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Cited by 163Neurotransmitter Receptor Influence on BehaviorNeuroendocrine regulation and behaviorNeural and Behavioral Psychology Studies

Social Play Behavior in Adolescent Rats is Mediated by Functional Activity in Medial Prefrontal Cortex and Striatum

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van Kerkhof, Linda WM, Damsteegt, Ruth, Trezza, Viviana, Voorn, Pieter, Vanderschuren, Louk JMJ·2013·Neuropsychopharmacology
DOI 10.1038/npp.2013.83PMC PMC3746695
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Abstract

Social play behavior is a characteristic, vigorous form of social interaction in young mammals. It is highly rewarding and thought to be of major importance for social and cognitive development. The neural substrates of social play are incompletely understood, but there is evidence to support a role for the prefrontal cortex (PFC) and striatum in this behavior. Using pharmacological inactivation methods, ie, infusions of GABA receptor agonists (baclofen and muscimol; B&M) or the AMPA/kainate receptor antagonist 6,7-dinitroquinoxaline-2,3(1H,4H)-dione (DNQX), we investigated the involvement of several subregions of the medial PFC and striatum in social play. Inactivation of the prelimbic cortex, infralimbic cortex, and medial/ventral orbitofrontal cortex using B&M markedly reduced frequency and duration of social play behavior. Local administration of DNQX into the dorsomedial striatum increased the frequency and duration of social play, whereas infusion of B&M tended to have the same effect. Inactivation of the nucleus accumbens (NAcc) core using B&M increased duration but not frequency of social play, whereas B&M infusion into the NAcc shell did not influence social play behavior. Thus, functional integrity of the medial PFC is important for the expression of social play behavior. Glutamatergic inputs into the dorsomedial striatum exert an inhibitory influence on social play, and functional activity in the NAcc core acts to limit the length of playful interactions. These results highlight the importance of prefrontal and striatal circuits implicated in cognitive control, decision making, behavioral inhibition, and reward-associated processes in social play behavior.

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Crossref · 10.1038/npp.2013.83

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  • Substantial evidence supports the involvement of both NAc shell and core in play fighting.

    “Substantial evidence supports the involvement of both NAc shell and core in play fighting.”

    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 [55]

    In 'Inactivation of the NAcc Core Enhances the Duration of Social Play Behavior,' the paper reports that core inactivation prolonged social play and that play was associated with increased activity in both the core and shell. But the same section says the shell experiments were confounded by feeding and that its involvement in social play remains difficult to establish. Thus, 'substantial evidence' for involvement of both regions overstates the evidence for the shell. (LLM, conf=0.86)

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  • Only pharmacological inactivation of the NAc core, but not shell, interfered with social play behavior.

    “A pronounced increase in c-Fos expression has been observed in both the NAc core and shell following play fighting in rats54; however, only pharmacological inactivation of the NAc core, but not shell, interfered with social play behavior55.”

    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 [55]

    In “Pharmacological Inactivation of Striatal Regions,” NAcc core inactivation increased total play time, while a lower, non-disruptive dose in the shell had no measured effect. The categorical “but not shell” overstates the comparison: the dose used in the core completely blocked play when given in the shell, although the authors attribute that blockade to intense eating rather than a direct effect on social play. (LLM, conf=0.83)

    Experimental — accuracy not yet measured

  • The medial prefrontal cortex has a crucial role in coordinating actions with partners as juveniles and as adults in both playful and non-playful social interactions.

    “and the mPFC has a crucial role in coordinating actions with partners as juveniles and as adults in both playful and non-playful social interactions (Bell et al., 2009; Van Kerkhof et al., 2013; Himmler et al., 2014; Stark and Pellis, 2020).”

    From The rough-and-tumble play of rats as a natural behavior suitable for studying the social brain (2022) · cites this paper as Van Kerkhof et al., 2013

    The Concluding Remarks say that medial PFC activity helps adolescent rats initiate play and respond appropriately to a partner’s play initiation. The paper’s discussion of non-playful social exploration does not establish a role in coordinating those interactions, and its mention of adult sexual behavior concerns neuronal activity rather than coordinated actions. The claim therefore extends beyond the paper’s findings. (LLM, conf=0.87)

    Experimental — accuracy not yet measured

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Research works printed but not linked: 2

  1. Paxinos G, Watson C (2007). The rat brain in sterotaxic coordinates. Academic Press: London.
  2. Pellis SM, Pellis VC (2009). The Playful Brain. OneWorld Publications: Oxford, UK.

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Authors
van Kerkhof, L. W., Damsteegt, R., Trezza, V., Voorn, P., & Vanderschuren, L. J.
Affiliations
  • University Medical Center Utrecht (NL)
  • Roma Tre University (IT)
  • Amsterdam Neuroscience (NL)
  • Utrecht University (NL)
Corresponding author
Vanderschuren, Louk JMJ
ORCID
Venue
Neuropsychopharmacology
Publisher
Springer Science and Business Media LLC
Published
2013-04-08
Volume
38
Issue
10
Pages
1899-1909
ISSN
  • 0893-133X (ISSN-L)
  • 1740-634X
DOI
10.1038/npp.2013.83
PMC
PMC3746695
OpenAlex
W2015184348
Cited by
161
References
71
Citations by year
2026: 8 · 2025: 8 · 2024: 13 · 2023: 15 · 2022: 11 · 2021: 17 · 2020: 10 · 2019: 13 · 2018: 18 · 2017: 10 · 2016: 18 · 2015: 8 · 2014: 7 · 2013: 5
FWCI
5.12
Type
journal article
Language
en
Open access
Licence
www.springer.com/tdm (tdm)
Locations
  • Neuropsychopharmacology (publishedVersion)
  • Europe PMC (PubMed Central) (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
  • Pure Amsterdam UMC (publishedVersion)
  • Amsterdam UMC (VU Amsterdam) - Institutional Repository (publishedVersion)
  • Utrecht University Repository (Utrecht University) (submittedVersion, other-oa)
  • Iris (Roma Tre University) (submittedVersion)
  • Data Archiving and Networked Services (DANS) (submittedVersion)
Funders
  • European Commission (293589)
  • Nederlandse Organisatie voor Wetenschappelijk Onderzoek
  • National Institute on Drug Abuse (R01DA022628, DA022628)
Topics
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
  • Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
Keywords
social play, adolescent rats, medial prefrontal cortex, striatum, dorsomedial striatum, nucleus accumbens, prelimbic cortex, infralimbic cortex, orbitofrontal cortex, baclofen, muscimol, DNQX, glutamatergic inhibition, behavioral inhibition, reward
MeSH terms
Animals, Baclofen, Corpus Striatum, Male, Microinjections, Muscimol, Nucleus Accumbens, Quinoxalines, Social Behavior, Prefrontal Cortex, Excitatory Amino Acid Antagonists, Rats, GABA-B Receptor Agonists

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