Testosterone implants into the amygdala during the neonatal period masculinize the social play of juvenile female rats.
Abstract
The masculinization of social play behavior in the rat is dependent upon the actions of androgens during the neonatal period. The amygdala, a major androgen-target region in the rat limbic brain, appears to be a critical site for this androgenic effect. We tested this hypothesis by implanting testosterone-bearing cannulae into the amygdala of female rat pups on Day 1 of life; the implants were removed on Day 8 of life. The animals were then observed daily between Days 26 and 40 of life and the frequency of play-fighting was recorded. Testosterone-implanted females, like normal males, engaged in significantly more play-fighting than did control females (implanted with cholesterol-bearing cannulae). We have also presented data indicating that the testosterone diffusion from the cannulae was, for the most part, restricted to the amygdala. Thus, testosterone implanted into the amygdala mimicked the effects previously reported for systemic testosterone injections, supporting the idea that the amygdala is a critical region for the actions of androgens on the sexual differentiation of social play behavior in the rat.
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Implanting androgens directly into the MeA of developing females increases the frequency of their play to that of males.
“Conversely, implanting androgens directly into the MeA of developing females increases the frequency of their play to that of males (Meaney & McEwen, 1986).”
From Developmental origins of sex differences in the neural circuitry of play (2020) · cites this paper as Meaney & McEwen, 1986
In rats, social play is perinatally organized by androgens.
“In rats, one such behavior that is perinatally organized by androgens is social play.”
From Androgens and environmental antiandrogens affect reproductive development and play behavior in the Sprague-Dawley rat. (2002) · cites this paper as Meaney and McEwen 1986
The critical time in the rat for organization of play is the early neonatal period, when interactions of androgens with the androgen receptor set up the sex difference observed in juveniles.
“The critical time in the rat for organization of play is the early neonatal period, when interactions of androgens with the AR set up the sex differ- ence observed in juveniles (Meaney et al. 1983; Meaney and McEwen 1986; Pellis and Pellis 1997).”
From Androgens and environmental antiandrogens affect reproductive development and play behavior in the Sprague-Dawley rat. (2002) · cites this paper as Meaney and McEwen 1986
Play is organized by the perinatal interaction of androgens with the androgen receptor.
“Play is organized by the peri- natal interaction of androgens with the AR (Meaney et al. 1983; Meaney and McEwen 1986; Pellis and Pellis 1997).”
From Androgens and environmental antiandrogens affect reproductive development and play behavior in the Sprague-Dawley rat. (2002) · cites this paper as Meaney and McEwen 1986
Juvenile social play behavior is classically thought to be due to activation of androgen receptors, with some data suggesting a possible involvement of estrogen receptors.
“Juvenile social play behavior is classically thought to be due to activation of androgen receptors (6,32), with some data suggesting a possible involvement of estrogen receptors (8).”
From The Nuclear Receptor Corepressor Has Organizational Effects within the Developing Amygdala on Juvenile Social Play and Anxiety-Like Behavior (2010) · cites this paper as [32]
Masculinization of the male brain may in part be dependent on the effects of androgens on androgen receptors.
“masculinization of the male brain may in part be dependent on the effects of androgens on androgen receptors (Auger, Tetel, & McCarthy, 2000;Bakker, Honda, Harada, & Balthazart, 2002;Meaney & McEwen, 1986;Morris, Jordan, Dugger, & Breedlove, 2005).”
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 & McEwen, 1986
EE2 treatment increased play behavior pinning frequencies in female rats, similar to the increase caused by developmental androgen treatment.
“For example, EE 2 treatment resulted in increased play behavior pinning frequencies by female rats similar to that caused by developmental androgen treatment (Meaney, 1989;Meaney and McEwen, 1986;Tonjes et al., 1987).”
From Developmental Treatment with Ethinyl Estradiol, but Not Bisphenol A, Causes Alterations in Sexually Dimorphic Behaviors in Male and Female Sprague Dawley Rats (2014) · cites this paper as Meaney and McEwen, 1986
Androgen exposure during the early neonatal time period is responsible for later juvenile rough-and-tumble play behavior, and juvenile hormone levels are not involved in its regulation.
