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Cited by 73Cannabis and Cannabinoid ResearchNeurotransmitter Receptor Influence on BehaviorNeuropeptides and Animal Physiology

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

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Manduca, Antonia, Lassalle, Olivier, Sepers, Marja, Campolongo, Patrizia, Cuomo, Vincenzo, Marsicano, Giovanni, Kieffer, Brigitte, Vanderschuren, Louk J. M. J +2 more·2016·Frontiers in Behavioral Neuroscience
DOI 10.3389/fnbeh.2016.00211PMC PMC5110529
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Abstract

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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  • Systemic injection of an endocannabinoid agonist increases play fighting through actions on the CB1 receptor, and the nucleus accumbens and basolateral amygdala are implicated in these effects.

    “Systemic injection of an endocannabinoid agonist was shown to increase play fighting though actions on the CB1 receptor, and the nucleus accumbens (NAc) and basolateral amygdala (BLA) have been implicated in these effects23,24.”

    From Peripubertal stress increases play fighting at adolescence and modulates nucleus accumbens CB1 receptor expression and mitochondrial function in the amygdala (2018) · cites this paper as [23]

    The Results report that systemic JZL184 increased pinning and pouncing in adolescent rats, and that a CB1 receptor antagonist blocked the effect. The Introduction implicates both the nucleus accumbens and basolateral amygdala in endocannabinoid-related social play. But JZL184 is a 2-AG hydrolysis inhibitor, not an injected endocannabinoid agonist. (LLM, conf=0.87)

    Experimental — accuracy not yet measured

  • Intra-BLA and intra-NAc infusions of an endocannabinoid agonist increase play fighting through actions on the CB1 receptor.

    “Given that both, intra-BLA and intra-NAc infusions of an endocannabinoid agonist increase play fighting23,24 through actions on the CB1 receptor23,24,53, we assessed CB1 mRNA levels in these brain regions.”

    From Peripubertal stress increases play fighting at adolescence and modulates nucleus accumbens CB1 receptor expression and mitochondrial function in the amygdala (2018) · cites this paper as [23]

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Authors
Manduca, A., Lassalle, O., Sepers, M., Campolongo, P., Cuomo, V., Marsicano, G., Kieffer, B., Vanderschuren, L. J. M. J., Trezza, V., & Manzoni, O. J. J.
Affiliations
  • Inserm (FR)
  • Sapienza University of Rome (IT)
  • Université de Bordeaux (FR)
  • Centre National de la Recherche Scientifique (FR)
  • Utrecht University (NL)
  • Roma Tre University (IT)
Corresponding author
  • Trezza, Viviana
  • Manzoni, Olivier J. J.
ORCID
Venue
Frontiers in Behavioral Neuroscience
Publisher
Frontiers Media SA
Published
2016-11-16
Volume
10
Pages
211-211
ISSN
1662-5153 (ISSN-L)
DOI
10.3389/fnbeh.2016.00211
PMC
PMC5110529
OpenAlex
W2554580891
Cited by
73
References
84
Citations by year
2026: 1 · 2025: 6 · 2024: 4 · 2023: 6 · 2022: 9 · 2021: 7 · 2020: 13 · 2019: 11 · 2018: 10 · 2017: 6
FWCI
7.28
Type
journal article
Language
en
Open access
Licence
cc-by
Locations
  • Frontiers in Behavioral Neuroscience (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • IRIS Research product catalog (Sapienza University of Rome) (submittedVersion, cc-by)
  • Iris (Roma Tre University) (submittedVersion, cc-by)
  • HAL (submittedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Utrecht University Repository (Utrecht University) (submittedVersion, other-oa)
Funders
  • Institut National de la Santé et de la Recherche Médicale
  • Institut National de la Recherche Agronomique
  • Association Nationale de la Recherche et de la Technologie (Presynaptic-CB1R)
  • National Institute on Drug Abuse
Topics
  • Health Sciences › Medicine › Pharmacology › Cannabis and Cannabinoid Research
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuropeptides and Animal Physiology
Keywords
social play, endocannabinoid system, opioid system, CB1 receptor, mu-opioid receptor, nucleus accumbens core, 2-arachidonoylglycerol, JZL184, morphine, naloxone, DAMGO, adolescent rats, synaptic transmission, opioid-cannabinoid interaction, social behavior

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