Mean Girls: Social Stress Models for Female Rodents
Open accessAbstract
Social stressors are known to have strong negative impacts on mental health. There is a long history of preclinical social defeat stress studies in rodents focusing on males that has produced important insights into the neural mechanisms that modulate depression- and anxiety-related behavior. Despite these impressive results, a historical weakness of rodent social stress models has been an under-representation of studies in females. This is problematic because rates of depression and anxiety are higher in women versus men. Recently there has been a surge of interest in adapting social stress methods for female rodents. Here we review new rodent models that have investigated numerous facets of social stress in females. The different models have different strengths and weaknesses, with some model systems having stronger ethological validity with other models having better access to molecular tools to manipulate neural circuits. Continued use and refinement of these complementary models will be critical for addressing gaps in understanding the function of neural circuits modulating depression- and anxiety-related behavior in females.
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California mice are an ideal species for studying sex differences in stress responses.
“California mice are an ideal species for studying sex differences in stress responses (44) and have a slower pace of development compared to other rodents (45, 46).”
From Sexual differentiation of neural mechanisms of stress sensitivity during puberty (2023) · cites this paper as [44]
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McLean, C. P., Asnaani, A., Litz, B. T., & Hofmann, S. G. (2011) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2011.03.006 · Cited by 2,519 · see citing works
A standardized protocol for repeated social defeat stress in mice
Golden, S. A., Covington, H. E., Berton, O., & Russo, S. J. (2011) · Nature Protocols · doi:10.1038/nprot.2011.361 · Cited by 1,581 · see citing works
The neurobiology of pair bonding.
Young, L. J., & Wang, Z. (2004) · Nature Neuroscience · doi:10.1038/nn1327 · Cited by 1,523 · see citing works
A role for central vasopressin in pair bonding in monogamous prairie voles
Winslow, J. T., Hastings, N., Carter, C. S., Harbaugh, C. R., & Insel, T. R. (1993) · Nature · doi:10.1038/365545a0 · Cited by 948 · see citing works
Functional identification of an aggression locus in the mouse hypothalamus
Lin, D., Boyle, M. P., Dollar, P., Lee, H., Lein, E. S., Perona, P., & Anderson, D. J. (2011) · Nature · doi:10.1038/nature09736 · Cited by 914 · see citing works
Sex-specific transcriptional signatures in human depression
Labonté, B., Engmann, O., Purushothaman, I., Menard, C., Wang, J., Tan, C., Scarpa, J. R., Moy, G., Loh, Y.-H. E., Cahill, M., et al. (2017) · Nature Medicine · doi:10.1038/nm.4386 · Cited by 748 · see citing works
Sex differences in stress-related psychiatric disorders: neurobiological perspectives
Bangasser, D. A., & Valentino, R. J. (2014) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2014.03.008 · Cited by 737 · see citing works
Physiological substrates of mammalian monogamy: The prairie vole model
Sue Carter, C., Courtney Devries, A., & Getz, L. L. (1995) · Neuroscience & Biobehavioral Reviews · doi:10.1016/0149-7634(94)00070-h · Cited by 615 · see citing works
Neurobiological Sequelae of Witnessing Stressful Events in Adult Mice
Warren, B. L., Vialou, V. F., Iñiguez, S. D., Alcantara, L. F., Wright, K. N., Feng, J., Kennedy, P. J., LaPlant, Q., Shen, L., Nestler, E. J., et al. (2013) · Biological Psychiatry · doi:10.1016/j.biopsych.2012.06.006 · Cited by 222 · see citing works
Social functioning in patients with depressive and anxiety disorders
Saris, I. M. J., Aghajani, M., van der Werff, S. J. A., van der Wee, N. J. A., & Penninx, B. W. J. H. (2017) · Acta Psychiatrica Scandinavica · doi:10.1111/acps.12774 · Cited by 218 · see citing works
Behavioral effects of chronic adolescent stress are sustained and sexually dimorphic
Bourke, C. H., & Neigh, G. N. (2011) · Hormones and Behavior · doi:10.1016/j.yhbeh.2011.03.011 · Cited by 201 · see citing works
Duque-Wilckens, N., Steinman, M. Q., Busnelli, M., Chini, B., Yokoyama, S., Pham, M., Laredo, S. A., Hao, R., Perkeybile, A. M., Minie, V. A., et al. (2018) · Biological Psychiatry · doi:10.1016/j.biopsych.2017.08.024 · Cited by 181 · see citing works
Self-citationTrainor, B. C., Pride, M. C., Villalon Landeros, R., Knoblauch, N. W., Takahashi, E. Y., Silva, A. L., & Crean, K. K. (2011) · PLoS ONE · doi:10.1371/journal.pone.0017405 · Cited by 157 · see citing works
Self-citationSex-Specific Role for the Long Non-coding RNA LINC00473 in Depression
Issler, O., van der Zee, Y. Y., Ramakrishnan, A., Wang, J., Tan, C., Loh, Y.-H. E., Purushothaman, I., Walker, D. M., Lorsch, Z. S., Hamilton, P. J., et al. (2020) · Neuron · doi:10.1016/j.neuron.2020.03.023 · Cited by 156 · see citing works
