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Vol. 288, Issue 1, 30-35, January 1999

Chronic Morphine Treatment Selectively Augments Metabotropic Glutamate Receptor-Induced Inhibition of N-Methyl-D-Aspartate Receptor-Mediated Neurotransmission in Nucleus Accumbens1

Gilles Martin, Riszard Przewlocki and George R. Siggins

The Scripps Research Institute, Department of Neuropharmacology, La Jolla, California (G.M and G.R.S); and Neuropeptide Research Department, Institute of Pharmacology, Polish Academy of Sciences, Krakow, Poland (R.P.)

We compared the effects of different metabotropic glutamate receptor (mGluR) agonists on pharmacologically isolated N-methyl-D-aspartate-excitatory postsynaptic currents (NMDA-EPSCs) in core nucleus accumbens neurons using conventional intracellular recording in untreated and morphine-treated rats. The rats were treated by s.c. implantation of two morphine pellets and studied over a 3- to 6-day period. This model is known to exhibit opiate tolerance and dependence. We elicited NMDA-EPSCs by stimulating locally in the presence of the alpha -amino-3-hydroxy-5-methly-4-isoxazolepropionic acid/kainate receptor antagonist 6-cyano-7-nitroquinoxaline-2,3-dione (10 µM) and the gamma -aminobutyric acid receptor antagonist bicuculline (15 µM). We found that trans-1-aminocyclopentane-1,3-decarboxylic acid, an agonist of group 1 and 2 mGluRs, decreased NMDA-EPSC areas (time-integrals) in a dose-dependent manner (1-10 µM) in slices taken from untreated rats. This inhibitory effect was significantly enhanced after chronic morphine treatment. In contrast, although the group 3 mGluR agonist L(+)-2-amino-4-phosphonobutyric acid also markedly reduced NMDA-EPSC areas, there was no apparent change in this effect after chronic morphine. We found that quisqualate, the group 1 mGluR agonist, failed to elicit any effect on NMDA-EPSCs in either untreated or chronically treated rats. Paired-pulse stimulation of core nucleus accumbens NMDA-EPSCs in slices from these groups showed that chronic morphine enhanced paired-pulse facilitation, consistent with a presynaptic reduction in glutamate release. Because of the relevance to opiate tolerance and dependence of the chronic model used, the brain region (accumbens), and the receptors studied, our data provide a cellular substrate that could account for some aspects of these phenomena.

0022-3565/99/2881-0030$03.00/0
THE JOURNAL OF PHARMACOLOGY AND EXPERIMENTAL THERAPEUTICS
Copyright © 1999 by The American Society for Pharmacology and Experimental Therapeutics


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