Endocannabinoids in Amygdala and Nucleus Accumbens Mediate Social Play Reward in Adolescent Rats
Open accessAbstract
The brain endocannabinoid system plays a crucial role in emotional processes. We have previously identified an important role for endocannabinoids in social play behavior, a highly rewarding form of social interaction in adolescent rats. Here, we tested the hypothesis that endocannabinoid modulation of social play behavior occurs in brain regions implicated in emotion and motivation. Social play increased levels of the endocannabinoid anandamide in the amygdala and nucleus accumbens (NAc), but not in prefrontal cortex or hippocampus of 4- to 5-week-old male Wistar rats. Furthermore, social play increased phosphorylation of CB1 cannabinoid receptors in the amygdala. Systemic administration of the anandamide hydrolysis inhibitor URB597 increased social play behavior, and augmented the associated elevation in anandamide levels in the amygdala, but not the NAc. Infusion of URB597 into the basolateral amygdala (BLA) increased social play behavior, and blockade of BLA CB1 cannabinoid receptors with the antagonist/inverse agonist SR141716A prevented the play-enhancing effects of systemic administration of URB597. Infusion of URB597 into the NAc also increased social play, but blockade of NAc CB1 cannabinoid receptors did not antagonize the play-enhancing effects of systemic URB597 treatment. Last, SR141716A did not affect social play after infusion into the core and shell subregions of the NAc, while it reduced social play when infused into the BLA. These data show that increased anandamide signaling in the amygdala and NAc augments social play, and identify the BLA as a prominent site of action for endocannabinoids to modulate the rewarding properties of social interactions in adolescent rats.
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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 [24]
The Results (page not provided) report that URB597 infused into either the BLA or NAc increased pinning and pouncing, measures of play fighting. CB1 antagonist infusion into the BLA blocked the play-enhancing effect of systemic URB597, but antagonist infusion into the NAc did not. The source therefore supports the CB1 mechanism in the BLA, not the claim that it was established in both regions. (LLM, conf=0.88)
Experimental — accuracy not yet measuredThe amygdala contributes to processing the rewarding aspects of play.
“The amygdala, in addition to regulating the sex difference in play, contributes to processing the rewarding aspects of play (Trezza et al., 2012).”
From Developmental origins of sex differences in the neural circuitry of play (2020) · cites this paper as Trezza et al., 2012
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.”
Pharmacological FAAH inhibition promotes social play in juvenile rats.
“Trezza et al. noted that pharmacological FAAH inhibition promotes social play in juvenile rats.14”
From Enhancement of anandamide-mediated endocannabinoid signaling corrects autism-related social impairment (2016) · cites this paper as [14]
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VanRyzin, J. W., Marquardt, A. E., & McCarthy, M. M. (2020) · International Journal of Play · doi:10.1080/21594937.2020.1723370 · Cited by 34 · see citing works
“The amygdala, in addition to regulating the sex difference in play, contributes to processing the rewarding aspects of play (Trezza et al., 2012).”
BackgroundCutuli, D., Berretta, E., Caporali, P., Sampedro-Piquero, P., De Bartolo, P., Laricchiuta, D., Gelfo, F., Pesoli, M., Foti, F., Farioli Vecchioli, S., et al. (2019) · Neuropharmacology · doi:10.1016/j.neuropharm.2018.02.015 · Cited by 30 · see citing works
p21-activated kinase 1 restricts tonic endocannabinoid signaling in the hippocampus
Xia, S., Zhou, Z., Leung, C., Zhu, Y., Pan, X., Qi, J., Morena, M., Hill, M. N., Xie, W., & Jia, Z. (2016) · eLife · doi:10.7554/elife.14653 · Cited by 21 · see citing works
The endocannabinoid system in social anxiety disorder: from pathophysiology to novel therapeutics
Ahmed, M., Boileau, I., Le Foll, B., Carvalho, A. F., & Kloiber, S. (2022) · Brazilian Journal of Psychiatry · doi:10.1590/1516-4446-2021-1926 · Cited by 11 · see citing works
- Authors
- Trezza, V., Damsteegt, R., Manduca, A., Petrosino, S., Van Kerkhof, L. W. M., Pasterkamp, R. J., Zhou, Y., Campolongo, P., Cuomo, V., Di Marzo, V., & Vanderschuren, L. J. M. J.
- Affiliations
- Roma Tre University (IT)
- University Medical Center Utrecht (NL)
- National Research Council (IT)
- Sapienza University of Rome (IT)
- Utrecht University (NL)
- ORCID
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2012-10-24
- Volume
- 32
- Issue
- 43
- Pages
- 14899-14908
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC3496852
- OpenAlex
- W2057821563
- Cited by
- 190
- References
- 77
- Citations by year
- 2026: 8 · 2025: 16 · 2024: 8 · 2023: 12 · 2022: 14 · 2021: 8 · 2020: 17 · 2019: 14 · 2018: 19 · 2017: 15 · 2016: 31 · 2015: 8 · 2014: 8 · 2013: 12
- FWCI
- 6.57
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- IRIS Research product catalog (Sapienza University of Rome) (submittedVersion)
- Utrecht University Repository (Utrecht University) (submittedVersion, other-oa)
- Iris (Roma Tre University) (submittedVersion)
- Funders
- European Commission (293589)
- Top Institute Pharma (T5-107)
- National Institute on Drug Abuse (R01DA022628, P01DA009789, DA022628, DA 009789)
- Topics
- Health Sciences › Medicine › Pharmacology › Cannabis and Cannabinoid Research
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Keywords
- endocannabinoid system, social play, anandamide, CB1 receptor, amygdala, nucleus accumbens, basolateral amygdala, adolescent rats, social reward, URB597, SR141716A
- MeSH terms
- Rimonabant, Fatty Acid Amide Hydrolases, Amidohydrolases, Amygdala, Analysis of Variance, Animals, Animals, Newborn, Benzamides, Carbamates, Dose-Response Relationship, Drug, Enzyme Inhibitors, Gene Expression Regulation, Interpersonal Relations, Male, Nucleus Accumbens, Phospholipase D, Phosphorylation, Piperidines, Play and Playthings, Pyrazoles, Reward, Rats, Wistar, Receptor, Cannabinoid, CB1, Rats, Cannabinoid Receptor Agonists, Endocannabinoids
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Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
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