Extrahypothalamic 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-citationMcNeal, N., Scotti, M.-A. L., Wardwell, J., Chandler, D. L., Bates, S. L., LaRocca, M., Trahanas, D. M., & Grippo, A. J. (2014) · Autonomic Neuroscience · doi:10.1016/j.autneu.2013.10.001 · Cited by 135 · see citing works
Orexins Mediate Sex Differences in the Stress Response and in Cognitive Flexibility
Grafe, L. A., Cornfeld, A., Luz, S., Valentino, R., & Bhatnagar, S. (2017) · Biological Psychiatry · doi:10.1016/j.biopsych.2016.10.013 · Cited by 135 · see citing works
Sex-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
Self-citationTerritoriality in Wild House Mice, Mus musculus L
Crowcroft, P. (1955) · Journal of Mammalogy · doi:10.2307/1375908 · Cited by 121 · see citing works
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. (2013) · Hormones and Behavior · doi:10.1016/j.yhbeh.2013.01.011 · Cited by 86 · see citing works
Gutzler, S. J., Karom, M., Erwin, W. D., & Albers, H. E. (2010) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2010.07190.x · Cited by 86 · see citing works
Ruscio, M. G., Sweeny, T., Hazelton, J., Suppatkul, P., & Sue Carter, C. (2007) · Hormones and Behavior · doi:10.1016/j.yhbeh.2006.08.004 · Cited by 81 · see citing works
Horie, K., Inoue, K., Suzuki, S., Adachi, S., Yada, S., Hirayama, T., Hidema, S., Young, L. J., & Nishimori, K. (2019) · Hormones and Behavior · doi:10.1016/j.yhbeh.2018.10.011 · Cited by 77 · see citing works
Sex 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
Self-citationIndividual differences in sexual responsiveness to estrogen and progesterone in ovariectomized rats
Powers, J. B., & Valenstein, E. S. (1972) · Physiology & Behavior · doi:10.1016/0031-9384(72)90093-5 · Cited by 49 · see citing works
Horie, K., Inoue, K., Nishimori, K., & Young, L. J. (2020) · Neuroscience · doi:10.1016/j.neuroscience.2020.08.023 · Cited by 46 · see citing works
Markham, C. M., Norvelle, A., & Huhman, K. L. (2009) · Behavioural Brain Research · doi:10.1016/j.bbr.2008.10.022 · Cited by 44 · see citing works
Sexual 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
Self-citation
Flagged first, then by citations
Research works printed but not linked: 134
- Akil H, Gordon J, Hen R, Javitch J, Mayberg H, McEwen B, (2018). Treatment resistant depression: A multi-scale, systems biology approach. Neurosci. Biobehav. Rev 84, 272– 288. doi: 10.1016/j.neubiorev.2017.08.019. 28859997 PMC5729118 · DOI
- Asher M, and Aderka IM (2018). Gender differences in social anxiety disorder. J. Clin. Psychol 74, 1730– 1741. doi: 10.1002/jclp.22624. 29667715 · DOI
- Avgustinovich DF, Gorbach OV, and Kudryavtseva NN (1997). Comparative analysis of anxiety-like behavior in partition and plus-maze tests after agonistic interactions in mice. Physiol. Behav 61, 37– 43. doi: 10.1016/S0031-9384(96)00303-4. 8976531 · DOI · Paper page
- Bäck S, Necarsulmer J, Whitaker LR, Coke LM, Koivula P, Heathward EJ, (2019). Neuron-Specific Genome Modification in the Adult Rat Brain Using CRISPR-Cas9 Transgenic Rats. Neuron 102, 105–119.e8. doi: 10.1016/j.neuron.2019.01.035. PMC11805586 30792150 · DOI
- Bae J, Park S, and Kwon J-W (2018). Factors associated with menstrual cycle irregularity and menopause. BMC Womens Health 18, 36. doi: 10.1186/s12905-018-0528-x. 29409520 PMC5801702 · DOI
- Beery AK, and Zucker I. (2011). Sex Bias in Neuroscience and Biomedical Research. Neurosci. Biobehav. Rev 35, 565– 572. doi: 10.1016/j.neubiorev.2010.07.002. 20620164 PMC3008499 · DOI · Paper page
- Bernhardt PC, Dabbs JM, and Fielden JA (1998). Testosterone changes during vicarious experiences of winning and losing among fans at sporting events. Physiol Behav 65, 59– 62. 9811365
- Berton O, McClung CA, DiLeone RJ, Krishnan V, Renthal W, Russo SJ, (2006). Essential Role of BDNF in the Mesolimbic Dopamine Pathway in Social Defeat Stress. Science 311, 864– 868. doi: 10.1126/science.1120972. 16469931 · DOI · Paper page
- Blanchard DC, Sakai RR, McEwen B, Weiss SM, and & Blanchard RJ (1993). Subordination stress: behavioral, brain, and neuroendocrine correlates. Behav. Brain Res 58, 113– 121. 8136039
- Bosch OJ, Nair HP, Ahern TH, Neumann ID, and Young LJ (2009). The CRF System Mediates Increased Passive Stress-Coping Behavior Following the Loss of a Bonded Partner in a Monogamous Rodent. Neuropsychopharmacology 34, 1406– 1415. doi: 10.1038/npp.2008.154. 18923404 PMC2669698 · DOI · Paper page
- Bowler CM, Cushing BS, and Sue Carter C. (2002). Social factors regulate female–female aggression and affiliation in prairie voles. Physiol. Behav 76, 559– 566. doi: 10.1016/S0031-9384(02)00755-2. 12126993 · DOI
- Bruchas MR, Schindler AG, Shankar H, Messinger DI, Miyatake M, Land BB, (2011). Selective p38a MAPK Deletion in Serotonergic Neurons Produces Stress Resilience in Models of Depression and Addiction. Neuron 71, 498– 511. 21835346 PMC3155685
- Carre J, Muir C, Belanger J, and Putnam S. (2006). Pre-competition hormonal and psychological levels of elite hockey players: Relationship to the ‘home advantage.’ Physiol. Behav 89, 392– 398. doi: 10.1016/j.physbeh.2006.07.011. 16934844 · DOI
