Sex differences in stress-induced social withdrawal: Independence from adult gonadal hormones and inhibition of female phenotype by corncob bedding
Open accessAbstract
There is compelling evidence for important sex differences in behavioral and hormonal responses to psychosocial stress. Here we examined the effects of gonadal hormones on behavioral responses to social defeat stress in monogamous California mice (Peromyscus californicus). Three episodes of social defeat induced social withdrawal in intact females but not males. Gonadectomy blocked corticosterone responses to defeat in females and sensitized male corticosterone responses. However, gonadectomy had no effects on social interaction behavior, suggesting that social withdrawal is not dependent on gonadal hormones in the adult California mouse. In contrast, defeat reduced exploratory behavior in the open field test for intact but not castrated males. We also examined the effects of social defeat on social interaction behavior when California mice were raised on corncob bedding, which has estrogenic properties. In this dataset of over 300 mice, we observed that social defeat did not induce social withdrawal when females were raised on corncob bedding. This finding suggests that the use of corncob in rodent studies could mask important sex differences in the effects of stress on brain and behavior. Although gonadal hormones do not affect social withdrawal behavior in adults, our data suggest that hormones may act earlier in development to induce a more resilient social phenotype.
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In adults, sex differences in behavioral responses to defeat are independent of gonadal hormones.
“In adults, sex differences in behavioral responses to defeat are independent of gonadal hormones (42, 43), suggesting that sex differences are organized during development.”
From Sexual differentiation of neural mechanisms of stress sensitivity during puberty (2023) · cites this paper as [43]
The Results (Experiment 1) show that defeat reduced social interaction in both intact and ovariectomized female California mice, but not males; gonadectomy had no effect on that social-withdrawal pattern. The Discussion concludes that adult gonadal hormones do not appear to mediate this sex difference. The citing sentence states the conclusion more broadly, without limiting it to California mice and the social-withdrawal behavior studied. (LLM, conf=0.82)
Experimental — accuracy not yet measuredPrepubertal castration also increased avoidance and social vigilance toward novel naive target mice, similar to stressed adult females.
“Prepubertal castration also increased avoidance and social vigilance toward novel naive target mice, similar to stressed adult females (43, 73).”
From Sexual differentiation of neural mechanisms of stress sensitivity during puberty (2023) · cites this paper as [43]
The Results (Experiment 1; page unavailable) report reduced social interaction and more time in corner zones for stressed adult females when a stimulus mouse was present. But the Methods specify that all mice were adults, and the Results found no effect of gonadectomy on those social measures. This paper does not establish that prepubertal castration increased avoidance or social vigilance. (LLM, conf=0.85)
Experimental — accuracy not yet measuredThese results contrast with adults, where social defeat decreases social approach and increases social vigilance in females but not males.
“These results contrast with observed sex differences in adults, which show that social defeat decreases social approach (38, 42, 43, 51) and increases social vigilance (40) in females but not males.”
From Sexual differentiation of neural mechanisms of stress sensitivity during puberty (2023) · cites this paper as [43]
Adult gonadal hormones have little impact on stress-induced social avoidance.
“our previous work clearly demonstrates that adult gonadal hormones have little impact on stress-induced social avoidance (43, 50).”
From Sexual differentiation of neural mechanisms of stress sensitivity during puberty (2023) · cites this paper as [43]
In adult California mice, androgens do not affect social approach regardless of stress exposure even though they blunt acute corticosterone responses to defeat.
“Interestingly, in adult California mice, androgens do not affect social approach regardless of stress exposure even though they blunt acute corticosterone responses to defeat (43).”
From Sexual differentiation of neural mechanisms of stress sensitivity during puberty (2023) · cites this paper as [43]
Male and female California mice were randomly assigned to control handling or social defeat for 3 consecutive days.
“Male and female mice were randomly assigned to control handling or social defeat for 3 consecutive days as described (16).”
From Oxytocin receptors in the anteromedial bed nucleus of the stria terminalis promote stress-induced social avoidance in female California mice (2018) · cites this paper as [16]
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- Greenberg GD Voigt H Trainor BC in review Low but not high doses of sertraline reverse defeat-induced social withdrawal and upregulation of brain derived neurotrophic factor in female California mice (Peromyscus californicus)
- Martinez M Calvo-Torrent A Pico-Alfonso MA 1998 Social defeat and subordination as models of social stress in laboratory rodents: A review Aggressive Behavior 24 241 256
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Sex differences in anxiety and depression: circuits and mechanisms
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“Male and female mice were randomly assigned to control handling or social defeat for 3 consecutive days as described (16).”
