Stress, social behavior, and resilience: Insights from rodents

Neurobiology of Stress

Volumn 1, Issue 1, 2015, Pages 116-127

  Beery, Annaliese K ^a   Kaufer, Daniela ^b  

^a SMITH COLLEGE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Anxiety; Social behavior; Social buffering; Social stress; Sociality; Stress

Indexed keywords

ARGIPRESSIN; BRAIN DERIVED NEUROTROPHIC FACTOR; CORTICOTROPIN; CORTICOTROPIN RELEASING FACTOR; GLUCOCORTICOID; GLYCOGEN SYNTHASE KINASE 3BETA; OXYTOCIN; OXYTOCIN RECEPTOR;

ADAPTIVE BEHAVIOR; ANXIETY; ARTICLE; CROWDING (AREA); DEPRESSION; DISEASE PREDISPOSITION; IMMOBILIZATION STRESS; MATERNAL BEHAVIOR; MATING; NEUROTRANSMISSION; NONHUMAN; PERSONAL EXPERIENCE; POSTTRAUMATIC STRESS DISORDER; PRIORITY JOURNAL; PSYCHOLOGICAL WELL BEING; PSYCHOSOCIAL WITHDRAWAL; RESILIENCE; RODENT; SEX DIFFERENCE; SOCIAL AVOIDANCE BEHAVIOR; SOCIAL BEHAVIOR; SOCIAL DOMINANCE; SOCIAL ENVIRONMENT; SOCIAL INTERACTION; SOCIAL INTERACTION TEST; SOCIAL ISOLATION; SOCIAL REJECTION; SOCIAL STRESS; SPECIES DIVERSITY; STOMACH ULCER; STRESS; WOUND HEALING;

EID: 84921930571     PISSN: None     EISSN: 23522895     Source Type: Journal    
DOI: 10.1016/j.ynstr.2014.10.004     Document Type: Review

References (249)

1. Abbott, D., Keverne, E., Bercovitch, F., Shively, C., Mendoza, S., Saltzman, W., Snowdon, C., Ziegler, T., Banjevic, M., Garlandm, T., Sapolsky, R., 2003. Are subordinates always stressed? a comparative analysis of rank differences in cortisol levels among primates. Horm. Behav. 43, 67-82.
2. Adler, N.E., Boyce, T., Chesney, M.A., Cohen, S., Folkman, S., Kahn, R.L., Leonard, S., 1994. Socioeconomic status and health: the challenge of the gradient. Am. Psychol. 49, 15-24.
3. Adrian, O., Kaiser, S., Sachser, N., Jandewerth, P., Löttker, P., Epplen, J.T., Hennessy, M.B., 2008. Female influences on pair formation, reproduction and male stress responses in a monogamous cavy (Galea monasteriensis). Horm. Behav. 53, 403-412.
4. Ahern, T.H., Young, L.J., 2009. The impact of early life family structure on adult social attachment, alloparental behavior, and the neuropeptide systems regulating affiliative behaviors in the monogamous prairie vole (Microtus ochrogaster). Front. Behav. Neurosci. 3, 17.
5. Amat, J., Aleksejev, R.M., Paul, E., Watkins, L.R., Maier, S.F., 2010. Behavioral control over shock blocks behavioral and neurochemical effects of later social defeat. Neuroscience 165, 1031-1038.
6. American Psychiatric Association, 2013. Diagnostic and Statistical Manual of Mental Disorders, fifth ed. American Psychiatric Publishing, Washington, D.C. DSM-5.
7. Anacker, A.M.J., Beery, A.K., 2013. Life in groups: the roles of oxytocin in mammalian sociality. Front. Behav. Neurosci. 7, 185.
8. Anacker, A.M.J., Loftis, J.M., Kaur, S., Ryabinin, A.E., 2011. Prairie voles as a novel model of socially facilitated excessive drinking. Addict. Biol. 16, 92-107.
9. Anacker, A.M.J., Reitz, K.M., Gunzel, E.R., Beery, A.K., 2014. Stress inhibits partner preference in same-sex pairs of female meadow voles. Program No 64112PP14 2014 Neurosci Meet Plan Wash DC Soc Neurosci 2014 Online.
