Sexual differentiation of social play in rat pups is mediated by the neonatal androgen-receptor system
Abstract
Social play in juvenile rats, like that in several primate species (including humans), is sexually dimorphic. Males initiate and become involved in more play-fights than do their female peers. The play-fighting of female pups can be masculinized by neonatal exposure to either testosterone or 5α-dihydrotestosterone, suggesting that in the rat the masculinization of social play is mediated by the androgen-receptor system. In this paper we present evidence that further supports this hypothesis. In the first study we found that male pups treated with the antiandrogen, flutamide, during the neonatal period (days 1 through 10 of life) engaged in less play-fighting than did control males. Moreover, flutamide-treated, male pups play-fought no more frequently than did untreated females. In a subsequent study we found that flutamide, which blocked the masculinization of social play, dramatically reduced a testosterone-induced translocation of androgen receptors to the nuclear compartment in various brain regions (as measured by a nuclear exchange assay) in neonates. In a final study we examined the play-fighting of juvenile rat pups bearing the testicular feminization mutation (Tfm); animals that are known to be insensitive to androgens and show a marked deficiency of androgen receptors. Tfm males engaged in significantly less play-fighting than did control males. The Tfm males, like the flutamide-treated males, engaged in play-fighting at rates that were comparable to those of females…
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AR is critical in the development of social play behavior.
“As AR is critical in the development of social play behavior, 15,16,48 a reduction in AR expression during development could also contribute to the lasting decrease in juvenile social play behavior in males.”
From Neonatal MeCP2 is important for the organization of sex differences in vasopressin expression (2012) · cites this paper as [48]
Male rats castrated as neonates play at a lower frequency than intact males.
“Males castrated as neonates play at a lower frequency than do intact males (Beatty, Dodge, Traylor, & Meaney, 1981;Meaney, 1988;Meaney, Stewart, Poulin, & McEwen, 1983).”
From Play fighting in androgen-insensitivetfm rats: Evidence that androgen receptors are necessary for the development of adult playful attack and defense (2006) · cites this paper as Meaney, Stewart, Poulin, & McEwen, 1983
In Long Evans male rats, the higher frequency of play fighting depends on the presence of testicular hormones during the perinatal period.
“In addition, it has been shown that, in Long Evans male rats, the higher frequency of play fighting depends on the presence of testicular hormones during the perinatal period.”
From Play fighting in androgen-insensitivetfm rats: Evidence that androgen receptors are necessary for the development of adult playful attack and defense (2006) · cites this paper as Meaney, Stewart, Poulin, & McEwen, 1983
The present findings are not consistent with previous findings where tfm males were found to have a female-typical pattern of play frequency.
“When viewed in this manner, the present findings are not consistent with previous findings where tfm males were found to have a female-typical pattern of play frequency (Meaney et al., 1983).”
From Play fighting in androgen-insensitivetfm rats: Evidence that androgen receptors are necessary for the development of adult playful attack and defense (2006) · cites this paper as Meaney et al., 1983
In the Meaney et al. (1983) study, mixed groups of six juveniles, each containing two tfm, two WT males, and two females, were observed during short sampling periods to record spontaneously occurring play of these groups in their home cages.
“In the study by Meaney et al. (1983), mixed groups of six juveniles, each containing two tfm, two WT males, and two females, were observed during short sampling periods to record spontaneously occurring play of these groups in their home cages.”
From Play fighting in androgen-insensitivetfm rats: Evidence that androgen receptors are necessary for the development of adult playful attack and defense (2006) · cites this paper as Meaney et al. (1983)
Previous analysis found that tfm males exhibit lower levels of play fighting than control males as juveniles.
“Previous analysis of the play behavior of tfm males found that they exhibit lower levels of play fighting than control males as juveniles (Meaney et al., 1983;Meaney, 1988).”
From Play fighting in androgen-insensitivetfm rats: Evidence that androgen receptors are necessary for the development of adult playful attack and defense (2006) · cites this paper as Meaney et al., 1983
The development of play is influenced by perinatal testosterone through its 5α-reduced products.
“The development of play is influenced by perinatal testosterone through its 5α-reduced products [14].”
From Developmental exposure to low levels of ethinylestradiol affects social play in juvenile male rats (2020) · cites this paper as [14]
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“Play is organized by the perinatal interaction of androgens with the AR (Meaney et al. 1983; Meaney and McEwen 1986; Pellis and Pellis 1997).”
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“Supporting this idea, male rats with nonfunctional androgen receptors, so-called ‘Tfm males’, engage in some aspects of play at male-typical levels (Field, Whishaw, Pellis, & Watson, 2006; Meaney et al., 1983).”
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- Authors
- Meaney, M. J., Stewart, J., Poulin, P., & McEwen, B. S.
- Affiliations
- Rockefeller University (US)
- Concordia University (CA)
- Venue
- Neuroendocrinology
- Publisher
- S. Karger AG
- Published
- 2008-03-27
- Volume
- 37
- Issue
- 2
- Pages
- 85-90
- ISSN
- 0028-3835 (ISSN-L)
- 1423-0194
- OpenAlex
- W2072750985
- Cited by
- 144
- References
- 0
- Citations by year
- 2026: 1 · 2025: 3 · 2024: 3 · 2023: 3 · 2022: 2 · 2021: 5 · 2020: 5 · 2019: 2 · 2018: 3 · 2017: 7 · 2016: 4 · 2015: 3 · 2014: 10 · 2013: 3 · 2012: 2
- FWCI
- 1.92
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Neuroendocrinology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute of Neurological Disorders and Stroke (R01NS007080)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Sexual Differentiation and Disorders
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic and Clinical Aspects of Sex Determination and Chromosomal Abnormalities
- Keywords
- social play, play fighting, sexual differentiation, androgen receptor, neonatal androgen exposure, flutamide, androgen receptor antagonists, testosterone, dihydrotestosterone, brain, young rats, sex differences
- MeSH terms
- Agonistic Behavior, Androgens, Animals, Animals, Newborn, Female, Flutamide, Humans, Male, Play and Playthings, Receptors, Androgen, Receptors, Steroid, Sex Characteristics, Social Behavior, Androgen-Insensitivity Syndrome, Testosterone, Rats
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