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“Interestingly, Trainor and colleagues [59] reported no effect of adult hormone manipulation in the paradigm, but an effect of corncob bedding (which has estrogenic properties) during development, together suggesting developmental hormonal programming.”
BackgroundChronic and acute effects of stress on energy balance: are there appropriate animal models?
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“The social defeat produces a greater increase in serum CORT and inhibition of social interaction in subordinate females than males (227, 228), but the effect of social defeat on body weight of the females has not been reported.”
BackgroundExtrahypothalamic oxytocin neurons drive stress-induced social vigilance and avoidance
Duque-Wilckens, N., Torres, L. Y., Yokoyama, S., Minie, V. A., Tran, A. M., Petkova, S. P., Hao, R., Ramos-Maciel, S., Rios, R. A., Jackson, K., et al. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2011890117 · Cited by 139 · see citing works
Self-citationSex-specific effects of stress on oxytocin neurons correspond with responses to intranasal oxytocin
Steinman, M. Q., Duque-Wilckens, N., Greenberg, G. D., Hao, R., Campi, K. L., Laredo, S. A., Laman-Maharg, A., Manning, C. E., Doig, I. E., Lopez, E. M., et al. (2016) · Biological Psychiatry · doi:10.1016/j.biopsych.2015.10.007 · Cited by 131 · see citing works
“Female California mice are aggressive (27), so male and female mice can be exposed to episodes of social defeat with similar intensity (28).”
InfluentialSelf-citationWilliams, A. V., Duque‐Wilckens, N., Ramos-Maciel, S., Campi, K. L., Bhela, S. K., Xu, C. K., Jackson, K., Chini, B., Pesavento, P. A., & Trainor, B. C. (2020) · Neuropsychopharmacology · doi:10.1038/s41386-020-0657-4 · Cited by 109 · see citing works
“Social interaction test and social vigilance Social interaction testing was performed as previously described [42, 43].”
MethodAcute stress impairs cognitive flexibility in men, not women
Shields, G. S., Trainor, B. C., Lam, J. C., & Yonelinas, A. P. (2016) · Stress · doi:10.1080/10253890.2016.1192603 · Cited by 93 · see citing works
“(Trainor et al., 2013); stress should not be presumed to influence”
Backgroundde Abreu, M. S., Demin, K. A., Giacomini, A. C. V. V., Amstislavskaya, T. G., Strekalova, T. V., Maslov, G. O., Kositsin, Y., Petersen, E. V., & Kalueff, A. V. (2021) · Neurobiology of Stress · doi:10.1016/j.ynstr.2021.100405 · Cited by 89 · see citing works
“Some sex differences have also been observed in this rodent model (Steinman and Trainor, 2017), as both sexes show similar rates of freezing when confronted with an aggressive resident, yet females make more attempts to flee (Trainor et al., 2013).”
Greenberg, G. D., Laman-Maharg, A., Campi, K. L., Voigt, H., Orr, V. N., Schaal, L., & Trainor, B. C. (2014) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2013.00223 · Cited by 89 · see citing works
Rapid effects of estrogens on behavior: Environmental modulation and molecular mechanisms
Laredo, S. A., Landeros, R. V., & Trainor, B. C. (2014) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2014.03.005 · Cited by 74 · see citing works
Stress and cognition: A user’s guide to designing and interpreting studies
Shields, G. S. (2020) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2019.104475 · Cited by 80 · see citing works
Laredo, S. A., Steinman, M. Q., Robles, C. F., Ferrer, E., Ragen, B. J., & Trainor, B. C. (2015) · European Journal of Neuroscience · doi:10.1111/ejn.12824 · Cited by 75 · see citing works
“In a previous study, we considered the effect of gonadectomy on stress hormones and behavior (Trainor et al., 2013).”
BackgroundMethodInfluentialSteinman, M. Q., Laredo, S. A., Lopez, E. M., Manning, C. E., Hao, R. C., Doig, I. E., Campi, K. L., Flowers, A. E., Knight, J. K., & Trainor, B. C. (2015) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2014.09.009 · Cited by 73 · see citing works
“In the social interaction test stressed male California mice generally approach unfamiliar social stimuli (Greenberg et al., 2014; Trainor et al., 2013) and in tests of spatial memory stressed males show more deficits in reversal learning (Laredo et al., in review).”
BackgroundMethodResultInfluentialRobles, C. F., McMackin, M. Z., Campi, K. L., Doig, I. E., Takahashi, E. Y., Pride, M. C., & Trainor, B. C. (2014) · Behavioural Brain Research · doi:10.1016/j.bbr.2014.01.003 · Cited by 65 · see citing works
“Social stress activates KOR signaling pathways, and in previous studies we observed that the effect of defeat stress on social interaction behavior is stronger in female California mice versus males (Trainor et al., 2011, Trainor et al., 2013, Greenberg et al., 2014).”