10. Aragona, B.J., 2009. Dopamine regulation of social choice in a monogamous rodent species. Available at: Front. Behav. Neurosci. 3 http://www.frontiersin.org/Journal/10.3389/neuro.08.015.2009/full (accessed 28.02.14.).
11. Araya-Callís, C., Hiemke, C., Abumaria, N., Flugge, G., 2012. Chronic psychosocial stress and citalopram modulate the expression of the glial proteins GFAP and NDRG2 in the hippocampus. Psychopharmacology (Berl) 224, 209-222.
12. Armario, A., Luna, G., Balasch, J., 1983a. The effect of conspecifics on corticoadrenal response of rats to a novel environment. Behav. Neural Biol. 37, 332-337.
13. Armario, A., Ortiz, R., Balasch, J., 1983b. Corticoadrenal and behavioral response to open field in pairs of male rats either familiar or non-familiar to each other. Experientia 39, 1316-1317.
14. Bale, T.L., Vale, W.W., 2004. CRF and CRF Receptors: role in stress responsivity and other behaviors. Annu. Rev. Pharmacol. Toxicol. 44, 525-557.
15. Bales, K.L., Carter, C.S., 2003. Sex differences and developmental effects of oxytocin on aggression and social behavior in prairie voles (Microtus ochrogaster). Horm. Behav. 44, 178-184.
16. Bangasser, D.A., Valentino, R.J., 2014. Sex differences in stress-related psychiatric disorders: neurobiological perspectives. Front. Neuroendocrinol. 35, 303-319.
17. Bartolomucci, A., Carola, V., Pascucci, T., Puglisi-Allegra, S., Cabib, S., Lesch, K.-P., Parmigiani, S., Palanza, P., Gross, C., 2010. Increased vulnerability to psychosocial stress in heterozygous serotonin transporter knockout mice. Dis. Model. Mech. 3, 459-470.
18. Baum, M., 1969. Extinction of an avoidance response motivated by intense fear: social facilitation of the action of response prevention (flooding) in rats. Behav. Res. Ther. 7, 57-62.
19. Beery, A.K., Francis, D.D., 2011. Adaptive significance of natural variations in maternal care in rats: a translational perspective. Neurosci. Biobehav. Rev. 35, 1552-1561.
20. Beery, A.K., Lacey, E.A., Francis, D.D., 2008a. Oxytocin and vasopressin receptor distributions in a solitary and a social species of tuco-tuco (Ctenomys haigi and Ctenomys sociabilis). J. Comp. Neurol. 507, 1847-1859.
21. Beery, A.K., Lin, J., Biddle, J.S., Francis, D.D., Blackburn, E.H., Epel, E.S., 2012. Chronic stress elevates telomerase activity in rats. Biol. Lett. 8, 1063-1066.
22. Beery, A.K., Loo, T.J., Zucker, I., 2008b. Day length and estradiol affect same-sex affiliative behavior in the female meadow vole. Horm. Behav. 54, 153-159.
23. Beery, A.K., Routman, D.M., Zucker, I., 2009. Same-sex social behavior in meadow voles: multiple and rapid formation of attachments. Physiol. Behav. 97, 52-57.
24. Beery, A.K., Vahaba, D.M., Grunberg, D.M., 2014. Corticotropin-releasing factor receptor densities vary with photoperiod and sociality. Horm. Behav. Available at: http://dx.doi.org/10.1016/j.yhbeh.2014.08.014 http://www.sciencedirect.com/science/article/pii/S0018506X14002001 (accessed 26.10.14).
25. Beery, A.K., Zucker, I., 2010. Oxytocin and same-sex social behavior in female meadow voles. Neuroscience 169, 665-673.
26. Beery, A.K., Zucker, I., 2011. Sex bias in neuroscience and biomedical research. Neurosci. Biobehav. Rev. 35, 565-572.
