Opioid peptides inhibit excitatory but not inhibitory synaptic transmission in the rat dorsal motor nucleus of the vagus

Kirsteen N. Browning, Alexander E. Kalyuzhny, R. Alberto Travagli

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60 Scopus citations

Abstract

Opioid peptides produce gastrointestinal inhibition and increase feeding when applied to the brainstem. The present studies were designed to determine the actions of opioid peptides on synaptic transmission within the dorsal motor nucleus of the vagus (DMV) and the localization of μ-opioid receptors. Whole-cell recordings were made from identified gastrointestinal-projecting DMV neurons in thin brainstem slices of the rat. Electrical stimulation of the nucleus of the tractus solitarius evoked EPSCs and IPSCs. In all neurons tested, methionine (Met)-enkephalin (0.003-30 μM) inhibited the peak amplitude of the EPSCs. The effect was prevented by naloxone (1 μM) as well as by naloxonazine (0.2 μM). An increase in the ratio of the evoked paired pulses indicated that the inhibition was attributable to actions at presynaptic receptors. This presynaptic inhibitory action was mimicked by [D-Ala2, N-Me-Phe4, Gly5-ol]-enkephalin (0.1 μM) and the analgesic dipeptide kyotorphin (10 μM) but not by cyclic[D- Pen2, D-Pen5]-enkephalin (1 μM) and trans-3,4-dichloro-N- methyl-N-[2-(1-pyrrolidinyl)-cyclohexyl]benzeneacetamide methanesulfonate (1 μM). In contrast, the amplitude of evoked IPSCs was not altered either by Met-enkephalin or by any of the opioid receptor-selective agonists. Immunohistochemical studies revealed that nerve terminals apposing DMV neurons showed immunoreactivity to μ-opioid receptors colocalized with glutamate immunoreactivity but not glutamic acid decarboxylase immunoreactivity. These results suggest that within the DMV, μ-opioid receptors are present on the nerve terminals of excitatory but not inhibitory inputs to Gl motoneurons. Such specificity may imply that the central inhibitory action of opioid peptides on gastrointestinal function targets selected pathways.

Original languageEnglish (US)
Pages (from-to)2998-3004
Number of pages7
JournalJournal of Neuroscience
Volume22
Issue number8
DOIs
StatePublished - Apr 15 2002

All Science Journal Classification (ASJC) codes

  • General Neuroscience

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