BackgroundMethodLukas, M., & Neumann, I. D. (2014) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2014.03.013 · Cited by 63 · see citing works
Sexual Dimorphism in the Brain of the Monogamous California Mouse (Peromyscus californicus)
Campi, K. L., Jameson, C. E., & Trainor, B. C. (2013) · Brain Behavior and Evolution · doi:10.1159/000353260 · Cited by 59 · see citing works
“For example, social stress in California mice induces a transient increase in corticosterone in females [Trainor et al., 2013] but an enduring increase in baseline corticosterone in males [Trainor et al., 2011].”
BackgroundSex differences in effects of dopamine D1 receptors on social withdrawal
Campi, K. L., Greenberg, G. D., Kapoor, A., Ziegler, T. E., & Trainor, B. C. (2014) · Neuropharmacology · doi:10.1016/j.neuropharm.2013.09.026 · Cited by 55 · see citing works
“Mice were randomly assigned to social defeat or control handling for three consecutive days (Trainor et al., 2011, 2013).”
InfluentialSelf-citationDifferential chronic social stress models in male and female mice
Furman, O., Tsoory, M., & Chen, A. (2021) · European Journal of Neuroscience · doi:10.1111/ejn.15481 · Cited by 57 · see citing works
“This sex-suitable research project revealed that the long-term effects of social defeat stress are sex specific (Trainor et al., 2011, 2013) and has resulted in follow-up studies on cognitive flexibility following stress in mice and humans (Laredo et al., 2015; Shields et al., 2016).”
BackgroundSteinman, M. Q., & Trainor, B. C. (2016) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2016.06.021 · Cited by 54 · see citing works
“Trainor, Sex diffe California mouse: Insights from a monogamous rodent, Semin Cell De id not alter the effect of defeat stress on social interaction behavor in males or females [42].”
BackgroundInfluentialEstes, M. L., Prendergast, K., MacMahon, J. A., Cameron, S., Aboubechara, J. P., Farrelly, K., Sell, G. L., Haapanen, L. A. D., Schauer, J. D., Horta, A., et al. (2020) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2020.04.061 · Cited by 54 · see citing works
“, 2018), bedding (Trainor et al., 2013), temperature and humidity (Hylander et al.”
BackgroundDuque‐Wilckens, N., Steinman, M. Q., Laredo, S. A., Hao, R., Perkeybile, A. M., Bales, K. L., & Trainor, B. C. (2016) · Neuropharmacology · doi:10.1016/j.neuropharm.2016.07.018 · Cited by 52 · see citing works
“This effect is independent of gonadal steroids (Trainor et al., 2013) and can be reversed with chronic but not acute sertraline treatment (Greenberg et al., 2014).”
InfluentialEvaluating social defeat as a model for psychopathology in adult female rodents
Solomon, M. B. (2016) · Journal of Neuroscience Research · doi:10.1002/jnr.23971 · Cited by 52 · see citing works
“Although the neuroendocrine responses to social defeat appear to be dependent upon the presence of circulating gonadal hormones, the behavioral responses to social defeat in both sexes are independent (Trainor et al., 2013).”
BackgroundWhat’s wrong with my experiment?: The impact of hidden variables on neuropsychopharmacology research
Butler-Struben, H. M., Kentner, A. C., & Trainor, B. C. (2022) · Neuropsychopharmacology · doi:10.1038/s41386-022-01309-1 · Cited by 47 · see citing works
“In female California mice, corncob bedding reduced but did not eliminate effects of social defeat stress in a social interaction test [57].”
BackgroundThe epidemiology of fighting in group-housed laboratory mice
Theil, J. H., Dallaire, J. A., Weber, E. M., Gaskill, B. N., Pritchett‐Corning, K. R., Felt, S. A., & Garner, J. P. (2020) · Scientific Reports · doi:10.1038/s41598-020-73620-0 · Cited by 50 · see citing works
Greenberg, G. D., Steinman, M. Q., Doig, I. E., Hao, R., & Trainor, B. C. (2015) · European Journal of Neuroscience · doi:10.1111/ejn.13099 · Cited by 49 · see citing works
“This social organization is unique and allows the study of males and females exposed to an equivalent intensity of defeat stress in a consistent ethological context (Trainor et al., 2013).”
