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Delta Opioid Receptors Regulate Temporoammonic-Activated Feedforward Inhibition to the Mouse CA1 Hippocampus

The opioid system influences learning and memory processes. However, neural mechanisms underlying the modulation of hippocampal activity by opioid receptors remain largely unknown. Here, we compared how mu and delta receptors operate within the mouse CA1 network, and used knock-in mice expressing fu...

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Autores principales: Rezai, Xavier, Kieffer, Brigitte L., Roux, Michel J., Massotte, Dominique
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2013
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3829835/
https://www.ncbi.nlm.nih.gov/pubmed/24260157
http://dx.doi.org/10.1371/journal.pone.0079081
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author Rezai, Xavier
Kieffer, Brigitte L.
Roux, Michel J.
Massotte, Dominique
author_facet Rezai, Xavier
Kieffer, Brigitte L.
Roux, Michel J.
Massotte, Dominique
author_sort Rezai, Xavier
collection PubMed
description The opioid system influences learning and memory processes. However, neural mechanisms underlying the modulation of hippocampal activity by opioid receptors remain largely unknown. Here, we compared how mu and delta receptors operate within the mouse CA1 network, and used knock-in mice expressing functional delta opioid receptors fused to the green fluorescent protein (DOR-eGFP) to determine how delta opioid receptor-expressing interneurons integrate within the hippocampal circuitry. Through whole cell patch-clamp recording of CA1 pyramidal neurons from wild-type and DOR-eGFP mice, we found that mu and delta receptors both modulate spontaneous GABAergic inhibition received by these cells. Interestingly, mu but not delta receptor activation decreased the feed-forward inhibitory input evoked by Schaffer collateral stimulation. However, mu and delta agonists modulated GABAergic feed-forward inhibition when evoked upon stimulation of the temporoammonic pathway. In addition, anterograde tracing using biotinylated dextran amine injected into the entorhinal cortex of DOR-eGFP mice suggests the existence of synaptic contacts between temporoammonic afferents and delta receptor-expressing interneurons processes in CA1. Altogether, our data demonstrate a distinct modulatory role of the hippocampal network activity by mu and delta opioid receptors, and show for the first time that delta receptor-expressing interneurons in the CA1 are recruited by the temporoammonic pathway rather than the Schaffer collateral.
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spelling pubmed-38298352013-11-20 Delta Opioid Receptors Regulate Temporoammonic-Activated Feedforward Inhibition to the Mouse CA1 Hippocampus Rezai, Xavier Kieffer, Brigitte L. Roux, Michel J. Massotte, Dominique PLoS One Research Article The opioid system influences learning and memory processes. However, neural mechanisms underlying the modulation of hippocampal activity by opioid receptors remain largely unknown. Here, we compared how mu and delta receptors operate within the mouse CA1 network, and used knock-in mice expressing functional delta opioid receptors fused to the green fluorescent protein (DOR-eGFP) to determine how delta opioid receptor-expressing interneurons integrate within the hippocampal circuitry. Through whole cell patch-clamp recording of CA1 pyramidal neurons from wild-type and DOR-eGFP mice, we found that mu and delta receptors both modulate spontaneous GABAergic inhibition received by these cells. Interestingly, mu but not delta receptor activation decreased the feed-forward inhibitory input evoked by Schaffer collateral stimulation. However, mu and delta agonists modulated GABAergic feed-forward inhibition when evoked upon stimulation of the temporoammonic pathway. In addition, anterograde tracing using biotinylated dextran amine injected into the entorhinal cortex of DOR-eGFP mice suggests the existence of synaptic contacts between temporoammonic afferents and delta receptor-expressing interneurons processes in CA1. Altogether, our data demonstrate a distinct modulatory role of the hippocampal network activity by mu and delta opioid receptors, and show for the first time that delta receptor-expressing interneurons in the CA1 are recruited by the temporoammonic pathway rather than the Schaffer collateral. Public Library of Science 2013-11-15 /pmc/articles/PMC3829835/ /pubmed/24260157 http://dx.doi.org/10.1371/journal.pone.0079081 Text en © 2013 Rezai et al http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Rezai, Xavier
Kieffer, Brigitte L.
Roux, Michel J.
Massotte, Dominique
Delta Opioid Receptors Regulate Temporoammonic-Activated Feedforward Inhibition to the Mouse CA1 Hippocampus
title Delta Opioid Receptors Regulate Temporoammonic-Activated Feedforward Inhibition to the Mouse CA1 Hippocampus
title_full Delta Opioid Receptors Regulate Temporoammonic-Activated Feedforward Inhibition to the Mouse CA1 Hippocampus
title_fullStr Delta Opioid Receptors Regulate Temporoammonic-Activated Feedforward Inhibition to the Mouse CA1 Hippocampus
title_full_unstemmed Delta Opioid Receptors Regulate Temporoammonic-Activated Feedforward Inhibition to the Mouse CA1 Hippocampus
title_short Delta Opioid Receptors Regulate Temporoammonic-Activated Feedforward Inhibition to the Mouse CA1 Hippocampus
title_sort delta opioid receptors regulate temporoammonic-activated feedforward inhibition to the mouse ca1 hippocampus
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3829835/
https://www.ncbi.nlm.nih.gov/pubmed/24260157
http://dx.doi.org/10.1371/journal.pone.0079081
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