- Chartoff EH, and Mavrikaki M. (2015). Sex Differences in Kappa Opioid Receptor Function and Their Potential Impact on Addiction. Front. Neurosci 9. doi: 10.3389/fnins.2015.00466. PMC4679873 26733781 · DOI
- Clauss JA, and Blackford JU (2012). Behavioral Inhibition and Risk for Developing Social Anxiety Disorder: A Meta-Analytic Study. J. Am. Acad. Child Adolesc. Psychiatry 51, 1066–1075.e1. doi: 10.1016/j.jaac.2012.08.002. PMC3611590 23021481 · DOI · Paper page
- Cooper MA, and Huhman KL (2010). Blocking corticotropin-releasing factor-2 receptors, but not corticotropin-releasing factor-1 receptors or glucocorticoid feedback, disrupts the development of conditioned defeat. Physiol. Behav 101, 527– 532. doi: 10.1016/j.physbeh.2010.08.003. 20705077 PMC2949480 · DOI
- Cromwell HC, and Berridge KC (1994). Mapping of globus pallidus and ventral pallidum lesions that produce hyperkinetic treading. Brain Res. 668, 16– 29. doi: 10.1016/0006-8993(94)90506-1. 7704601 · DOI
- Dalla C, Pitychoutis PM, Kokras N, and Papadopoulou-Daifoti Z. (2010). Sex Differences in Animal Models of Depression and Antidepressant Response. Basic Clin. Pharmacol. Toxicol 106, 226– 233. doi: 10.1111/j.1742-7843.2009.00516.x. 20050844 · DOI
- Davis ES, and Marler CA (2003). The progesterone challenge: steroid hormone changes following a simulated territorial intrusion in female Peromyscus californicus. Horm Behav 44, 189– 198. 14609541
- De Vries GJ, and Boyle PA (1998). Double duty for sex differences in the brain. Behav. Brain Res 92, 205– 213. doi: 10.1016/S0166-4328(97)00192-7. 9638962 · DOI · Paper page
- Donaldson ZR, and Manoli DS (2020). Blueprints for Bonding? New Genetic Tools to Parse the Neural Basis of Pair Bonding in Prairie Voles. Neuroscience 448, 311. doi: 10.1016/j.neuroscience.2020.08.038. 33092783 · DOI
- Dulka BN, Bagatelas ED, Bress KS, Grizzell JA, Cannon MK, Whitten CJ, (2020). Chemogenetic activation of an infralimbic cortex to basolateral amygdala projection promotes resistance to acute social defeat stress. Sci. Rep 10, 6884. doi: 10.1038/s41598-020-63879-8. 32327679 PMC7181792 · DOI
- Duque-Wilckens N, Steinman MQ, Laredo SA, Hao R, Perkeybile AM, Bales KL, (2016). Inhibition of vasopressin V1a receptors in the medioventral bed nucleus of the stria terminalis has sex- and context-specific anxiogenic effects. Neuropharmacology 110, 59– 68. doi: 10.1016/j.neuropharm.2016.07.018. 27452721 PMC5028294 · DOI
- Erskine MS, Barfield RJ, and Goldman BD (1978). Intraspecific fighting during late pregnancy and lactation in rats and effects of litter removal. Behav. Biol 23, 206– 218. doi: 10.1016/S0091-6773(78)91814-X. 567060 · DOI
- Fan Z, Li W, Lee SR, Meng Q, Shi B, Bunch TD, (2014). Efficient Gene Targeting in Golden Syrian Hamsters by the CRISPR/Cas9 System. PLOS ONE 9, e109755. doi: 10.1371/journal.pone.0109755. PMC4192357 25299451 · DOI
- Faruzzi AN, Solomon MB, Demas GE, and Huhman KL (2005). Gonadal hormones modulate the display of submissive behavior in socially defeated female Syrian hamsters. Horm. Behav 47, 569– 575. doi: 10.1016/j.yhbeh.2004.11.023. 15811359 · DOI
- Fava M. (2003). Diagnosis and definition of treatment-resistant depression. Biol. Psychiatry 53, 649– 659. doi: 10.1016/S0006-3223(03)00231-2. 12706951 · DOI · Paper page
- Finnell JE, Muniz BL, Padi AR, Lombard CM, Moffitt CM, Wood CS, (2018). Essential Role of Ovarian Hormones in Susceptibility to the Consequences of Witnessing Social Defeat in Female Rats. Biol. Psychiatry 84, 372– 382. doi: 10.1016/j.biopsych.2018.01.013. 29544773 PMC6067999 · DOI
- Fox NA, Henderson HA, Marshall PJ, Nichols KE, and Ghera MM (2005). Behavioral inhibition: linking biology and behavior within a developmental framework. Annu Rev Psychol 56, 235– 262. 15709935
- Fuxjager MJ, Forbes-Lorman RM, Coss DJ, Auger CJ, Auger AP, and Marler CA (2010a). Winning territorial disputes selectively enhances androgen sensitivity in neural pathways related to motivation and social aggression. Proc. Natl. Acad. Sci 107, 12393–12398. doi: 10.1073/pnas.1001394107. PMC2901436 20616093 · DOI
- Fuxjager MJ, Forbes-Lorman RM, Coss DJ, Auger CJ, Auger AP, and Marler CA (2010b). Winning territorial disputes selectively enhances androgen sensitivity in neural pathways related to motivation and social aggression. Proc. Natl. Acad. Sci 107, 12393–12398. doi: 10.1073/pnas.1001394107. PMC2901436 20616093 · DOI
- Garrett JW, and Campbell CS (1980). Changes in social behavior of the male golden hamster accompanying photoperiodic changes in reproduction. Horm Behav 14, 303– 318. 7194307
- Gattermann R, Fritzsche P, Neumann K, Al-Hussein I, Kayser A, Abiad M, (2001). Notes on the current distribution and the ecology of wild golden hamsters (Mesocricetus auratus). J. Zool 254, 359– 365. doi: 10.1017/S0952836901000851. · DOI
- Glasper ER, and DeVries AC (2005). Social structure influences effects of pair-housing on wound healing. Brain. Behav. Immun 19, 61– 68. doi: 10.1016/j.bbi.2004.03.002. 15581739 · DOI
