Oxytocin and vasopressin enhance synaptic transmission in the hypoglossal motor nucleus of young rats by acting on distinct receptor types

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Title: Oxytocin and vasopressin enhance synaptic transmission in the hypoglossal motor nucleus of young rats by acting on distinct receptor types
Authors: Wrobel, L. J., Reymond-Marron, I., Dupre, A., Raggenbass, Mario
Source: Neuroscience, Vol. 165, No 3 (2010) pp. 723-735
Publisher Information: Elsevier BV, 2010.
Publication Year: 2010
Subject Terms: 0301 basic medicine, Glycine/metabolism, Aging, Receptors, Vasopressin, 616.8, Gamma-Aminobutyric Acid/metabolism, Inhibitory Postsynaptic Potentials/physiology, Excitatory Postsynaptic Potentials/physiology, Glycine, Medulla Oblongata/ physiology, In Vitro Techniques, Vasopressins/ metabolism, Oxytocin, Synaptic Transmission, Rats, Sprague-Dawley, 03 medical and health sciences, Interneurons, Animals, Oxytocin/ metabolism, Dendrites/physiology, Neurons, Receptors, Vasopressin/ metabolism, Medulla Oblongata, 0303 health sciences, Cell Membrane, Excitatory Postsynaptic Potentials, Dendrites, Receptors, Oxytocin/ metabolism, Interneurons/physiology, Axons, ddc:616.8, Rats, Cell Membrane/physiology, Animals, Newborn, Inhibitory Postsynaptic Potentials, Synaptic Transmission/ physiology, Receptors, Oxytocin, Synapses, Axons/physiology, Neurons/physiology, Synapses/physiology
Description: Hypoglossal (XII) motoneurons innervate extrinsic and intrinsic muscles of the tongue and control behaviors such as suckling, swallowing, breathing or chewing. In young rats, XII motoneurons express V1a vasopressin and oxytocin receptors. Previous studies have shown that activation of these receptors induces direct powerful excitation in XII motoneurons. In addition, by activating V1a receptors vasopressin can also enhance inhibitory synaptic transmission in the XII nucleus. In the present work, we have further characterized the effect of these neuropeptides on synaptic transmission in the XII nucleus. We have used brainstem slices of young rats and whole-cell patch clamp recordings. Oxytocin enhanced the frequency of spontaneous inhibitory postsynaptic currents by a factor of two and a half. GABAergic and glycinergic events were both affected. The oxytocin effect was mediated by uterine-type oxytocin receptors. Vasopressin and oxytocin also increased the frequency of excitatory synaptic currents, the enhancement being sixfold for the former and twofold for the latter compound. These effects were mediated by V1a and oxytocin receptors, respectively. Miniature synaptic events were unaffected by either vasopressin or oxytocin. This indicates that the peptide-dependent facilitation of synaptic currents was mediated by receptors located on the somatodendritic membrane of interneurons or premotor neurons, and not by receptors sited on axon terminals contacting XII motoneurons. Accordingly, recordings obtained from non-motoneurons located near the border of the XII nucleus showed that part of these cells possess functional V1a and oxytocin receptors whose activation leads to excitation. Some of these neurons could be antidromically activated following electrical stimulation of the XII nucleus, suggesting that they may act as premotor neurons. We propose that in young rats, oxytocin and vasopressin may function as neuromodulators in brainstem motor circuits responsible of tongue movements.
Document Type: Article
File Description: application/pdf
Language: English
ISSN: 0306-4522
DOI: 10.1016/j.neuroscience.2009.11.001
Access URL: https://pubmed.ncbi.nlm.nih.gov/19896520
https://archive-ouverte.unige.ch/unige:10520
https://core.ac.uk/display/60786708
https://pubmed.ncbi.nlm.nih.gov/19896520/
https://www.sciencedirect.com/science/article/abs/pii/S0306452209017965
https://www.ncbi.nlm.nih.gov/pubmed/19896520
http://europepmc.org/abstract/MED/19896520
https://archive-ouverte.unige.ch/unige:10520
https://doi.org/10.1016/j.neuroscience.2009.11.001
https://archive-ouverte.unige.ch/unige:10520
Rights: Elsevier TDM
Accession Number: edsair.doi.dedup.....73e12d58c5f573b95f7ecba1876faf6c
Database: OpenAIRE
Description
Abstract:Hypoglossal (XII) motoneurons innervate extrinsic and intrinsic muscles of the tongue and control behaviors such as suckling, swallowing, breathing or chewing. In young rats, XII motoneurons express V1a vasopressin and oxytocin receptors. Previous studies have shown that activation of these receptors induces direct powerful excitation in XII motoneurons. In addition, by activating V1a receptors vasopressin can also enhance inhibitory synaptic transmission in the XII nucleus. In the present work, we have further characterized the effect of these neuropeptides on synaptic transmission in the XII nucleus. We have used brainstem slices of young rats and whole-cell patch clamp recordings. Oxytocin enhanced the frequency of spontaneous inhibitory postsynaptic currents by a factor of two and a half. GABAergic and glycinergic events were both affected. The oxytocin effect was mediated by uterine-type oxytocin receptors. Vasopressin and oxytocin also increased the frequency of excitatory synaptic currents, the enhancement being sixfold for the former and twofold for the latter compound. These effects were mediated by V1a and oxytocin receptors, respectively. Miniature synaptic events were unaffected by either vasopressin or oxytocin. This indicates that the peptide-dependent facilitation of synaptic currents was mediated by receptors located on the somatodendritic membrane of interneurons or premotor neurons, and not by receptors sited on axon terminals contacting XII motoneurons. Accordingly, recordings obtained from non-motoneurons located near the border of the XII nucleus showed that part of these cells possess functional V1a and oxytocin receptors whose activation leads to excitation. Some of these neurons could be antidromically activated following electrical stimulation of the XII nucleus, suggesting that they may act as premotor neurons. We propose that in young rats, oxytocin and vasopressin may function as neuromodulators in brainstem motor circuits responsible of tongue movements.
ISSN:03064522
DOI:10.1016/j.neuroscience.2009.11.001