27. Ben-Ami Bartal, I., Decety, J., Mason, P., 2011. Empathy and pro-social behavior in rats. Science 334, 1427-1430.
28. Ben-Ami Bartal, I., Rodgers, D.A., Bernardez Sarria, M.S., Decety, J., Mason, P., 2014. Pro-social behavior in rats is modulated by social experience. eLife 3. Available at: http://elife.elifesciences.org/content/3/e01385.abstract (accessed 28.07.14.).
29. Berkman, L.F., Kawachi, I., 2000. Social Epidemiology. Oxford University Press.
30. Berton, O., McClung, C.A., DiLeone, R.J., Krishnan, V., Renthal, W., Russo, S.J., Graham, D., Tsankova, N.M., Bolanos, C.A., Rios, M., Monteggia, L.M., Self, D.W., Nestler, E.J., 2006. Essential role of BDNF in the mesolimbic dopamine pathway in social defeat stress. Science 311, 864-868.
31. Blanchard, D.C., Spencer, R.L., Weiss, S.M., Blanchard, R.J., McEwen, B., Sakai, R.R., 1995. Visible burrow system as a model of chronic social stress: behavioral and neuroendocrine correlates. Psychoneuroendocrinology 20, 117-134.
32. Blanchard, R.J., Hebert, M., Sakai, R.R., McKittrick, C., Henrie, A., Yudko, E., McEwen, B.S., Blanchard, D.C., 1998. Chronic social stress: changes in behavioral and physiological indices of emotion. Aggress. Behav. 24, 307-321.
33. Blanchard, R.J., McKittrick, C.R., Blanchard, D.C., 2001. Animal models of social stress: effects on behavior and brain neurochemical systems. Physiol. Behav. 73, 261-271.
34. Boonstra, R., Boag, P.T., 1992. Spring declines in Microtus pennsylvanicus and the role of steroid hormones. J. Anim. Ecol. 61, 339-352.
35. Bosch, O.J., Nair, H.P., Ahern, T.H., Neumann, I.D., Young, L.J., 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.
36. Botelho, S., Estanislau, C., Morato, S., 2007. Effects of under- and overcrowding on exploratory behavior in the elevated plus-maze. Behav. Process. 74, 357-362.
37. Bowen, M.T., Keats, K., Kendig, M.D., Cakic, V., Callaghan, P.D., McGregor, I.S., 2012. Aggregation in quads but not pairs of rats exposed to cat odor or bright light. Behav. Process. 90, 331-336.
38. Bowen, M.T., McGregor, I.S., 2014. Oxytocin and vasopressin modulate the social response to threat: a preclinical study. Int. J. Neuropsychopharmacol. 1-13.
39. Brain, P.F., 1972. Effects of isolation/grouping on endocrine function and fighting behavior in male and female golden hamsters. (Mesocricetus auratus Waterhouse. Behav. Biol. 7, 349-357.
40. Braun, K., Antemano, R., Helmeke, C., Büchner, M., Poeggel, G., 2009. Juvenile separation stress induces rapid region- and layer-specific changes in S100ss- and glial fibrillary acidic protein-immunoreactivity in astrocytes of the rodent medial prefrontal cortex. Neuroscience 160, 629-638.
41. Brown, K.J., Grunberg, N.E., 1995. Effects of housing on male and female rats: crowding stresses males but calms females. Physiol. Behav. 58, 1085-1089.
42. Buwalda, B., Felszeghy, K., Horváth, K.M., Nyakas, C., de Boer, S.F., Bohus, B., Koolhaas, J.M., 2001. Temporal and spatial dynamics of corticosteroid receptor down-regulation in rat brain following social defeat. Physiol. Behav. 72, 349-354.
43. Buwalda, B., Kole, M.H.P., Veenema, A.H., Huininga, M., de Boer, S.F., Korte, S.M., Koolhaas, J.M., 2005. Long-term effects of social stress on brain and behavior: a focus on hippocampal functioning. Neurosci. Biobehav. Rev. 29, 83-97.
