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The Journal of Neuroscience, January 1, 2003, 23(1):122-130

Distinct Functional Roles of the Metabotropic Glutamate Receptors 1 and 5 in the Rat Globus Pallidus

Olga V. Poisik¹, Guido Mannaioni², Stephen Traynelis², Yoland Smith^{1, 3}, and P. Jeffrey Conn⁴

¹ Yerkes National Primate Research Center, Departments of ² Pharmacology and ³ Neurology, Emory University, Atlanta, Georgia 30322, and ⁴ Department of Neuroscience, Merck Research Laboratories, West Point, Pennsylvania 19486

Group I metabotropic glutamate receptors (mGluRs) 1 and 5 frequently colocalize in the same neurons throughout the CNS. Because both receptors can couple to the same effector systems, the purpose of their cellular coexpression remains unclear. Here, we report that group I mGluR1 and mGluR5 have distinct functional roles in type II neurons of the rat globus pallidus (GP). Type II GP neurons form a large population of GABAergic projection neurons that are characterized by the presence of inwardly rectifying current I_h, low-threshold voltage-activated calcium current I_t, and activity at rest. Although immunocytochemical analysis reveals a high degree of neuronal colocalization of the two group I mGluRs in the GP, activation of mGluR1 only directly depolarizes type II GP neurons. Interestingly, blockade of mGluR5 by a highly selective antagonist, methylphenylethynylpyridine, leads to the potentiation of the mGluR1-mediated depolarization in this neuronal subpopulation. Metabotropic GluR1 desensitizes during repeated activation with the agonist in type II GP neurons, and blocking mGluR5 prevents the desensitization of the mGluR1-mediated depolarization. Elimination of the activity of protein kinase C (PKC) by an application of 1 µM bisendolylmaleimide or 1 µM chelerythrine, both protein kinase C inhibitors, potentiates the mGluR1-mediated response and prevents the desensitization of mGluR1 in type II GP neurons, suggesting that the effect of mGluR5 on mGluR1 signaling may involve PKC. Together, these data illustrate a novel mechanism by which mGluR1 and mGluR5, members of the same family of G-protein-coupled receptors, can interact to modulate neuronal activity in the rat GP.

Key words: globus pallidus; group I metabotropic glutamate receptors; mGluR1; mGluR5; desensitization; protein kinase C; basal ganglia

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Copyright © 2003 Society for Neuroscience  0270-6474/03/231122-09$05.00/0

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