuronal network data as well as the consequences of GluR5 and GluR6 expression for cellular and synaptic physiology, we propose that the functional interplay of GluR5-containing KARs on axons of interneurons and GluR6-containing KARs in the somatodendritic region of both interneurons and pyramidal cells underlie the oscillogenic and epileptogenic effects of kainate.

Key words: kainate receptors; gamma oscillations; interneurons; hippocampus; knock-out mice; epilepsy

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Received Feb 11, 2004; accepted August 3, 2004.

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