BackgroundMethodInfluentialSelf-citationBambico, F. R., Lacoste, B., Hattan, P. R., & Gobbi, G. (2013) · Cerebral Cortex · doi:10.1093/cercor/bht310 · Cited by 47 · see citing works
Nakata, M., Sano, K., Musatov, S. A., Yamaguchi, N., Sakamoto, T., & Ogawa, S. (2016) · eNeuro · doi:10.1523/eneuro.0155-15.2016 · Cited by 47 · see citing works
“However, because we used corncob bedding, which has been reported to contain phytoestrogens (Landeros et al., 2012; Trainor et al., 2013), it is still possible that regardless of AAV treatment, all mice used in the present study may have been exposed estrogenic stimulation enough to partially organize neural circuitry…”
MethodWilliams, A. V., Laman-Maharg, A., Armstrong, C. V., Ramos-Maciel, S., Minie, V. A., & Trainor, B. C. (2018) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2018.06.001 · Cited by 49 · see citing works
“Two days after sucrose testing females were tested in social interaction as previously described (Greenberg et al., 2014; Trainor et al., 2013) in both experiment 2 and experiment 3.”
Convergent neuroendocrine mechanisms of social buffering and stress contagion
Peen, N. F., Duque‐Wilckens, N., & Trainor, B. C. (2021) · Hormones and Behavior · doi:10.1016/j.yhbeh.2021.104933 · Cited by 44 · see citing works
Wang, L., Hou, W., He, Z., Yuan, W., Yang, J., Yang, Y., Jia, R., Zhu, Z., Zhou, Y., & Tai, F. (2017) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2017.11.002 · Cited by 43 · see citing works
“For example, social defeat increases anxiety response (Greenberg et al., 2015), induces social withdrawal (Trainor et al., 2013) and reduces social interaction behavior in female California mice (Trainor et al., 2011; Greenberg et al., 2015), and this effect can be seen as long as ten weeks after…”
BackgroundSex Differences in the Effects of a Kappa Opioid Receptor Antagonist in the Forced Swim Test
Laman-Maharg, A., Williams, A. V., Zufelt, M. D., Minie, V. A., Ramos-Maciel, S., Hao, R., Sanchez, E. O., Copeland, T., Silverman, J. L., Leigh, A., et al. (2018) · Frontiers in Pharmacology · doi:10.3389/fphar.2018.00093 · Cited by 42 · see citing works
“Female California mice were randomly assigned to social defeat stress or control handling for 3 consecutive days (Trainor et al., 2011, 2013).”
MethodAnxious to see you: Neuroendocrine mechanisms of social vigilance and anxiety during adolescence
Wright, E. C., Hostinar, C. E., & Trainor, B. C. (2020) · European Journal of Neuroscience · doi:10.1111/ejn.14628 · Cited by 55 · see citing works
“In adult California mice, gonadal hormones are not a critical mechanism driving sex differences (Trainor et al., 2011, 2013).”
BackgroundSocial withdrawal and gender differences: Clinical phenotypes and biological bases
Masi, G., Berloffa, S., Milone, A., & Brovedani, P. (2021) · Journal of Neuroscience Research · doi:10.1002/jnr.24802 · Cited by 42 · see citing works
Environmental Health Factors and Sexually Dimorphic Differences in Behavioral Disruptions
Rosenfeld, C. S., & Trainor, B. C. (2014) · Current Environmental Health Reports · doi:10.1007/s40572-014-0027-7 · Cited by 37 · see citing works
Stress, sex, and motivated behaviors
Laman-Maharg, A., & Trainor, B. C. (2016) · Journal of Neuroscience Research · doi:10.1002/jnr.23815 · Cited by 35 · see citing works
“…but not stressed males show decreased social interaction after exposure to 3 consecutive days of social defeat consisting of 7 min or seven attacks (Trainor et al., 2011, 2013; Greenberg et al., 2014, 2015), and this behavioral change is not accompanied by reduced locomotor or exploratory behavior.”
BackgroundSexual differentiation of neural mechanisms of stress sensitivity during puberty
Wright, E. C., Luo, P. X., Zakharenkov, H. C., Serna Godoy, A., Lake, A. A., Prince, Z. D., Sekar, S., Culkin, H. I., Ramirez, A. V., Dwyer, T., et al. (2023) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2306475120 · Cited by 34 · see citing works
Social Defeat Stress, Sex, and Addiction-Like Behaviors
Shimamoto, A. (2018) · International review of neurobiology · doi:10.1016/bs.irn.2018.07.009 · Cited by 35 · see citing works
Tickerhoof, M. C., Hale, L. H., Butler, M. J., & Smith, A. S. (2019) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2019.104542 · Cited by 30 · see citing works
Need for gender-specific pre-analytical testing: The dark side of the moon in laboratory testing
Franconi, F., Rosano, G. M. C., & Campesi, I. (2014) · International Journal of Cardiology · doi:10.1016/j.ijcard.2014.11.019 · Cited by 30 · see citing works
“For example, corncob bedding, which has estrogenic activity, blunted response to defeat in female mice but not in male mice [174].”