- Gleason ED, and Marler CA (2010). Testosterone response to courtship predicts future paternal behavior in the California mouse, Peromyscus californicus. Horm. Behav 57, 147– 154. doi: 10.1016/j.yhbeh.2009.10.006. 19833131 PMC2814952 · DOI
- Gray CL, Norvelle A, Larkin T, and Huhman KL (2015). Dopamine in the nucleus accumbens modulates the memory of social defeat in Syrian hamsters (Mesocricetus auratus). Behav. Brain Res 286, 22– 28. doi: 10.1016/j.bbr.2015.02.030. 25721736 PMC4390511 · DOI
- Greenberg GD, Laman-Maharg A, Campi KL, Voigt H, Orr VN, Schaal L, (2014). Sex differences in stress-induced social withdrawal: role of brain derived neurotrophic factor in the bed nucleus of the stria terminalis. Front. Behav. Neurosci 7. doi: 10.3389/fnbeh.2013.00223. PMC3885825 24409132 · DOI · Paper page
- Grippo AJ, Cushing BS, and Carter CS (2007). Depression-like behavior and stressor-induced neuroendocrine activation in female prairie voles exposed to chronic social isolation. Psychosom. Med 69, 149– 157. doi: 10.1097/PSY.0b013e31802f054b. 17289829 PMC3006075 · DOI · Paper page
- Grippo AJ, McNeal N, Normann MC, Colburn W, Dagner A, and Woodbury M. (2020). Behavioral and neuroendocrine consequences of disrupting a long-term monogamous social bond in aging prairie voles. Stress, 1– 12. doi: 10.1080/10253890.2020.1812058. PMC7914264 32820956 · DOI
- Grippo AJ, Wu KD, Hassan I, and Carter CS (2008). Social isolation in prairie voles induces behaviors relevant to negative affect: toward the development of a rodent model focused on co-occurring depression and anxiety. Depress. Anxiety 25, E17– E26. doi: 10.1002/da.20375. 17935206 PMC2563041 · DOI
- Grissom N, and Bhatnagar S. (2009). Habituation to repeated stress: Get used to it. Neurobiol. Learn. Mem 92, 215– 224. doi: 10.1016/j.nlm.2008.07.001. 18667167 PMC2773683 · DOI · Paper page
- Gruene TM, Flick K, Stefano A, Shea SD, and Shansky RM (2015). Sexually divergent expression of active and passive conditioned fear responses in rats. eLife 4, e11352. doi: 10.7554/eLife.11352. PMC4709260 26568307 · DOI
- Haney M, Maccari S, Le Moal M, Simon H, and Vincenzo Piazza P. (1995). Social stress increases the acquisition of cocaine self-administration in male and female rats. Brain Res. 698, 46– 52. doi: 10.1016/0006-8993(95)00788-R. 8581502 · DOI
- Harris AZ, Atsak P, Bretton ZH, Holt ES, Alam R, Morton MP, (2018). A Novel Method for Chronic Social Defeat Stress in Female Mice. Neuropsychopharmacol. Off. Publ. Am. Coll. Neuropsychopharmacol 43, 1276– 1283. doi: 10.1038/npp.2017.259. PMC5916350 29090682 · DOI
- Harris BN, de Jong TR, Yang V, and Saltzman W. (2013). Chronic variable stress in fathers alters paternal and social behavior but not pup development in the biparental California mouse (Peromyscus californicus). Horm. Behav 64, 799– 811. doi: 10.1016/j.yhbeh.2013.10.007. 24157379 PMC3894746 · DOI
- Hashikawa K, Hashikawa Y, Falkner A, and Lin D. (2016). The neural circuits of mating and fighting in male mice. Curr. Opin. Neurobiol 38, 27– 37. doi: 10.1016/j.conb.2016.01.006. 26849838 PMC4921288 · DOI
- Hashikawa K, Hashikawa Y, Tremblay R, Zhang J, Feng JE, Sabol A, (2017). Esr1 + cells in the ventromedial hypothalamus control female aggression. Nat. Neurosci 20, 1580– 1590. doi: 10.1038/nn.4644. 28920934 PMC5953764 · DOI
- Henley ED, Moisset B, and Welch BL (1973). Catecholamine Uptake in Cerebral Cortex: Adaptive Change Induced by Fighting. Science 180, 1050– 1052. doi: 10.1126/science.180.4090.1050. 4735902 · DOI
- Hodes GE, Pfau ML, Purushothaman I, Ahn HF, Golden SA, Christoffel DJ, (2015). Sex differences in nucleus accumbens transcriptome profiles associated with susceptibility versus resilience to subchronic variable stress. J Neurosci 35, 16362– 16376. 26674863 PMC4679819
- Hodges TE, Baumbach JL, and McCormick CM (2018). Predictors of social instability stress effects on social interaction and anxiety in adolescent male rats. Dev. Psychobiol 60, 651– 663. doi: 10.1002/dev.21626. 29926894 · DOI
- Holly EN, Shimamoto A, DeBold JF, and Miczek KA (2012). Sex differences in behavioral and neural cross-sensitization and escalated cocaine taking as a result of episodic social defeat stress in rats. Psychopharmacology (Berl.) 224, 179– 188. 22926005 PMC3684960
- Huhman KL (2006). Social conflict models: Can they inform us about human psychopathology? Horm. Behav 50, 640– 646. doi: 10.1016/j.yhbeh.2006.06.022. 16870189 · DOI · Paper page
- Huhman KL, Solomon MB, Janicki M, Harmon AC, Lin SM, Israel JE, (2003). Conditioned defeat in male and female syrian hamsters. Horm. Behav 44, 293– 299. doi: 10.1016/j.yhbeh.2003.05.001. 14609551 · DOI · Paper page
- Hyer MM, Khantsis S, Venezia AC, Madison FN, Hallgarth L, Adekola E, (2017). Estrogen-dependent modifications to hippocampal plasticity in paternal California mice (Peromyscus californicus). Horm. Behav 96, 147– 155. doi: 10.1016/j.yhbeh.2017.09.015. 28954216 · DOI
- Iñiguez SD, Flores-Ramirez FJ, Riggs LM, Alipio JB, Garcia-Carachure I, Hernandez MA, (2018). Vicarious social defeat strress induces depression-related outcomes in female mice. Biol Psychiatry 83, 9– 17. 28888327 PMC5730407
