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Voltage-Controlled Plasticity at GluR2-Deficient Synapses Onto Hippocampal Interneurons

Department of Pharmacology, Emory University School of Medicine, Atlanta, Georgia 30322

Submitted 26 April 2004; accepted in final form 23 August 2004

High-frequency stimulation of pyramidal cell inputs to developing (P9-12) hippocampal stratum radiatum interneurons expressing GluR2-lacking, Ca²⁺-permeable AMPA receptors produces long-term depression of synaptic transmission, if N-methyl-D-aspartate (NMDA) receptors are blocked. Here we show that these same synapses display a remarkably versatile signal integration if postsynaptic NMDA receptors are activated. At synapses expressing GluR2-deficient AMPA receptors, tetanic stimulation that activates NMDA receptors triggered long-term potentiation or depression (LTP or LTD) depending on membrane potential. LTP was elicited at most synapses when the interneuron was held at –30 mV during the stimulus train but was typically prevented by postsynaptic hyperpolarization to –70 mV, by strong depolarization to 0 mV, by D-2-amino-5-phosphonovaleric acid, or by postsynaptic injection of the Ca²⁺ chelator bis-(o-aminophenoxy)-N,N,N',N'-tetraacetic acid. At synapses with predominantly GluR2-containing AMPA receptors, repetitive stimulation did not change synaptic strength regardless of whether NMDA receptors were activated. The interactions among GluR2 expression, NMDA receptor expression, and membrane potential thus confer on hippocampal interneurons a distinctive means for differential decoding of high-frequency inputs, resulting in enhanced or depressed transmission depending on the functional state of the interneuron.

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