The challenge hypothesis revisited: Focus on reproductive experience and neural mechanisms
Marler, C. A., & Trainor, B. C. (2019) · Hormones and Behavior · doi:10.1016/j.yhbeh.2019.104645 · Cited by 29 · see citing works
Oxytocin receptor behavioral effects and cell types in the bed nucleus of the stria terminalis
Luo, P. X., Zakharenkov, H. C., Torres, L. Y., Rios, R. A., Gegenhuber, B., Black, A. M., Xu, C. K., Minie, V. A., Tran, A. M., Tollkuhn, J., et al. (2022) · Hormones and Behavior · doi:10.1016/j.yhbeh.2022.105203 · Cited by 27 · see citing works
Mean Girls: Social Stress Models for Female Rodents
Kuske, J. X., & Trainor, B. C. (2021) · Current Topics in Behavioral Neurosciences · doi:10.1007/7854_2021_247 · Cited by 27 · see citing works
Kowalczyk, A. S., Davila, R., & Trainor, B. C. (2018) · Hormones and Behavior · doi:10.1016/j.yhbeh.2017.12.010 · Cited by 25 · see citing works
“Males assigned to defeat were placed in the home cage of a vasectomized resident male for either 7 min or until the male received 7 bites (Trainor et al., 2013; Greenberg et al., 2014).”
MethodSex-specific effects of social defeat stress on miRNA expression in the anterior BNST
Luo, P. X., Manning, C., Fass, J. N., Williams, A. V., Hao, R., Campi, K. L., & Trainor, B. C. (2020) · Behavioural Brain Research · doi:10.1016/j.bbr.2020.113084 · Cited by 25 · see citing works
Interconnected neural circuits mediating social reward
Isaac, J., & Murugan, M. (2024) · Trends in Neurosciences · doi:10.1016/j.tins.2024.10.004 · Cited by 25 · see citing works
Influence of housing variables on the development of stress-sensitive behaviors in the rat
Sakhai, S. A., Preslik, J. M., & Francis, D. D. (2013) · Physiology & Behavior · doi:10.1016/j.physbeh.2013.08.003 · Cited by 23 · see citing works
“The most recent paper using the California mouse as amodel provides evidence, in linewith our own, demonstrating that the effects of corncob bedding on adult stress-relevant behaviors appears to be generated during the postnatal, developmental window and not in adulthood [55].”
BackgroundWright, E. C., Johnson, S., Hao, R., Kowalczyk, A. S., Greenberg, G. D., Sanchez, E. O., Laman-Maharg, A., Trainor, B. C., & Rosenfeld, C. S. (2017) · Journal of Neuroendocrinology · doi:10.1111/jne.12475 · Cited by 22 · see citing works
Laman-Maharg, A., Copeland, T., Sanchez, E. O., Campi, K. L., & Trainor, B. C. (2017) · Behavioural Brain Research · doi:10.1016/j.bbr.2017.06.015 · Cited by 21 · see citing works
Hou, W., He, Z., Yang, Y., Yuan, W., Wang, L., Zhang, J., Zhang, X., Cai, W., Guo, Q., & Tai, F. (2020) · European Journal of Neuroscience · doi:10.1111/ejn.14691 · Cited by 21 · see citing works
“…dark box (length × width × height, 27 cm × 18 cm × 27 cm) and a hyaline bright box (length × width × height, 27 cm × 27 cm × 27 cm) with a small door (length × width, 7 cm × 6 cm) between them that allowed the voles to move freely between the boxes (Kinsey et al., 2007; Trainor et al., 2013).”
