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

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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
StatePublished - Apr 15 2002

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Opioid Peptides
Opioid Receptors
Synaptic Transmission
Methionine Enkephalin
Neurons
kyotorphin
Brain Stem
(trans)-Isomer 3,4-Dichloro-N-methyl-N-(2-(1-pyrrolidinyl)-cyclohexyl)-benzeneacetamide
D-Penicillamine (2,5)-Enkephalin
Presynaptic Receptors
Solitary Nucleus
Glutamate Decarboxylase
Dipeptides
Enkephalins
Motor Neurons
Patch-Clamp Techniques
Naloxone
Electric Stimulation
Analgesics
Glutamic Acid

All Science Journal Classification (ASJC) codes

  • Neuroscience(all)

Cite this

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title = "Opioid peptides inhibit excitatory but not inhibitory synaptic transmission in the rat dorsal motor nucleus of the vagus",
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.",
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Opioid peptides inhibit excitatory but not inhibitory synaptic transmission in the rat dorsal motor nucleus of the vagus. / Browning, Kirsteen; Kalyuzhny, Alexander E.; Travagli, Renato Alberto.

In: Journal of Neuroscience, Vol. 22, No. 8, 15.04.2002, p. 2998-3004.

Research output: Contribution to journalArticle

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AB - 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.

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