44. Cahill, L., 2006. Why sex matters for neuroscience. Nat. Rev. Neurosci. 7, 477-484.
45. Calcagnoli, F., de Boer, S.F., Beiderbeck, D.I., Althaus, M., Koolhaas, J.M., Neumann, I.D., 2014. Local oxytocin expression and oxytocin receptor binding in the male rat brain is associated with aggressiveness. Behav. Brain Res. 261, 315-322.
46. Campbell, P., Ophir, A.G., Phelps, S.M., 2009. Central vasopressin and oxytocin receptor distributions in two species of singing mice. J. Comp. Neurol. 516, 321-333.
47. Carnevali, L., Mastorci, F., Graiani, G., Razzoli, M., Trombini, M., Pico-Alfonso, M.A., Arban, R., Grippo, A.J., Quaini, F., Sgoifo, A., 2012. Social defeat and isolation induce clear signs of a depression-like state, but modest cardiac alterations in wild-type rats. Physiol. Behav. 106, 142-150.
48. Carter, C.S., 1998. Neuroendocrine perspectives on social attachment and love. Psychoneuroendocrinology 23, 779-818.
49. Carter, C.S., 2007. Sex differences in oxytocin and vasopressin: Implications for autism spectrum disorders? Behav. Brain Res. 176, 170-186.
50. Carter, C.S., DeVries, A.C., Taymans, S.E., Roberts, R.L., Williams, J.R., Chrousos, G.P., 1995. Adrenocorticoid hormones and the development and expression of mammalian monogamy. Ann. N.Y. Acad. Sci. 771, 82-91.
51. Carter, C.S., Grippo, A.J., Pournajafi-Nazarloo, H., Ruscio, M.G., Porges, S.W., 2008. Oxytocin, vasopressin and sociality. Prog. Brain Res. 170, 331-336.
52. Chetty, S., Friedman, A.R., Taravosh-Lahn, K., Kirby, E.D., Mirescu, C., Guo, F., Krupik, D., Nicholas, A., Geraghty, A.C., Krishnamurthy, A., Tsai, M.-K., Covarrubias, D., Wong, A.T., Francis, D.D., Sapolsky, R.M., Palmer, T.D., Pleasure, D., Kaufer, D., 2014. Stress and glucocorticoids promote oligodendrogenesis in the adult hippocampus. Mol. Psychiatry. http://dx.doi.org/10.1038/mp.2013.190 (Epub ahead of print).
53. Cho, M.M., DeVries, A.C., Williams, J.R., Carter, C.S., 1999. The effects of oxytocin and vasopressin on partner preferences in male and female prairie voles (Microtus ochrogaster). Behav. Neurosci. 113, 1071.
54. Choleris, E., Gustafsson, J.-A.A., Korach, K.S., Muglia, L.J., Pfaff, D.W., Ogawa, S., 2003. An estrogen-dependent four-gene micronet regulating social recognition: a study with oxytocin and estrogen receptor-alpha and -beta knockout mice. Proc. Natl. Acad. Sci. U.S.A. 100, 6192-6197.
55. Chou, D., Huang, C.-C., Hsu, K.-S., 2014. Brain-derived neurotrophic factor in the amygdala mediates susceptibility to fear conditioning. Exp. Neurol. 255, 19-29.
56. Christian, J.J., 1971. Population density and reproductive efficiency. Biol. Reprod. 4, 248-294.
57. Christian, J.J., Lemunyan, C.D., 1958. Adverse effects of crowding on lacation and reproduction of mice and two generations of their progeny. Endocrinology 63, 517-529.
58. Coe, C.L., Mendoza, S.P., Smotherman, W.P., Levine, S., 1978. Mother-infant attachment in the squirrel monkey: adrenal response to separation. Behav. Biol. 22, 256-263.
59. Conger, J.J., Sawrey, W.L., Turrell, E.S., 1958. The role of social experience in the production of gastric ulcers in hooded rats placed in a conflict situation. J. Abnorm. Soc. Psychol. 57, 214-220.
