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The Journal of Neuroscience, June 15, 1999, 19(12):4796-4803

Presynaptic µ and  Opioid Receptor Modulation of GABA_A IPSCs in the Rat Globus Pallidus In Vitro

Ian M. Stanford and Alison J. Cooper

The Department of Pharmacology, The Division of Neuroscience, The Medical School, The University of Birmingham, Edgbaston, Birmingham B15 2TT, United Kingdom

The role of enkephalin and the opioid receptors in modulating GABA release within the rat globus pallidus (GP) was investigated using whole-cell patch recordings made from visually identified neurons. Two major GP neuronal subtypes were classified on the basis of intrinsic membrane properties, action potential characteristics, the presence of the anomalous inward rectifier (I_h), and anode break depolarizations.

The µ opioid receptor agonist [D-Ala²-N-Me-Phe⁴-Glycol⁵]-enkephalin (DAMGO) (1 µM) reduced GABA_A receptor-mediated IPSCs evoked by stimulation within the striatum. DAMGO also increased paired-pulse facilitation, indicative of presynaptic µ opioid receptor modulation of striatopallidal input. In contrast, the  opioid agonist D-Pen-[D-Pen^2,5]-enkephalin (DPDPE) (1 µM) was without effect.

IPSCs evoked by stimulation within the GP were depressed by application of [methionine 5']-enkephalin (met-enkephalin) (30 µM). Met-enkephalin also reduced the frequency, but not the amplitude, of miniature IPSCs (mIPSCs) and increased paired-pulse facilitation of evoked IPSCs, indicative of a presynaptic action. Both DAMGO and DPDPE reduced evoked IPSCs and the frequency, but not amplitude, of mIPSCs. However, spontaneous action potential-driven IPSCs were reduced in frequency by met-enkephalin and DAMGO, whereas DPDPE was without effect.

Overall, these results indicate that presynaptic µ opioid receptors are located on striatopallidal terminals and pallidopallidal terminals of spontaneously firing GP neurons, whereas presynaptic  opioid receptors are preferentially located on terminals of quiescent GP cells. Enkephalin, acting at both of these receptor subtypes, serves to reduce GABA release in the GP and may therefore act as an adaptive mechanism, maintaining the inhibitory function of the GP in basal ganglia circuitry.

Key words: whole-cell patch clamp; brain slices; basal ganglia; enkephalin; GABA_A IPSC; opioid receptors

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Copyright © 1999 Society for Neuroscience  0270-6474/99/19124796-08$05.00/0

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