Received for publication July 20, 2004.
Revised September 21, 2004.
Accepted for publication September 22, 2004.

Effect of the µ Opioid on Excitatory and Inhibitory Synaptic Inputs to Periaqueductal Gray-Projecting Neurons in the Amygdala

Abstract

Opioids are potent analgesics but the sites of their action and cellular mechanisms are not fully understood. The central nucleus of the amygdala (CeA) is important for opioid analgesia through the projection to the periaquaductal gray (PAG). In this study, we examined the effects of µopioid receptor stimulation on inhibitory and excitatory synaptic inputs to PAG-projecting CeA neurons retrogradely labeled with a fluorescent tracer injected into the ventrolateral PAG of rats. Whole-cell voltage-clamp recordings were performed on labeled CeA neurons in brain slices. The specific m opioid receptor agonist, [D-Ala²,N-Me-Phe⁴,Gly⁵-ol]-enkephalin (DAMGO, 1 µM), significantly reduced the frequency of mIPSCs without altering the amplitude and decay constant of mIPSCs in 47.6% (10 of 21) of cells tested. DAMGO also significantly decreased the peak amplitude of evoked IPSCs in 69% (9 of 13) of cells examined. However, DAMGO did not significantly alter the frequency of mEPSCs and the amplitude of eEPSCs in 69% (9 of 13) and 83% (10 of 12) of labeled cells, respectively. The IPSCs were blocked by the GABA_A receptor antagonist bicuculline, while the EPSCs were largely abolished by the non-NMDA antagonist CNQX. Immunofluorescent labeling revealed that the immunoreactivity of m opioid receptors was co-localized with synaptophysin, a presynaptic marker, in close appositions to labeled CeA neurons. These results suggest that activation of µ opioid receptors on presynaptic terminals primarily attenuates GABAergic synaptic inputs to PAG-projecting neurons in the CeA.

Key words: analgesia, brainstem, descending modulation, opioids, pain, synaptic transmission

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