60. Cordero, M.I., Sandi, C., 2007. Stress amplifies memory for social hierarchy. Front. Neurosci. 1, 175-184.
61. Couzin-Frankel, J., 2014. Needed: more females in animal and cell studies. Science 344, 679.
62. Clarke, F.M., Faulkes, C.G., 1997. Dominance and queen succession in captive colonies of the eusocial naked moleerat, Heterocephalus glaber. Proc. R. Soc. Lond. B. Biol. Sci. 264, 993-1000.
63. Clarke, F.M., Faulkes, C.G., 2001. Intracolony aggression in the eusocial naked molerat, Heterocephalus glaber. Anim. Behav. 61, 311-324.
64. Clayton, J.A., Collins, F.S., 2014. Policy: NIH to balance sex in cell and animal studies. Nature 509, 282-283.
65. Crawley, J.N., 2007. Social behavior tests for mice. Available at: http://ccsystems.us/v2mag/L018.pdf (accessed 05.08.14.).
66. Czéh, B., Michaelis, T., Watanabe, T., Frahm, J., de Biurrun, G., van Kampen, M., Bartolomucci, A., Fuchs, E., 2001. Stress-induced changes in cerebral metabolites, hippocampal volume, and cell proliferation are prevented by antidepressant treatment with tianeptine. Proc. Natl. Acad. Sci. U.S.A. 98, 12796-12801.
67. Davitz, J.R., Mason, D.J., 1955. Socially facilitated reduction of a fear response in rats. J. Comp. Physiol. Psychol. 48, 149-151.
68. Detillion, C.E., Craft, T.K.S., Glasper, E.R., Prendergast, B.J., DeVries, A.C., 2004. Social facilitation of wound healing. Psychoneuroendocrinology 29, 1004-1011.
69. DeVries, A.C., 2002. Interaction among social environment, the hypothalamicepituitaryeadrenal axis, and behavior. Horm. Behav. 41, 405-413.
70. DeVries, A.C., DeVries, M.B., Taymans, S., Carter, C.S., 1995. Modulation of pair bonding in female prairie voles (Microtus ochrogaster) by corticosterone. Proc. Natl. Acad. Sci. U.S.A. 92, 7744-7748.
71. DeVries, A.C., DeVries, M.B., Taymans, S.E., Carter, C.S., 1996. The effects of stress on social preferences are sexually dimorphic in prairie voles. Proc. Natl. Acad. Sci. U.S.A. 93, 11980-11984.
72. DeVries, A.C., Glasper, E.R., Detillion, C.E., 2003. Social modulation of stress responses. Physiol. Behav. 79, 399-407.
73. DeVries, A.C., Guptaa, T., Cardillo, S., Cho, M., Carter, C.S., 2002. Corticotropinreleasing factor induces social preferences in male prairie voles. Psychoneuroendocrinology 27, 705-714.
74. DeVries, A.C., Taymans, S.E., Carter, C.S., 1997. Social modulation of corticosteroid responses in male prairie voles. Ann. N.Y. Acad. Sci. 807, 494-497.
75. Dewsbury, D.A., 1984. Aggression, copulation, and differential reproduction of deer mice (Peromyscus maniculatus) in a semi-natural enclosure. Behaviour 91, 1-23.
76. Donahue, R.J., Muschamp, J.W., Russo, S.J., Nestler, E.J., Carlezon, W.A., 2014. Effects of striatal DFosB overexpression and ketamine on social defeat stress-induced anhedonia in mice. Biol. Psychiatry. http://dx.doi.org/10.1016/j.biopsych.2013.12.014.
77. Donaldson, Z.R., Young, L.J., 2008. Oxytocin, vasopressin, and the neurogenetics of sociality. Science 322, 900-904.
78. Elliott, E., Ezra-Nevo, G., Regev, L., Neufeld-Cohen, A., Chen, A., 2010. Resilience to social stress coincides with functional DNA methylation of the Crf gene in adult mice. Nat. Neurosci. 13, 1351-1353.
79. Engh, A.L., Beehner, J.C., Bergman, T.J., Whitten, P.L., Hoffmeier, R.R., Seyfarth, R.M., Cheney, D.L., 2006. Behavioural and hormonal responses to predation in female chacma baboons (Papio hamadryas ursinus). Proc. Biol. Sci. 273, 707-712.