- Jašarević E, Williams SA, Roberts RM, Geary DC, and Rosenfeld CS (2012). Spatial navigation strategies in Peromyscus: a comparative study. Anim. Behav 84, 1141– 1149. doi: 10.1016/j.anbehav.2012.08.015. 23355748 PMC3551599 · DOI
- Jasnow A, Shi C, Israel J, Davis M, and Huhman K. (2005). Memory of social defeat is facilitated by cAMP response element-binding protein overexpression in the amygdala. Behav. Neurosci 119, 1125– 30. doi: 10.1037/0735-7044.119.4.1125. 16187840 · DOI
- Johnston RE (1975). Scent marking by male golden hamsters (Mesocricetus auratus): I. Effects of odors and social encounters. Z. Für Tierpsychol 37, 75– 98. doi: 10.1111/j.1439-0310.1975.tb01128.x. 1172341 · DOI
- Johnston RE (1977). The causation of two scent-marking behaviour patterns in female hamsters (Mesocricetus auratus). Anim. Behav 25, 317– 327. doi: 10.1016/0003-3472(77)90007-0. 560812 · DOI
- Kenkel WM, Perkeybile AM, and Carter CS (2017). The neurobiological causes and effects of alloparenting. Dev. Neurobiol 77, 214– 232. doi: 10.1002/dneu.22465. 27804277 PMC5768312 · DOI
- Kiecolt-Glaser JK, Dura JR, Speicher CE, Trask OJ, and Glaser R. (1991). Spousal caregivers of dementia victims: longitudinal changes in immunity and health. Psychosom. Med 53, 345– 362. doi: 10.1097/00006842-199107000-00001. 1656478 · DOI · Paper page
- Kollack-Walker S, and Newman SW (1995). Mating and agonistic behavior produce different patters of Fos immunolabeling in the male Syrian hamster brain. Neuroscience 66, 721– 736. 7644033
- Krishnan V, Han M-H, Graham DL, Berton O, Renthal W, Russo SJ, (2007). Molecular adaptations underlying susceptibility and resistance to social defeat in brain reward regions. Cell 131, 391– 404. 17956738
- Kudryavtseva NN, Bakshtanovskaya IV, and Koryakina LA (1991). Social model of depression in mice of C57BL/6J strain. Pharmacol. Biochem. Behav 38, 315– 320. doi: 10.1016/0091-3057(91)90284-9. 2057501 · DOI · Paper page
- Laman-Maharg AR, Copeland T, Sanchez EO, Campi KL, and Trainor BC (2017). The long-term effects of stress and kappa opioid receptor activation on conditioned place aversion in male and female California mice. Behav. Brain Res 332, 299– 307. doi: 10.1016/j.bbr.2017.06.015. 28625549 PMC5563500 · DOI
- Laman-Maharg A, Williams AV, Zufelt MD, Minie VA, Ramos-Maciel S, Hao R, (2018). Sex differences in the effects of a Kappa Opioid receptor antagonist in the forced swim test. Front. Pharmacol 9. doi: 10.3389/fphar.2018.00093. PMC5817081 29491835 · DOI
- Laredo SA, Steinman MQ, Robles CF, Ferrer E, Ragen BJ, and Trainor BC (2015). Effects of defeat stress on behavioral flexibility in males and females: Modulation by the mu-opioid receptor. Eur. J. Neurosci 41. doi: 10.1111/ejn.12824. PMC4331223 25615538 · DOI · Paper page
- Lee H, Kim D-W, Remedios R, Anthony TE, Chang A, Madisen L, (2014). Scalable control of mounting and attack by Esr1 + neurons in the ventromedial hypothalamus. Nature 509, 627– 632. doi: 10.1038/nature13169. 24739975 PMC4098836 · DOI · Paper page
- Li L-F, Yuan W, He Z-X, Wang L-M, Jing X-Y, Zhang J, (2019). Involvement of oxytocin and GABA in consolation behavior elicited by socially defeated individuals in mandarin voles. Psychoneuroendocrinology 103, 14– 24. doi: 10.1016/j.psyneuen.2018.12.238. 30605804 · DOI
- Lukas M, and Neumann ID (2014). Social preference and maternal defeat-induced social avoidance in virgin female rats: sex differences in involvment of brain oxytocin and vasopressin. J Neurosci Methods 234, 101– 107. 24709115
- Mamlouk GM, Dorris DM, Barrett LR, and Meitzen J. (2020). Sex bias and omission in neuroscience research is influenced by research model and journal, but not reported NIH funding. Front. Neuroendocrinol 57, 100835. doi: 10.1016/j.yfrne.2020.100835. PMC7225067 32070715 · DOI
- Marler CA, and Trainor BC (2020). The challenge hypothesis revisited: Focus on reproductive experience and neural mechanisms. Horm. Behav 123, 104645. doi: 10.1016/j.yhbeh.2019.104645. 31778720 · DOI
- Marrocco J, Petty GH, Ríos MB, Gray JD, Kogan JF, Waters EM, (2017). A sexually dimorphic pre-stressed translational signature in CA3 pyramidal neurons of BDNF Val66Met mice. Nat. Commun 8, 808. doi: 10.1038/s41467-017-01014-4. 28993643 PMC5634406 · DOI
- Martinez M, Calvo-Torrent A, and Pico-Alfonso MA (1998). Social defeat and subordination as models of social stress in laboratory rodents: A review. Aggress. Behav 24, 241– 256. doi: 10.1002/(SICI)1098-2337(1998)24:4<241::AID-AB1>3.0.CO;2-M. · DOI
- McCann KE, Sinkiewicz DM, Rosenhauer AM, Beach LQ, and Huhman KL (2019). Transcriptomic Analysis Reveals Sex-Dependent Expression Patterns in the Basolateral Amygdala of Dominant and Subordinate Animals After Acute Social Conflict. Mol. Neurobiol 56, 3768– 3779. doi: 10.1007/s12035-018-1339-7. 30196395 PMC6408310 · DOI
- McCormick CM, Robarts D, Kopeikina K, and Kelsey JE (2005). Long-lasting, sex- and age-specific effects of social stressors on corticosterone responses to restraint and on locomotor responses to psychostimulants in rats. Horm. Behav 48, 64– 74. 15919386
