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Group I Metabotropic Glutamate Receptors on Second-Order Baroreceptor Neurons Are Tonically Activated and Induce a Na⁺–Ca²⁺ Exchange Current

Department of Pharmacology, School of Medicine, University of California, Davis, California

Submitted 21 July 2005; accepted in final form 26 September 2005

The nucleus tractus solitarius (NTS) is essential for coordinating baroreflex control of blood pressure. The baroreceptor sensory fibers make glutamatergic synapses onto second-order NTS neurons. Glutamate spillover activates Group II and III presynaptic metabotropic glutamate receptors (mGluRs) on the baroreceptor central terminals to inhibit synaptic transmission, but the role of postsynaptic mGluRs is less understood. We used whole cell patch-clamping in anatomically identified second-order baroreceptor neurons in a brain stem slice to test whether Group I, II, and III mGluRs had postsynaptic effects at this first central synapse in the baroreceptor afferent pathway. The Group I agonist DHPG induced a depolarization and spiking that was mimicked by endogenous glutamate. Group I mGluR blockade prevented the depolarization and slightly hyperpolarized the neurons, suggesting a small tonic Group I mGluR activation. The DHPG-induced inward current consisted of voltage-dependent and -independent components; the former was blocked by TEA and the latter was blocked by replacing extracellular NaCl with LiCl or Tris-HCl. The DHPG current was potentiated in a Ca²⁺-free external solution and was diminished by intracellular dialysis with BAPTA and by perfusion with Na⁺–Ca²⁺ exchanger blockers, KB-R7943 or 3',4'-dichlorobenzamil. Intracellular dialysis with GDPS or heparin and perfusion with the PLC inhibitor U-73122 or the Ca²⁺-calmodulin inhibitor W-7 significantly decreased the DHPG current. The data suggest that Group I mGluRs on baroreceptor neurons are functional; are activated by endogenous glutamate; and activate a Na⁺–Ca²⁺ exchanger through G-protein, PLC, IP₃, and Ca²⁺-calmodulin mechanisms to excite the cell, thus providing postsynaptic mechanisms to enhance or prolong baroreceptor signal transmission.

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