80. Everts, H.G.J., De Ruiter, A.J.H., Koolhaas, J.M., 1997. Differential lateral septal vasopressin in wild-type rats: correlation with aggression. Horm. Behav. 31, 136-144.
81. Ferguson, J.N., Young, L.J., Insel, T.R., 2002. The neuroendocrine basis of social recognition. Front. Neuroendocr 23, 200-224.
82. File, S.E., Hyde, J.R., 1978. Can social interaction be used to measure anxiety? Br. J. Pharmacol. 62, 19-24.
83. Füchsl, A.M., Neumann, I.D., Reber, S.O., 2013. Stress resilience: a low-anxiety genotype protects male mice from the consequences of chronic psychosocial stress. Endocrinology 155, 117-126.
84. Gadek-Michalska, A., Bugajski, J., 2003. Repeated handling, restraint, or chronic crowding impair the hypothalamic-pituitary-adrenocortical response to acute restraint stress. J. Physiol. Pharmacol. Off. J. Pol. Physiol. Soc. 54, 449-459.
85. Galea, L.A., McEwen, B.S., 1999. Sex and seasonal differences in the rate of cell proliferation in the dentate gyrus of adult wild meadow voles. Neuroscience 89, 955-964.
86. Gamallo, A., Villanua, A., Trancho, G., Fraile, A., 1986. Stress adaptation and adrenal activity in isolated and crowded rats. Physiol. Behav. 36, 217-221.
87. Gattermann, R., Fritzsche, P., Neumann, K., Al-Hussein, I., Kayser, A., Abiad, M., Yakti, R., 2001. Notes on the current distribution and the ecology of wild golden hamsters (Mesocricetus auratus). J. Zool. 254, 359-365.
88. Geraghty, A.C., Muroy, S., Zhao, S., Kriegsfeld, L.J., Bentley, G.E., Kaufer, D., 2013. Chronic stress causes an increase in RFRP expression and leads to reproductive dysfunction in the adult female rat. Program No 37504III1 2013 Neurosci Meet Plan Wash DC Soc Neurosci 2013 Online.
89. Germann, P.G., Kohler, M., Ernst, H., Baumgart, H., Mohr, U., 1990. The relation of amyloidosis to social stress induced by crowding in the Syrian hamster (Mesocricetus auratus). Z. Für Vers. 33, 271-275.
90. Getz, L.L., Carter, C.S., Gavish, L., 1981. The mating system of the prairie vole, Microtus ochrogaster: field and laboratory evidence for pair-bonding. Behav. Ecol. Sociobiol. 8, 189-194.
91. Getz, L.L., Hofmann, J.E., 1986. Social organization in free-living prairie voles, Microtus ochrogaster. Behav. Ecol. Sociobiol. 18, 275-282.
92. Glasper, E.R., DeVries, A.C., 2005. Social structure influences effects of pair-housing on wound healing. Brain Behav. Immunol. 19, 61-68.
93. Gonzalez, A., Lovic, V., Ward, G.R., Wainwright, P.E., Fleming, A.S., 2001. Intergenerational effects of complete maternal deprivation and replacement stimulation on maternal behavior and emotionality in female rats. Dev. Psychobiol. 38, 11-32.
94. Gouin, J.-P., Carter, C.S., Pournajafi-Nazarloo, H., Glaser, R., Malarkey, W.B., Loving, T.J., Stowell, J., Kiecolt-Glaser, J.K., 2010. Marital behavior, oxytocin, vasopressin, and wound healing. Psychoneuroendocrinology 35, 1082-1090.
95. Gould, E., Tanapat, P., McEwen, B.S., Flügge, G., Fuchs, E., 1998. Proliferation of granule cell precursors in the dentate gyrus of adult monkeys is diminished by stress. Proc. Natl. Acad. Sci. U.S.A. 95, 3168-3171.
96. Graves, F.C., Hennessy, M.B., 2000. Comparison of the effects of the mother and an unfamiliar adult female on cortisol and behavioral responses of pre- and postweaning guinea pigs. Dev. Psychobiol. 36, 91-100.
