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The Journal of Neuroscience, July 23, 2003, 23(16):6660-6670

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Distribution and Properties of Functional Postsynaptic Kainate Receptors on Neocortical Layer V Pyramidal Neurons

Matthias Eder,¹ Klaus Becker,¹ Gerhard Rammes,^1,2 Anja Schierloh,¹ Shahnaz Christina Azad,^1,3 Walter Zieglgänsberger,¹ and Hans-Ulrich Dodt¹

¹Clinical Neuropharmacology, Max-Planck-Institute of Psychiatry, 80804 Munich, Germany, ²Department of Anesthesiology, Technical University of Munich, 81675 Munich, Germany, and ³Clinic for Anesthesiology, Pain Treatment Unit, Ludwig-Maximilians-University, 81377 Munich, Germany

The distribution of glutamate receptor subtypes on the surface of neurons is highly relevant for synaptic transmission and signal processing. In the present study we investigated the location and properties of functional kainate receptors (KARs) on the somatodendritic membrane of rat neocortical layer V pyramidal neurons. Infrared-guided laser stimulation was used to apply glutamate photolytically to the soma and various sites along the apical dendrite. Electrical currents, resulting from the activation of pharmacologically isolated KARs, were measured by whole-cell patch-clamp recording. In addition, KARs on somatic and dendritic outside-out patches were activated while still within the brain tissue. We found that functional KARs are located on the entire somatodendritic membrane that was examined. Fast kinetics, a linear I-V relationship, and a relatively high single-channel conductance are characteristic features of these receptors. We provide evidence that the unitary properties of somatic and dendritic KARs are identical. Regarding the subcellular distribution of KARs, our results indicate that the density of these receptors increases toward the distal dendrite. They are located mainly at extrasynaptic sites but also mediate fast synaptic signaling triggered by afferent stimulation. The differential distribution speaks in favor of a selective targeting of KARs on central neurons and may reflect a mechanism for a location-dependent regulation of synaptic efficacy. Furthermore, it is feasible to assume that extrasynaptic KARs could be activated by a "spillover" of synaptically released glutamate, ambient glutamate in the CSF, or glutamate released from adjacent astrocytes.

Key words: AMPA receptors; brain slices; caged glutamate; dendrite; distribution; extrasynaptic; kainate receptors; layer V; neocortex; photostimulation; pyramidal neuron; rat; somatosensory; synaptic

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Received Apr. 14, 2003; revised May. 29, 2003; accepted Jun. 6, 2003.

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