BackgroundMethodInfluentialSerotonin 2C receptor contributes to gender differences in stress-induced hypophagia in aged mice
Yamada, C., Sadakane, C., Nahata, M., Saegusa, Y., Nakagawa, K., Okubo, N., Ohnishi, S., Hattori, T., & Takeda, H. (2015) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2015.02.006 · Cited by 18 · see citing works
Harris, B., Roberts, B. R., DiMarco, G. M., Maldonado, K. A., Okwunwanne, Z., Savonenko, A., & Soto, P. (2022) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2022.114126 · Cited by 14 · see citing works
Comparison of Four Beddings for Ammonia Control in Individually Ventilated Mouse Cages
Tataryn, N. M., Buckmaster, C. A., Schwiebert, R. S., & Swennes, A. G. (2020) · Journal of the American Association for Laboratory Animal Science · doi:10.30802/aalas-jaalas-20-000051 · Cited by 16 · see citing works
Ulfhake, B., Lerat, H., Honetschlager, J., Pernold, K., Rynekrová, M., Escot, K., Recordati, C., Kuiper, R., Rosati, G., Rigamonti, M., et al. (2022) · PLoS ONE · doi:10.1371/journal.pone.0267281 · Cited by 16 · see citing works
“In particular, corn cob and pine chips have been considered toxic or troublesome in a variety of contexts [83–87], but also other wood shavings like the widely used aspen chips have only been tested for a non-exhaustive library of chemicals and the users are left uninformed about potential…”
Sex Differences in the Social Behavior Network and Mesolimbic Dopamine System
Greenberg, G. D., & Trainor, B. C. (2015) · Elsevier eBooks · doi:10.1016/b978-0-12-802114-9.00004-4 · Cited by 15 · see citing works
“As the California mouse is one of the few species in which females are aggressive toward other females, this provides a unique opportunity to study both males and females exposed to an equivalent intensity of defeat stress (Trainor et al., 2013).”
BackgroundAspen shaving versus chip bedding: effects on breeding and behavior
Jackson, E., Demarest, K., Eckert, W. J., Cates‐Gatto, C., Nadav, T., Cates, L., Howard, H., & Roberts, A. J. (2014) · Laboratory Animals · doi:10.1177/0023677214553320 · Cited by 14 · see citing works
Minie, V. A., Petric, R., Ramos-Maciel, S., Wright, E. C., Trainor, B. C., & Duque-Wilckens, N. (2021) · Applied Animal Behaviour Science · doi:10.1016/j.applanim.2021.105381 · Cited by 13 · see citing works
Schuler, H., Eid, R. S., Wu, S. S., Tse, Y. C., Cvetkovska, V., Lopez, J., Quinn, R., Zhou, D., Meccia, J., Dion‐Albert, L., et al. (2024) · Biological Psychiatry · doi:10.1016/j.biopsych.2024.11.017 · Cited by 13 · see citing works
“To further examine generalizability, we explored 2 models of interfemale aggression (40,41), and found that ΔVelocity did not capture robust stress effects in either model, although notably SI ratio was also quite variable (Figure S5).”
Williams, A. V., Peña, C. J., Ramos-Maciel, S., Laman-Maharg, A., Sanchez, E. O., Britton, M., Durbin-Johnson, B. P., Settles, M. L., Hao, R., Yokoyama, S., et al. (2022) · Biological Psychiatry · doi:10.1016/j.biopsych.2022.06.030 · Cited by 11 · see citing works
“Similar to previous studies of California mice (38,44), stressed females but not males showed a decrease in social interaction ratio when the target was present (Figure 1B) (stress 3 sex interaction effect, F 1,29 = 4.37, p , .05), and planned comparisons showed an effect of stress in females but…”
ResultInfluentialWright, E. C., Parks, T. V., Alexander, J. O., Supra, R., & Trainor, B. C. (2018) · Behavioural Brain Research · doi:10.1016/j.bbr.2018.05.011 · Cited by 11 · see citing works
“In a novel environment, three episodes of social defeat induces social avoidance in females [31,32] and in males that receive an acute injection immediately before behavior testing [33,34].”
Navarrete, J. S., Schneider, K. N., Smith, B. M., Goodwin, N. L., Zhang, Y. Y., Salazar, A. S., Gonzalez, Y. E., Anumolu, P., Gross, E., Tsai, V. S., et al. (2024) · Biological Psychiatry · doi:10.1016/j.biopsych.2024.01.007 · Cited by 10 · see citing works
Lake, A. A., & Trainor, B. C. (2024) · Hormones and Behavior · doi:10.1016/j.yhbeh.2024.105487 · Cited by 9 · see citing works
Micro- and Macroenvironmental Conditions and Stability of Terrestrial Models
Lee, V. K., David, J. M., & Huerkamp, M. J. (2019) · ILAR Journal · doi:10.1093/ilar/ilaa013 · Cited by 10 · see citing works
Sex differences in responses to aggressive encounters among California mice
Kuske, J. X., Godoy, A. S., Ramirez, A. V., & Trainor, B. C. (2023) · Hormones and Behavior · doi:10.1016/j.yhbeh.2024.105537 · Cited by 8 · see citing works
Jones, S. L., Antonie, R. A., & Pfaus, J. G. (2015) · Hormones and Behavior · doi:10.1016/j.yhbeh.2015.05.002 · Cited by 6 · see citing works
“Trainor et al. (2013) recently suggested that housing on corncob bedding during development may masculinize brain circuits controlling behavioral responses to social defeat, since females housed on corncob (rather than Sani-Chips) behave more male-like.”
