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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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