- McCormick CM 2022. Methods and Challenges in Investigating Sex-Specific Consequences of Social Stressors in Adolescence in Rats: Is It the Stress or the Social or the Stage of Development? Curr Top Behav Neurosci 54, 23– 58. doi: 10.1007/7854_2021_245. 34455576 · DOI
- Meduri JD, Farnbauch LA, and Jasnow AM (2013). Paradoxical enhancement of fear expression and extinction deficits in mice resilient to social defeat. Behav. Brain Res 256, 580– 590. doi: 10.1016/j.bbr.2013.09.009. 24029700 · DOI
- Miller LR, Marks C, Becker JB, Hurn PD, Chen W-J, Woodruff T, (2017). Considering sex as a biological variable in preclinical research. FASEB J. 31, 29– 34. doi: 10.1096/fj.201600781R. 27682203 PMC6191005 · DOI
- Morrison KE, Curry DW, and Cooper MA (2012). Social status alters defeat-induced neural activation in Syrian hamsters. Neuroscience 210, 168– 178. doi: 10.1016/j.neuroscience.2012.03.002. 22433296 PMC3358589 · DOI
- Newman EL, Covington HE, Suh J, Bicakci MB, Ressler KJ, DeBold JF, (2019). Fighting Females: Neural and Behavioral Consequences of Social Defeat Stress in Female Mice. Biol. Psychiatry 86, 657– 668. doi: 10.1016/j.biopsych.2019.05.005. 31255250 PMC6788975 · DOI
- Normann MC, McNeal N, Dagner A, Ihm E, Woodbury M, and Grippo AJ (2018). The Influence of Environmental Enrichment on Cardiovascular and Behavioral Responses to Social Stress. Psychosom. Med 80, 271– 277. doi: 10.1097/PSY.0000000000000558. 29360667 PMC8283515 · DOI
- Oliveira RF, Lopos M, Carneiro LA, and Canario AVM (2001). Watching fights raises fish hormone levels. Nature 409, 784. 11206533
- Otabi H, Goto T, Okayama T, Kohari D, and Toyoda A. (2016). Subchronic and mild social defeat stress alter mouse nest building behavior. Behav. Processes 122, 21– 25. doi: 10.1016/j.beproc.2015.10.018. 26524409 · DOI
- Oyegbile TO, and Marler CA (2005). Winning fights elevates testosterone levels in California mice and enhances future ability to win fights. Horm. Behav 48, 259– 267. doi: 10.1016/j.yhbeh.2005.04.007. 15979073 · DOI
- Payne AP, and Swanson HH (1970). Agonistic Behaviour between Pairs of Hamsters of the Same and Opposite Sex in a Neutral Observation Area. Behaviour 36, 259– 269. 5531509
- Pizzuto T, and Getz LL (1998). Female prairie voles (Microtus ochrogaster) fail to form a new pair after loss of mate. Behav. Processes 43, 79– 86. doi: 10.1016/S0376-6357(97)00091-0. 24897643 · DOI · Paper page
- Pollard I, White BM, Bassett JR, and Cairncross KD (1975). Plasma glucocorticoid elevation and desynchronization of the estrous cycle following unpredictable stress in the rat. Behav. Biol 14, 103– 108. doi: 10.1016/S0091-6773(75)90374-0. 1169936 · DOI
- Potegal M, Huhman K, Moore T, and Meyerhoff J. (1993). Conditioned defeat in the Syrian golden hamster (Mesocricetus auratus). Behav. Neural Biol 60, 93– 102. doi: 10.1016/0163-1047(93)90159-F. 8117243 · DOI
- Pournajafi-Nazarloo H, Kenkel W, Mohsenpour SR, Sanzenbacher L, Saadat H, Partoo L, (2013). Exposure to chronic isolation modulates receptors mRNAs for oxytocin and vasopressin in the hypothalamus and heart. Peptides 43, 20– 26. doi: 10.1016/j.peptides.2013.02.007. 23439320 · DOI
- Prendergast BJ, Onishi KG, and Zucker I. (2014). Female mice liberated for inclusion in neuroscience and biomedical research. Neurosci Biobehav Rev 40, 1– 5. 24456941
- Pultorak JD, Fuxjager MJ, Kalcounis-Rueppell MC, and Marler CA (2015). Male fidelity expressed through rapid testosterone suppression of ultrasonic vocalizations to novel females in the monogamous California mouse. Horm. Behav 70, 47– 56. doi: 10.1016/j.yhbeh.2015.02.003. 25725427 · DOI
- Robles CF, McMackin MZ, Campi KL, Doig IE, Takahashi EY, Pride M, (2014). Effects of kappa opioid receptors on conditioned place aversion and social interaction in males and females. Behav. Brain Res 262, 84– 93. doi: 10.1016/j.bbr.2014.01.003. 24445073 PMC4073310 · DOI
- Rosenhauer AM, McCann KE, Norvelle A, and Huhman KL (2017). An acute social defeat stressor in early puberty increases susceptibility to social defeat in adulthood. Horm. Behav 93, 31– 38. doi: 10.1016/j.yhbeh.2017.04.002. 28390864 · DOI
- Rosenson LM, and Asheroff AK (1975). Maternal aggression in CD-1 mice: Influence of the hormonal condition of the intruder. Behav. Biol 15, 219– 224. doi: 10.1016/S0091-6773(75)91603-X. 1238077 · DOI
- Ross AP, Norvelle A, Choi DC, Walton JC, Albers HE, and Huhman KL (2017). Social housing and social isolation: Impact on stress indices and energy balance in male and female Syrian hamsters (Mesocricetus auratus). Physiol. Behav 177, 264– 269. doi: 10.1016/j.physbeh.2017.05.015. 28511867 PMC5538356 · DOI
- Ruscio MG, Sweeny TD, Gomez A, Parker K, and Carter CS (2009). Social Environment Alters Central Distribution of Estrogen Receptor-α in Juvenile Prairie Voles. Physiol. Behav 98, 296– 301. doi: 10.1016/j.physbeh.2009.06.005. 19539635 PMC2765375 · DOI
