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Cited by 64Neuroscience and Neuropharmacology ResearchNeuroendocrine regulation and behaviorNeurotransmitter Receptor Influence on Behavior

Dynamic changes in extracellular release of GABA and glutamate in the lateral septum during social play behavior in juvenile rats: Implications for sex-specific regulation of social play behavior

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Bredewold, R., Schiavo, J.K., van der Hart, M., Verreij, M., Veenema, A.H.·2015·Neuroscience
DOI 10.1016/j.neuroscience.2015.08.052PMC PMC4591248
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Abstract

Social play is a motivated and rewarding behavior that is displayed by nearly all mammals and peaks in the juvenile period. Moreover, social play is essential for the development of social skills and is impaired in social disorders like autism. We recently showed that the lateral septum (LS) is involved in the regulation of social play behavior in juvenile male and female rats. The LS is largely modulated by GABA and glutamate neurotransmission, but their role in social play behavior is unknown. Here, we determined whether social play behavior is associated with changes in the extracellular release of GABA and glutamate in the LS and to what extent such changes modulate social play behavior in male and female juvenile rats. Using intracerebral microdialysis in freely behaving rats, we found no sex difference in extracellular GABA concentrations, but extracellular glutamate concentrations are higher in males than in females under baseline conditions and during social play. This resulted in a higher glutamate/GABA concentration ratio in males vs. females and thus, an excitatory predominance in the LS of males. Furthermore, social play behavior in both sexes is associated with significant increases in extracellular release of GABA and glutamate in the LS. Pharmacological blockade of GABA-A receptors in the LS with bicuculline (100 ng/0.5 μl, 250 ng/0.5 μl) dose-dependently decreased the duration of social play behavior in both sexes. In contrast, pharmacological blockade of ionotropic glutamate receptors (NMDA and AMPA/kainate receptors) in the LS with AP-5+CNQX (2mM+0.4mM/0.5 μl, 30 mM+3mM/0.5 μl) dose-dependently decreased the duration of social play behavior in females, but did not alter social play behavior in males. Together, these data suggest a role for GABA neurotransmission in the LS in the regulation of juvenile social play behavior in both sexes, while glutamate neurotransmission in the LS is involved in the sex-specific regulation of juvenile social play behavior.

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  • AVP, glutamate, and GABA systems in the LS each modulate social play behavior in both male and female juvenile rats.

    “We previously showed that arginine-vasopressin (AVP), glutamate, and GABA systems in the LS each modulate social play behavior in both male and female juvenile rats (Veenema et al., 2013, Bredewold et al., 2014, 2015).”

    From Vasopressin regulates social play behavior in sex-specific ways through glutamate modulation in the lateral septum (2025) · cites this paper as Bredewold et al., 2015

    The Discussion reports that LS GABA-A receptor blockade reduced social play in both juvenile males and females, and it describes earlier findings that LS vasopressin-receptor blockade affected both sexes. But it reports that glutamate-receptor blockade reduced social play in females and did not alter it in males, so this source does not support the claim that all three systems modulate play in both sexes. (LLM, conf=0.90)

    Experimental — accuracy not yet measured

  • Of the AVP, glutamate, and GABA systems in the LS, AVP and glutamate regulate social play behavior in sex-specific ways.

    “Of these three systems, AVP and glutamate regulated social play behavior in sex-specific ways.”

    From Vasopressin regulates social play behavior in sex-specific ways through glutamate modulation in the lateral septum (2025) · cites this paper as Bredewold et al., 2015

  • Administration of glutamate receptor antagonists into the LS decreases social play levels in females, while no changes are seen in males.

    “In detail, administration of the AVP V1a receptor (V1aR) antagonist into the LS increased social play levels in males and decreased it in females (Veenema et al., 2013, Bredewold et al., 2014) while administration of glutamate receptor antagonists into the LS decreased social play levels in females, while no changes in social play levels were seen in males (Bredewold et al., 2015).”

    From Vasopressin regulates social play behavior in sex-specific ways through glutamate modulation in the lateral septum (2025) · cites this paper as Bredewold et al., 2015

  • Drug doses were chosen based on previous microinjection studies in rats inducing changes in behavior.

    “Drug doses were chosen based on previous microinjection studies in rats inducing changes in behavior (Veenema et al., 2012(Veenema et al., , 2013;;Bredewold et al., 2015;Stanley et al., 1993;Numan et al., 2010).”

    From Vasopressin regulates social play behavior in sex-specific ways through glutamate modulation in the lateral septum (2025) · cites this paper as Bredewold et al., 2015

  • LS-V1aR blockade induced a sex difference in social play.

    “Furthermore, we confirmed previous findings that LS-V1aR blockade induced a sex difference in social play (Veenema et al., 2013;Bredewold et al., 2015).”

    From Vasopressin regulates social play behavior in sex-specific ways through glutamate modulation in the lateral septum (2025) · cites this paper as Bredewold et al., 2015

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Research works printed but not linked: 80

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Authors
Bredewold, R., Schiavo, J. K., van der Hart, M., Verreij, M., & Veenema, A. H.
Affiliations
Boston College (US)
Corresponding author
Bredewold, R.
ORCID
Venue
Neuroscience
Publisher
Elsevier BV
Published
2015-10
Volume
307
Pages
117-127
ISSN
0306-4522 (ISSN-L)
DOI
10.1016/j.neuroscience.2015.08.052
PMC
PMC4591248
OpenAlex
W1707998845
Cited by
64
References
103
Citations by year
2026: 2 · 2025: 3 · 2024: 7 · 2023: 5 · 2022: 5 · 2021: 10 · 2020: 8 · 2019: 7 · 2018: 9 · 2017: 5 · 2016: 1 · 2015: 1 · 2014: 1
FWCI
2.49
Type
journal article
Language
en
Open access
Licence
www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations
  • Neuroscience (publishedVersion)
  • PubMed (publishedVersion)
  • PubMed Central (acceptedVersion)
Funders
National Institute of Mental Health (R01MH102456)
Topics
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
  • Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
Keywords
social play, lateral septum, GABAergic neurotransmission, glutamatergic neurotransmission, sex differences, young rats, bicuculline, AP5, CNQX, NMDA receptor, non-NMDA receptors, glutamate/GABA ratio, autism spectrum disorder
MeSH terms
Analysis of Variance, Animals, Chromatography, High Pressure Liquid, Extracellular Space, Female, gamma-Aminobutyric Acid, Humans, Male, Play and Playthings, Septal Nuclei, Sex Characteristics, Social Behavior, Case-Control Studies, Rats, Sprague-Dawley, Microdialysis, GABA Agents, Excitatory Amino Acid Agents, Glutamic Acid, Rats, Tandem Mass Spectrometry

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