BackgroundWhitten, C. J., King, J. E., Rodriguez, R. M., Hennon, L. M., Scarborough, M. C., Hooker, M. K., Jenkins, M. S., Katigbak, I. M., & Cooper, M. A. (2024) · Hormones and Behavior · doi:10.1016/j.yhbeh.2024.105577 · Cited by 6 · see citing works
Whitten, C. J., Kelly, J. R., Gillespie, A. L., Brooks, H. J. B., Hooker, M. K., Temple, A., Hennon, L. M., Kilgore, B. J., Singamaneni, Y. B., Schulz, K. M., et al. (2025) · Developmental Psychobiology · doi:10.1002/dev.70020 · Cited by 7 · see citing works
Estes, M. L., Farrelly, K., Cameron, S., Aboubechara, J. P., Haapanen, L. A. D., Schauer, J. D., Horta, A., Prendergast, K., MacMahon, J. A., Shaffer, C. I., et al. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/699983 · Cited by 4 · see citing works
“Vivariumspecific environmental factors such as cage system (13), bedding (14), temperature and humidity (15), technician sex (16), and microbiota (17) exposure may all contribute to MIA susceptibility and outcomes (11) (Supplemental Note 1).”
BackgroundButler-Struben, H. M., Black, A. M., Wright, S. M., Dye, A. F., & Trainor, B. C. (2025) · Animal Behaviour · doi:10.1016/j.anbehav.2025.123098 · Cited by 5 · see citing works
Levoe, S. N., Flannery, B. M., Brignolo, L. L., Imai, D. M., Koehne, A. L., Austin, A. T., Bruun, D. A., Tancredi, D. J., & Lein, P. J. (2014) · PubMed · Cited by 5 · see citing works
Barbetti, M., Smiley, C. E., Savi, M., Sgoifo, A., Wood, S. K., & Carnevali, L. (2025) · Neurobiology of Stress · doi:10.1016/j.ynstr.2025.100751 · Cited by 4 · see citing works
“…males attack female intruders (Huhman, 2006), and female-to-female aggression has been described in highly aggressive lactating rats (Shimamoto et al., 2015; Ver Hoeve et al., 2013) and in the Peromyscus mouse species (e.g., California mice) (Steinman and Trainor, 2017; Trainor et al., 2013).”
Sexual dimorphism in zebrafish aggression and metabolism under acute ammonia stress
Chua, F. Z., Lin, L., Tseng, Y., & Chou, M. (2025) · Comparative Biochemistry and Physiology Part C Toxicology & Pharmacology · doi:10.1016/j.cbpc.2025.110131 · Cited by 4 · see citing works
Risk factors for barbering in laboratory mice
Ratuski, A. S., Theil, J. H., Ahloy-Dallaire, J., Gaskill, B., Pritchett-Corning, K., Felt, S. A., & Garner, J. P. (2025) · Scientific Reports · doi:10.1038/s41598-025-91687-5 · Cited by 5 · see citing works
“Corncob bedding additionally raises several red flags for rodent welfare, including increased aggression 7,41 , altered reproductive behavior 42 , hormone disruption 43 , and the fact that rodents prefer wood-based bedding over corncob 44 .”
Luo, P. X., Godoy, A. S., Zakharenkov, H. C., Vang, N., Wright, E. C., Balantac, T. A., Archdeacon, S. C., Black, A. M., Lake, A. A., Ramirez, A. V., et al. (2024) · Neuropsychopharmacology · doi:10.1038/s41386-024-01937-9 · Cited by 4 · see citing works
Balancing Act: An Interdisciplinary Exploration of Trade-offs in Reproducing Females
Josefson, C. C., Fitzwater, B. M., Beltran, R. S., da Costa, D. P., Fornara, J. H., Garland, T., Harris, B. N., Hinde, K., Hood, W. R., Hunt, E. S. E., et al. (2024) · Integrative and Comparative Biology · doi:10.1093/icb/icae092 · Cited by 4 · see citing works
Quantifying Sex Differences in Behavior in the Era of “Big” DataPreprint
Trainor, B. C., & Falkner, A. L. (2021) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a039164 · Cited by 4 · see citing works
Walker, S. L., & Glasper, E. R. (2024) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2024.101162 · Cited by 3 · see citing works
Sex differences in chronic social stress models in micePreprint
Furman, O., Tsoory, M., & Chen, A. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/605527 · Cited by 3 · see citing works
“GD on male mice exposed stress effects on CORT levels (no differences between stress and control group unless mice underwent GD) but GD on female mice erased stress effects on CORT (higher CORT in stressed vs. control intact females, no differences after GD; Trainor et al. 2013).”
