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Interacting Cannabinoid and Opioid Receptors in the Nucleus Accumbens Core Control Adolescent Social Play

Social play behavior is a highly rewarding, developmentally important form of social interaction in young mammals. However, its neurobiological underpinnings remain incompletely understood. Previous work has suggested that opioid and endocannabinoid neurotransmission interact in the modulation of so...

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Autores principales: Manduca, Antonia, Lassalle, Olivier, Sepers, Marja, Campolongo, Patrizia, Cuomo, Vincenzo, Marsicano, Giovanni, Kieffer, Brigitte, Vanderschuren, Louk J. M. J, Trezza, Viviana, Manzoni, Olivier J. J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5110529/
https://www.ncbi.nlm.nih.gov/pubmed/27899885
http://dx.doi.org/10.3389/fnbeh.2016.00211
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author Manduca, Antonia
Lassalle, Olivier
Sepers, Marja
Campolongo, Patrizia
Cuomo, Vincenzo
Marsicano, Giovanni
Kieffer, Brigitte
Vanderschuren, Louk J. M. J
Trezza, Viviana
Manzoni, Olivier J. J.
author_facet Manduca, Antonia
Lassalle, Olivier
Sepers, Marja
Campolongo, Patrizia
Cuomo, Vincenzo
Marsicano, Giovanni
Kieffer, Brigitte
Vanderschuren, Louk J. M. J
Trezza, Viviana
Manzoni, Olivier J. J.
author_sort Manduca, Antonia
collection PubMed
description Social play behavior is a highly rewarding, developmentally important form of social interaction in young mammals. However, its neurobiological underpinnings remain incompletely understood. Previous work has suggested that opioid and endocannabinoid neurotransmission interact in the modulation of social play. Therefore, we combined behavioral, pharmacological, electrophysiological, and genetic approaches to elucidate the role of the endocannabinoid 2-arachidonoylglycerol (2-AG) in social play, and how cannabinoid and opioid neurotransmission interact to control social behavior in adolescent rodents. Systemic administration of the 2-AG hydrolysis inhibitor JZL184 or the opioid receptor agonist morphine increased social play behavior in adolescent rats. These effects were blocked by systemic pretreatment with either CB1 cannabinoid receptor (CB1R) or mu-opioid receptor (MOR) antagonists. The social play-enhancing effects of systemic morphine or JZL184 treatment were also prevented by direct infusion of the CB1R antagonist SR141716 and the MOR antagonist naloxone into the nucleus accumbens core (NAcC). Searching for synaptic correlates of these effects in adolescent NAcC excitatory synapses, we observed that CB1R antagonism blocked the effect of the MOR agonist DAMGO and, conversely, that naloxone reduced the effect of a cannabinoid agonist. These results were recapitulated in mice, and completely abolished in CB1R and MOR knockout mice, suggesting that the functional interaction between CB1R and MOR in the NAcC in the modulation of social behavior is widespread in rodents. The data shed new light on the mechanism by which endocannabinoid lipids and opioid peptides interact to orchestrate rodent socioemotional behaviors.
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spelling pubmed-51105292016-11-29 Interacting Cannabinoid and Opioid Receptors in the Nucleus Accumbens Core Control Adolescent Social Play Manduca, Antonia Lassalle, Olivier Sepers, Marja Campolongo, Patrizia Cuomo, Vincenzo Marsicano, Giovanni Kieffer, Brigitte Vanderschuren, Louk J. M. J Trezza, Viviana Manzoni, Olivier J. J. Front Behav Neurosci Neuroscience Social play behavior is a highly rewarding, developmentally important form of social interaction in young mammals. However, its neurobiological underpinnings remain incompletely understood. Previous work has suggested that opioid and endocannabinoid neurotransmission interact in the modulation of social play. Therefore, we combined behavioral, pharmacological, electrophysiological, and genetic approaches to elucidate the role of the endocannabinoid 2-arachidonoylglycerol (2-AG) in social play, and how cannabinoid and opioid neurotransmission interact to control social behavior in adolescent rodents. Systemic administration of the 2-AG hydrolysis inhibitor JZL184 or the opioid receptor agonist morphine increased social play behavior in adolescent rats. These effects were blocked by systemic pretreatment with either CB1 cannabinoid receptor (CB1R) or mu-opioid receptor (MOR) antagonists. The social play-enhancing effects of systemic morphine or JZL184 treatment were also prevented by direct infusion of the CB1R antagonist SR141716 and the MOR antagonist naloxone into the nucleus accumbens core (NAcC). Searching for synaptic correlates of these effects in adolescent NAcC excitatory synapses, we observed that CB1R antagonism blocked the effect of the MOR agonist DAMGO and, conversely, that naloxone reduced the effect of a cannabinoid agonist. These results were recapitulated in mice, and completely abolished in CB1R and MOR knockout mice, suggesting that the functional interaction between CB1R and MOR in the NAcC in the modulation of social behavior is widespread in rodents. The data shed new light on the mechanism by which endocannabinoid lipids and opioid peptides interact to orchestrate rodent socioemotional behaviors. Frontiers Media S.A. 2016-11-16 /pmc/articles/PMC5110529/ /pubmed/27899885 http://dx.doi.org/10.3389/fnbeh.2016.00211 Text en Copyright © 2016 Manduca, Lassalle, Sepers, Campolongo, Cuomo, Marsicano, Kieffer, Vanderschuren, Trezza and Manzoni. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Neuroscience
Manduca, Antonia
Lassalle, Olivier
Sepers, Marja
Campolongo, Patrizia
Cuomo, Vincenzo
Marsicano, Giovanni
Kieffer, Brigitte
Vanderschuren, Louk J. M. J
Trezza, Viviana
Manzoni, Olivier J. J.
Interacting Cannabinoid and Opioid Receptors in the Nucleus Accumbens Core Control Adolescent Social Play
title Interacting Cannabinoid and Opioid Receptors in the Nucleus Accumbens Core Control Adolescent Social Play
title_full Interacting Cannabinoid and Opioid Receptors in the Nucleus Accumbens Core Control Adolescent Social Play
title_fullStr Interacting Cannabinoid and Opioid Receptors in the Nucleus Accumbens Core Control Adolescent Social Play
title_full_unstemmed Interacting Cannabinoid and Opioid Receptors in the Nucleus Accumbens Core Control Adolescent Social Play
title_short Interacting Cannabinoid and Opioid Receptors in the Nucleus Accumbens Core Control Adolescent Social Play
title_sort interacting cannabinoid and opioid receptors in the nucleus accumbens core control adolescent social play
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5110529/
https://www.ncbi.nlm.nih.gov/pubmed/27899885
http://dx.doi.org/10.3389/fnbeh.2016.00211
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