“Therefore, it is believed that androgen exposure during the early neonatal time period is responsible for later juvenile rough-and-tumble play behavior, and that juvenile hormone levels are not involved in its regulation (18, 25).”
From Puberty Blocker, Leuprolide, Reduces Sex Differences in Rough-and-Tumble Play and Anxiety-like Behavior in Juvenile Rats (2024) · cites this paper as [25]
High levels of androgen exposure around birth increases the level of rough-and-tumble play behavior during the juvenile period.
“Previous research has shown that high levels of androgen exposure around birth increases the level of rough-and-tumble play behavior during the juvenile period (25).”
From Puberty Blocker, Leuprolide, Reduces Sex Differences in Rough-and-Tumble Play and Anxiety-like Behavior in Juvenile Rats (2024) · cites this paper as [25]
Cites
Temporal boundary of the sensitive period for hormonal organization of social play in juvenile rats.
Beatty, W. W., Dodge, A. M., Traylor, K. L., & Meaney, M. J. (1981) · Physiology & Behavior · doi:10.1016/0031-9384(81)90017-2 · Cited by 70 · see citing works
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VanRyzin, J. W., Marquardt, A. E., Argue, K. J., Vecchiarelli, H. A., Ashton, S. E., Arambula, S. E., Hill, M. N., & McCarthy, M. M. (2019) · Neuron · doi:10.1016/j.neuron.2019.02.006 · Cited by 272 · see citing works
The influence of natural variations in maternal care on play fighting in the rat
Parent, C. I., & Meaney, M. J. (2008) · Developmental Psychobiology · doi:10.1002/dev.20342 · Cited by 175 · see citing works
Self-citationHermes, G., Li, N., Duman, C., & Duman, R. (2011) · Physiology & Behavior · doi:10.1016/j.physbeh.2010.12.019 · Cited by 111 · see citing works
Nilsson, C., Niklasson, M., Eriksson, E., Björntorp, P., & Holmäng, A. (1998) · Journal of Clinical Investigation · doi:10.1172/jci1353 · Cited by 103 · see citing works
A new view of sexual differentiation of mammalian brain
McCarthy, M. M. (2020) · Journal of Comparative Physiology A · doi:10.1007/s00359-019-01376-8 · Cited by 85 · see citing works
Taylor, P. V., Veenema, A. H., Paul, M. J., Bredewold, R., Isaacs, S., & de Vries, G. J. (2012) · Biology of Sex Differences · doi:10.1186/2042-6410-3-15 · Cited by 86 · see citing works
Hotchkiss, A. K., Ostby, J. S., Vandenburgh, J. G., & Gray, L. E. (2002) · Environmental Health Perspectives · doi:10.1289/ehp.02110s3435 · Cited by 82 · see citing works
Characterization of juvenile play in rats: importance of sex of self and sex of partner
Argue, K. J., & McCarthy, M. M. (2015) · Biology of Sex Differences · doi:10.1186/s13293-015-0034-x · Cited by 71 · see citing works
Dean, S. L., Knutson, J. F., Krebs‐Kraft, D. L., & McCarthy, M. M. (2012) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2012.08032.x · Cited by 70 · see citing works
Jessen, H. M., Kolodkin, M. H., Bychowski, M. E., Auger, C. J., & Auger, A. P. (2010) · Endocrinology · doi:10.1210/en.2009-0594 · Cited by 53 · see citing works
Argue, K. J., VanRyzin, J. W., Falvo, D. J., Whitaker, A. R., Yu, S. J., & McCarthy, M. M. (2017) · eneuro · doi:10.1523/eneuro.0344-16.2017 · Cited by 47 · see citing works
Developmental origins of sex differences in the neural circuitry of play
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
“Conversely, implanting androgens directly into the MeA of developing females increases the frequency of their play to that of males (Meaney & McEwen, 1986).”