BackgroundChrisman, A. N., Sugimoto, C., Butler-Struben, H. M., Minie, V. A., Eagle, A. L., Anderson, D., Duque‐Wilckens, N., Ramos, A., Lewis, Y. I., Archdeacon, S. C., et al. (2026) · Neuropsychopharmacology · doi:10.1038/s41386-026-02352-y · Cited by 1 · see citing works
“All procedures followed NIH guidelines and were approved by UC Davis and Michigan State University Institutional Animal Care and Use Committees.”
Comparison of two bedding types on the breeding fecundity of C57BL/6J mice
Pinckard, J., Gibson, L. A., & Williams, W. R. (2024) · Laboratory Animals · doi:10.1177/00236772241249783 · Cited by 1 · see citing works
Otsuka, T., Onishi, H., Suzuki, M., & Marusawa, M. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.06.13.495888 · Cited by 1 · see citing works
Salazar, V. I. C., Boender, A. J., Seelke, A. M. H., Gaard, L., Mederos, S. L., Rogers, S., Gutierrez, X. Z., Bales, K. L., Young, L. J., & Trainor, B. C. (2025) · Hormones and Behavior · doi:10.1016/j.yhbeh.2025.105845
Knollenberg, B. L., Dye, A. F., Oakland, Z. T., Redding, J. C., & Trainor, B. C. (2025) · Applied Animal Behaviour Science · doi:10.1016/j.applanim.2025.106905
Sayers, K., Allen, J., Bellanca, R. U., Brown, T. A., Coleman, K., Janavaris, M., Khuu, J. H., Lee, G. H., Perlman, J. E., Pomerantz, O., et al. (2026) · American Journal of Primatology · doi:10.1002/ajp.70149
Differential effects of stress by sex and stress model: the source matters
Carrillo, P. T., Yahel Vidal de la, O., Paz-Trejo, D. B., la Paz, L. D. O.-D., Trujillo-Gutiérrez, N., Sanchez-Flores, F., & Sánchez-Castillo, H. (2026) · Stress · doi:10.1080/10253890.2026.2712384
Estradiol and social withdrawal in addiction: a sex-specific neuroendocrine perspective
Kimble, V. M. (2026) · Oxford Open Neuroscience · doi:10.1093/oons/kvag009
“However, evidence also indicates that not all components of social stress reactivity are estrogen-dependent, underscoring that E2 acts as a modulatory rather than a deterministic factor ( Trainor et al. 2013).”
- Authors
- Trainor, B. C., Takahashi, E. Y., Campi, K. L., Florez, S. A., Greenberg, G. D., Laman-Maharg, A., Laredo, S. A., Orr, V. N., Silva, A. L., & Steinman, M. Q.
- Affiliations
- University of California, Davis (US)
- Corresponding author
- Trainor, Brian C.
- ORCID
- Trainor, Brian C.
- Venue
- Hormones and Behavior
- Publisher
- Elsevier BV
- Published
- 2013-03
- Volume
- 63
- Issue
- 3
- Pages
- 543-550
- ISSN
- 0018-506X (ISSN-L)
- PMC
- PMC3637973
- OpenAlex
- W2006912314
- Cited by
- 86
- References
- 63
- Citations by year
- 2026: 4 · 2025: 7 · 2024: 9 · 2023: 2 · 2022: 6 · 2021: 8 · 2020: 7 · 2019: 7 · 2018: 5 · 2017: 4 · 2016: 6 · 2015: 6 · 2014: 11 · 2013: 4
- FWCI
- 4.10
- Type
- journal article
- Language
- en
- Open access
- green
- europepmc.org
- Locations
- Hormones and Behavior (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Scholar Commons (Santa Clara University) (submittedVersion)
- Funders
- National Institutes of Health
- National Institute of Mental Health (R01 MH0850069-03, R01MH085069)
- Topics
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Sexual Differentiation and Disorders
- Keywords
- sex differences, social defeat stress, social withdrawal, gonadal hormones, gonadectomy, corticosterone, estrogenic effects, California mouse, Peromyscus californicus, exploratory behavior, social interaction behavior, stress resilience
- MeSH terms
- Animals, Behavior, Animal, Castration, Corticosterone, Female, Housing, Animal, Male, Neuropsychological Tests, Peromyscus, Phenotype, Sex Characteristics, Stress, Psychological, Gonadal Hormones, Phytoestrogens
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