- Russell SE, Rachlin AB, Smith KL, Muschamp JW, Berry L, Zhao Z, (2014). Sex difference in sensitivity to the depressive-like effects of the kappa opioid receptor agonist U-50488 in rats. Biol Psychiatry 76, 213– 222. 24090794 PMC4476271
- Safronetz D, Ebihara H, Feldmann H, and Hooper JW (2012). The Syrian hamster model of hantavirus pulmonary syndrome. Antiviral Res. 95, 282– 292. doi: 10.1016/j.antiviral.2012.06.002. 22705798 PMC3425723 · DOI
- Scott JP (1966). Agonistic Behavior of Mice and Rats: A Review. Am. Zool 6, 683– 701. doi: 10.1093/icb/6.4.683. 4859807 · DOI
- Scribner JL, Vance EA, Protter DSW, Sheeran WM, Saslow E, Cameron RT, (2020). A neuronal signature for monogamous reunion. Proc. Natl. Acad. Sci. U. S. A 117, 11076–11084. doi: 10.1073/pnas.1917287117. PMC7245077 32381740 · DOI
- Shansky RM (2018). Sex differences in behavioral strategies: avoiding interpretational pitfalls. Curr. Opin. Neurobiol 49, 95– 98. doi: 10.1016/j.conb.2018.01.007. 29414071 · DOI
- Shields GS, Trainor BC, Lam JCW, and Yonelinas AP (2016). Acute stress impairs cognitive flexibility in men, not women. Stress 19. doi: 10.1080/10253890.2016.1192603. PMC5134841 27230831 · DOI
- Shimamoto A, Debold JF, Holly EN, and Miczek KA (2011). Blunted accumbal dopamine response to cocaine following chronic social stress in female rats: exploring a link between depression and drug abuse. Psychopharmacology (Berl.) 218, 271– 279. doi: 10.1007/s00213-011-2364-7. 21638221 PMC3901580 · DOI · Paper page
- Sial OK, Warren BL, Alcantara LF, Parise EM, and Bolaños-Guzmán CA (2016). Vicarious social defeat stress: Bridging the gap between physical and emotional stress. J. Neurosci. Methods 258, 94– 103. doi: 10.1016/j.jneumeth.2015.10.012. 26545443 PMC4691556 · DOI
- Siegel HI (1985). The Hamster: Reproduction and Behavior. Springer Science & Business Media.
- Smith AS, Lieberwirth C, and Wang Z. (2013). Behavioral and physiological responses of female prairie voles (Microtus ochrogaster) to various stressful conditions. Stress 16, 531– 539. doi: 10.3109/10253890.2013.794449. 23647082 PMC3947756 · DOI
- Solomon MB (2017). Evaluating social defeat as a model for psychopathology in adult female rodents. J. Neurosci. Res 95, 763– 776. doi: 10.1002/jnr.23971. 27870445 · DOI
- Solomon MB, Karom MC, and Huhman KL (2007). Sex and estrous cycle differences in the display of conditioned defeat in Syrian hamsters. Horm. Behav 52, 211– 219. doi: 10.1016/j.yhbeh.2007.04.007. 17555756 · DOI
- Steinman MQ, Duque-Wilckens N, and Trainor BC (2019). Complementary Neural Circuits for Divergent Effects of Oxytocin: Social Approach Versus Social Anxiety. Biol. Psychiatry 85, 792– 801. doi: 10.1016/j.biopsych.2018.10.008. 30503164 PMC6709863 · DOI · Paper page
- Steinman MQ, Laredo SA, Lopez EM, Manning CE, Hao RC, Doig IE, (2015). Hypothalamic vasopressin systems are more sensitive to the long term effects of social defeat in males versus females. Psychoneuroendocrinology 51. doi: 10.1016/j.psyneuen.2014.09.009. PMC4268083 25306217 · DOI · Paper page
- Stroebe M, Schut H, and Stroebe W. (2007). Health outcomes of bereavement. The Lancet 370, 1960– 1973. doi: 10.1016/S0140-6736(07)61816-9. 18068517 · DOI · Paper page
- Svare B, and Gandelman R. (1973). Postpartum aggression in mice: Experiential and environmental factors. Horm. Behav 4, 323– 334. doi: 10.1016/0018-506X(73)90032-9. 1035202 · DOI
- Takahashi A, Chung J-R, Zhang S, Zhang H, Grossman Y, Aleyasin H, (2017). Establishment of a repeated social defeat stress model in female mice. Sci. Rep 7, 12838. doi: 10.1038/s41598-017-12811-8. PMC5634448 28993631 · DOI · Paper page
- Tannenbaum C, Schwarz JM, Clayton JA, de Vries GJ, and Sullivan C. (2016). Evaluating sex as a biological variable in preclinical research: the devil in the details. Biol. Sex Differ 7. doi: 10.1186/s13293-016-0066-x. PMC4750169 26870316 · DOI
- Tickerhoof MC, Hale LH, Butler MJ, and Smith AS (2019). Regulation of defeat-induced social avoidance by medial amygdala DRD1 in male and female prairie voles. Psychoneuroendocrinology 113. doi: 10.1016/j.psyneuen.2019.104542. 31862611 · DOI
- Tidey JW, and Miczek KA (1996). Social defeat stress selectively alters mesocorticolimbic dopamine release: an in vivo microdialysis study. Brain Res. 721, 140– 149. doi: 10.1016/0006-8993(96)00159-x. 8793094 · DOI · Paper page
- Tornatzky W, and Miczek KA (1993). Long-term impairment of autonomic circadian rhythms after brief intermittent social stress. Physiol. Behav 53, 983– 993. doi: 10.1016/0031-9384(93)90278-N. 8511216 · DOI · Paper page
- Trainor BC, Takahashi EY, Silva AL, Crean KK, and Hostetler C. (2010). Sex differences in hormonal responses to social conflict in the monogamous California mouse. Horm. Behav 58, 506– 512. doi: 10.1016/j.yhbeh.2010.04.008. 20430027 PMC2917544 · DOI
- Ver Hoeve ES, Kelly G, Luz S, Ghanshani S, and Bhatnagar S. (2013). Short-term and long-term effects of repeated social defeat during adolescence or adulthood in female rats. Neuroscience 249, 63– 73. doi: 10.1016/j.neuroscience.2013.01.073. 23402852 PMC3743933 · DOI