BackgroundFerguson, S. A., Law, C. D., & Kissling, G. E. (2014) · Toxicological Sciences · doi:10.1093/toxsci/kfu077 · Cited by 32 · see citing works
“For example, EE2 treatment resulted in increased play behavior pinning frequencies by female rats similar to that caused by developmental androgen treatment (Meaney, 1989; Meaney and McEwen, 1986; Tonjes et al., 1987).”
BackgroundField, E. F., Whishaw, I. Q., Pellis, S. M., & Watson, N. V. (2006) · Developmental Psychobiology · doi:10.1002/dev.20121 · Cited by 30 · see citing works
Maternal Touch Moderates Sex Differences in Juvenile Social Play Behavior
Edelmann, M. N., Demers, C. H., & Auger, A. P. (2013) · PLoS ONE · doi:10.1371/journal.pone.0057396 · Cited by 27 · see citing works
Achterberg, E. J. M., Burke, C. J., & Pellis, S. M. (2023) · Behavioural Processes · doi:10.1016/j.beproc.2023.104933 · Cited by 20 · see citing works
Blake, B. E., & McCoy, K. A. (2015) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2015.04.021 · Cited by 20 · see citing works
Sex differences in juvenile play behavior differ among rat strains
Northcutt, K. V., & Nwankwo, V. C. (2018) · Developmental Psychobiology · doi:10.1002/dev.21760 · Cited by 20 · see citing works
Oliveira, G. D. F., Nguyen, A. T., Carreras-Simons, L., Niepsuj, T., Gadelhak, S. H., Johnson, A. K., Abdalla, A., Lev, E., Torres Román, S. G., Fuchs, S. N., et al. (2024) · Endocrinology · doi:10.1210/endocr/bqae046 · Cited by 5 · see citing works
Orsucci, I. C., Becker, K. D., Ham, J. R., Lee, J. D. A., Bowden, S. M., & Veenema, A. H. (2025) · Physiology & Behavior · doi:10.1016/j.physbeh.2025.115080 · Cited by 3 · see citing works
Forbes-Lorman, R. M. (2021) · Behavioral and Brain Functions · doi:10.1186/s12993-021-00183-z · Cited by 1 · see citing works
Partner Choice and Context‐Dependent Sex Differences in Rat Rough‐and‐Tumble Play
Ham, J. R., Pellis, S. M., & McDonald, R. J. (2026) · European Journal of Neuroscience · doi:10.1111/ejn.70426 · Cited by 1 · see citing works
- Authors
- Meaney, M. J., & McEwen, B. S.
- Affiliations
- Douglas Mental Health University Institute (CA)
- Corresponding author
- Meaney, Michael J.
- Venue
- Brain Research
- Publisher
- Elsevier BV
- Published
- 1986-11
- Volume
- 398
- Issue
- 2
- Pages
- 324-328
- ISSN
- 0006-8993 (ISSN-L)
- OpenAlex
- W2009712356
- Cited by
- 122
- References
- 1
- Citations by year
- 2026: 1 · 2025: 2 · 2024: 6 · 2023: 3 · 2022: 3 · 2021: 6 · 2020: 4 · 2019: 3 · 2018: 4 · 2017: 3 · 2016: 6 · 2015: 7 · 2014: 4 · 2013: 5 · 2012: 3
- FWCI
- 0.29
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Brain Research (publishedVersion)
- PubMed (publishedVersion)
- Funders
- U.S. Public Health Service (RF 81062)
- National Institute of Neurological Disorders and Stroke (NS 07080)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Sexual Differentiation and Disorders
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Health Sciences › Medicine › Reproductive Medicine › Hypothalamic control of reproductive hormones
- Keywords
- testosterone implants, amygdala, neonatal androgen exposure, social play, play fighting, female rats, androgen action, limbic system
- MeSH terms
- Amygdala, Animals, Animals, Newborn, Female, Gender Identity, Play and Playthings, Sex Characteristics, Testosterone, Rats
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