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The Journal of Neuroscience, May 4, 2005, 25(18):4473-4484; doi:10.1523/JNEUROSCI.4050-04.2005

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Development/Plasticity/Repair
Endogenous Activation of Kainate Receptors Regulates Glutamate Release and Network Activity in the Developing Hippocampus

Sari E. Lauri,¹ Mikael Segerstråle,¹ Aino Vesikansa,¹ Francois Maingret,² Christophe Mulle,³ Graham L. Collingridge,² John T. R. Isaac,^2,4 and Tomi Taira¹

¹Neuroscience Center and Department of Biological and Environmental Sciences, University of Helsinki, 00014 Helsinki, Finland, ²Medical Research Council Centre for Synaptic Plasticity, Department of Anatomy, Medical School, University of Bristol, Bristol BS8 1TD, United Kingdom, ³Laboratoire Physiologie Cellulaire de la Synapse, Centre National de la Recherche Scientifique, Unité Mixte de Recherche 5091, Institut Francois Magendie, Université Bordeaux 2, 33076 Bordeaux Cedex, France, and ⁴National Institutes of Health-National Institute of Neurological Disorders and Stroke, Bethesda, Maryland 20892

Kainate receptors (KARs) are highly expressed throughout the neonatal brain, but their function during development is unclear. Here, we show that the maturation of the hippocampus is associated with a switch in the functional role of presynaptic KARs. In a developmental period restricted to the first postnatal week, endogenous L-glutamate tonically activates KARs at CA3 glutamatergic synapses to regulate release in an action potential-independent manner. At synapses onto pyramidal cells, KARs inhibit glutamate release via a G-protein and PKC-dependent mechanism. In contrast, at glutamatergic terminals onto CA3 interneurons, presynaptic KARs can facilitate release in a G-protein-independent mechanism. In both cell types, however, KAR activation strongly upregulates inhibitory transmission. We show that, through the interplay of these novel diverse mechanisms, KARs strongly regulate the characteristic synchronous network activity observed in the neonatal hippocampus. By virtue of this, KARs are likely to play a central role in the development of hippocampal synaptic circuits.

Key words: development; interneuron; presynaptic; plasticity; pyramidal cell; synaptic transmission

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Received Sep 30, 2004; revised February 23, 2005; accepted March 18, 2005.

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