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The Journal of Neuroscience, September 23, 2009, 29(38):11807-11816; doi:10.1523/JNEUROSCI.2617-09.2009

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Development/Plasticity/Repair
A Novel Postsynaptic Group II Metabotropic Glutamate Receptor Role in Modulating Baroreceptor Signal Transmission

Shin-ichi Sekizawa, Andrea G. Bechtold, Rick C. Tham, and Ann C. Bonham

Department of Pharmacology, School of Medicine, University of California Davis, Davis, California 95616-0635

Correspondence should be addressed to Dr. Shin-ichi Sekizawa, Department of Pharmacology, School of Medicine, University of California Davis, GBSF Room 3617, 451 Health Sciences Drive, Davis, CA 95616. Email: ssekizawa{at}ucdavis.edu

The nucleus tractus solitarius (NTS) is essential for orchestrating baroreflex control of blood pressure. When a change in blood pressure occurs, the information is transmitted by baroreceptor afferent fibers to the central network by glutamate binding to ionotropic glutamate receptors on second-order baroreceptor neurons. Glutamate also activates presynaptic group II and III metabotropic glutamate receptors (mGluRs), depressing both glutamate and GABA release to modulate baroreceptor signal transmission. Here we present a novel role for postsynaptic group II mGluRs to further fine-tune baroreceptor signal transmission at the first central synapses. In a brainstem slice with ionotropic glutamate and GABA receptors blocked, whole-cell patch-clamp recordings of second-order baroreceptor neurons revealed that two group II mGluR agonists evoked concentration-dependent membrane hyperpolarizations. The hyperpolarization remained when a presynaptic contribution was prevented with Cd2+, was blocked by a postsynaptic intervention of intracellular dialysis of the G-protein signaling inhibitor, was mimicked by endogenous release of glutamate by tractus solitarius stimulation, and was prevented by a group II mGluR antagonist. Postsynaptic localization of group II mGluRs was confirmed by fluorescent confocal immunohistochemistry and light microscopy. Group II mGluR induced-currents consisted of voltage-dependent outward and inward components, prevented by tetraethylammonium chloride and tetrodotoxin, respectively. In contrast to group II mGluR-induced hyperpolarization, there was no effect on intrinsic excitability as determined by action potential shape or firing in response to depolarizing current injections. The data suggest a novel mechanism for postsynaptic group II mGluRs to fine-tune baroreceptor signal transmission in the NTS.

Received June 4, 2009; revised July 20, 2009; accepted Aug. 10, 2009.

Correspondence should be addressed to Dr. Shin-ichi Sekizawa, Department of Pharmacology, School of Medicine, University of California Davis, GBSF Room 3617, 451 Health Sciences Drive, Davis, CA 95616. Email: ssekizawa{at}ucdavis.edu
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