- Walker DM, Zhou X, Ramakrishnan A, Cates HM, Cunningham AM, Peña CJ, (2020). Adolescent Social Isolation Reprograms the Medial Amygdala: Transcriptome and Sex Differences in Reward. bioRxiv, 2020.02.18.955187. doi: 10.1101/2020.02.18.955187. · DOI
- Wang L, Hou W, He Z, Yuan W, Yang J, Yang Y, (2018). Effects of chronic social defeat on social behaviors in adult female mandarin voles (Microtus mandarinus): Involvement of the oxytocin system in the nucleus accumbens. Prog. Neuropsychopharmacol. Biol. Psychiatry 82, 278– 288. doi: 10.1016/j.pnpbp.2017.11.002. 29126982 · DOI
- Wang L, Zhu Z, Hou W, Zhang X, He Z, Yuan W, (2019). Serotonin Signaling Trough Prelimbic 5-HT1A Receptors Modulates CSDS-Induced Behavioral Changes in Adult Female Voles. Int. J. Neuropsychopharmacol 22, 208– 220. doi: 10.1093/ijnp/pyy093. 30445535 PMC6403097 · DOI
- Warren BL, Mazei-Robison M, Robison AJ, and Iñiguez SD (2020). Can I get a witness? Using vicarious defeat stress to study mood-related illnesses in traditionally understudied populations. Biol. Psychiatry 0. doi: 10.1016/j.biopsych.2020.02.004. PMC7725411 32228871 · DOI
- Weintraub A, Singaravelu J, and Bhatnagar S. (2010). Enduring and sex-specific effects of adolescent social isolation in rats on adult stress reactivity. Brain Res. 1343, 83– 92. doi: 10.1016/j.brainres.2010.04.068. 20438720 · DOI
- Williams AV, Duque-Wilckens N, Ramos-Maciel S, Campi KL, Bhela SK, Xu CK, (2020a). Social approach and social vigilance are differentially regulated by oxytocin receptors in the nucleus accumbens. Neuropsychopharmacology 45, 1423– 1430. doi: 10.1038/s41386-020-0657-4. 32198453 PMC7360746 · DOI
- Williams AV, Laman-Maharg A, Armstrong CV, Ramos-Maciel S, Minie VA, and Trainor BC (2018). Acute inhibition of kappa opioid receptors before stress blocks depression-like behaviors in California mice. Prog. Neuropsychopharmacol. Biol. Psychiatry 86, 166– 174. doi: 10.1016/j.pnpbp.2018.06.001. 29879438 PMC6054130 · DOI
- Williams AV, and Trainor BC (2018). The impact of sex as a biological variable in the search for novel antidepressants. Front. Neuroendocrinol 50, 107– 117. doi: 10.1016/j.yfrne.2018.05.003. 29859882 PMC6139050 · DOI
- Williams ES, Manning CE, Eagle AL, Swift-Gallant A, Duque-Wilckens N, Chinnusamy S, (2020b). Androgen-Dependent Excitability of Mouse Ventral Hippocampal Afferents to Nucleus Accumbens Underlies Sex-Specific Susceptibility to Stress. Biol. Psychiatry 87, 492– 501. doi: 10.1016/j.biopsych.2019.08.006. 31601425 PMC7035179 · DOI · Paper page
- Wood SK, Walker HE, Valentino RJ, and Bhatnagar S. (2010). Individual differences in reactivity to social stress predict susceptibility and resilience to a depressive phenotype: role of corticotropin-releasing factor. Endocrinology 151, 1795– 1805. doi: 10.1210/en.2009-1026. 20160137 PMC2850230 · DOI · Paper page
- Wright EC, Culkin HI, Sekar S, Kapoor A, Corbett C, and Trainor BC (2020). Pubertal Androgens Reduce the Effects of Social Stress on Anxiety-related Behaviors in California Mice. Developmental Biology doi: 10.1101/2020.12.02.408526. · DOI
- Yang M, Silverman JL, and Crawley JN (2011). Automated Three-Chambered Social Approach Task for Mice. Curr. Protoc. Neurosci 56, 8.26.1–8.26.16. doi: 10.1002/0471142301.ns0826s56. PMC4904775 21732314 · DOI · Paper page
- Yin W, Gallagher NR, Sawicki CM, McKim DB, Godbout JP, and Sheridan JF (2019). Repeated social defeat in female mice induces anxiety-like behavior associated with enhanced myelopoiesis and increased monocyte accumulation in the brain. Brain. Behav. Immun 78, 131– 142. doi: 10.1016/j.bbi.2019.01.015. 30684650 PMC6488440 · DOI
- Yohn CN, Dieterich A, Bazer AS, Maita I, Giedraitis M, and Samuels BA (2019). Chronic non-discriminatory social defeat is an effective chronic stress paradigm for both male and female mice. Neuropsychopharmacology 44, 2220– 2229. doi: 10.1038/s41386-019-0520-7. 31493767 PMC6898575 · DOI
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Self-citation
- Authors
- Kuske, J. X., & Trainor, B. C.
- Affiliations
- University of California, Davis (US)
- Corresponding author
- Trainor, Brian C.
- ORCID
- Trainor, Brian C.
- Venue
- Current Topics in Behavioral Neurosciences
- Publisher
- Springer International Publishing
- Published
- 2021
- Volume
- 54
- Pages
- 95-124
- ISSN
- 1866-3370 (ISSN-L)
- 1866-3389
- PMC
- PMC9812211
- OpenAlex
- W3199169544
- Cited by
- 27
- References
- 28
- Citations by year
- 2026: 4 · 2025: 4 · 2024: 10 · 2023: 2 · 2022: 7
- FWCI
- 11.88
- Type
- book chapter
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Current topics in behavioral neurosciences (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- Funders
- National Institute of Mental Health (R01MH121829)
- Topics
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Keywords
- social stress, female rodents, social defeat stress, sex differences, depression, anxiety, rodent models, neural circuits, sex bias in research
- MeSH terms
- Animals, Anxiety, Anxiety Disorders, Female, Humans, Male, Rodentia, Social Behavior, Stress, Psychological
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