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The Journal of Neuroscience, April 15, 2002, 22(8):2998-3004
Opioid Peptides Inhibit Excitatory But Not Inhibitory Synaptic Transmission in the Rat Dorsal Motor Nucleus of the Vagus
Kirsteen N. Browning1, Alexander E. Kalyuzhny2, and R. Alberto Travagli1 1 Division of Gastroenterology and Department of Physiology, University of Michigan Medical Center, Ann Arbor, Michigan 48109-0682, and 2 Department of Neuroscience, University of Minnesota, Minneapolis, Minnesota 55455
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 GI motoneurons. Such specificity may imply that the central inhibitory action of opioid peptides on gastrointestinal function targets selected pathways.
Key words: dorsal motor nucleus of the vagus; opioids; dorsal vagal complex; gastrointestinal function; immunoreactivity; feeding
Copyright © 2002 Society for Neuroscience 0270-6474/02/2282998-07$05.00/0
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