97. Grippo, A.J., Carter, C.S., McNeal, N., Chandler, D.L., LaRocca, M.A., Bates, S.L., Porges, S.W., 2011. 24-Hour autonomic dysfunction and depressive behaviors in an animal model of social isolation: implications for the study of depression and cardiovascular disease. Psychosom. Med. 73, 59-66.
98. Grippo, A.J., Ihm, E., Wardwell, J., McNeal, N., Scotti, M.-A.L., Moenk, D.A., Chandler, D.L., LaRocca, M.A., Preihs, K., 2014. The effects of environmental enrichment on depressive and anxiety-relevant behaviors in socially isolated prairie voles. Psychosom. Med. 76, 277-284.
99. Grippo, A.J., Lamb, D.G., Carter, C.S., Porges, S.W., 2007. Social isolation disrupts autonomic regulation of the heart and influences negative affective behaviors. Biol. Psychiatry 62, 1162-1170.
100. Grippo, A.J., Sgoifo, A., Mastorci, F., McNeal, N., Trahanas, D.M., 2010. Cardiac dysfunction and hypothalamic activation during a social crowding stressor in prairie voles. Auton. Neurosci. 156, 44-50.
101. Grippo, A.J., Trahanas, D.M., Zimmerman, R.R., Porges, S.W., Carter, C.S., 2009. Oxytocin protects against negative behavioral and autonomic consequences of long-term social isolation. Psychoneuroendocrinology 34, 1542-1553.
102. Grippo, A.J., Wu, K.D., Hassan, I., Carter, C.S., 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.
103. Grosenick, L., Clement, T.S., Fernald, R.D., 2007. Fish can infer social rank by observation alone. Nature 445, 429-432.
104. Hall, F.S., 1998. Social deprivation of neonatal, adolescent, and adult rats has distinct neurochemical and behavioral consequences. Crit. Rev. Neurobiol. 12, 129-162.
105. Hall, J.C., 1955. Some conditions of anxiety extinction. J. Abnorm. Soc. Psychol. 51, 126-132.
106. Haller, J., Fuchs, E., Halász, J., Makara, G.B., 1999. Defeat is a major stressor in males while social instability is stressful mainly in females: towards the development of a social stress model in female rats. Brain Res. Bull. 50, 33-39.
107. Harvey, P.W., Chevins, P.F.D., 1987. Crowding during pregnancy delays puberty and alters estrous cycles of female offspring in mice. Experientia 43, 306-308.
108. Hatch, A.M., Wiberg, G.S., Zawidzka, Z., Cann, M., Airth, J.M., Grice, H.C., 1965. Isolation syndrome in the rat. Toxicol. Appl. Pharmacol. 7, 737-745.
109. Heidbreder, C.A., Weiss, I.C., Domeney, A.M., Pryce, C., Homberg, J., Hedou, G., Feldon, J., Moran, M.C., Nelson, P., 2000. Behavioral, neurochemical and endocrinological characterization of the early social isolation syndrome. Neuroscience 100, 749-768.
110. Heinrichs, M., Baumgartner, T., Kirschbaum, C., Ehlert, U., 2003. Social support and oxytocin interact to suppress cortisol and subjective responses to psychosocial stress. Biol. Psychiatry 54, 1389-1398.
111. Heinrichs, S.C., Koob, G.F., 2006. Application of experimental stressors in laboratory rodents. Curr Protoc Neurosci Editor Board Jacqueline N Crawley Al Chapter 8: Unit8.4.
112. Hellemans, K.G.C., Benge, L.C., Olmstead, M.C., 2004. Adolescent enrichment partially reverses the social isolation syndrome. Dev. Brain Res. 150, 103-115.
113. Hennessy, M.B., Hornschuh, G., Kaiser, S., Sachser, N., 2006. Cortisol responses and social buffering: a study throughout the life span. Horm. Behav. 49, 383-390.
114. Hennessy, M.B., Maken, D.S., Graves, F.C., 2000. Consequences of the presence of the mother or unfamiliar adult female on cortisol, ACTH, testosterone and behavioral responses of periadolescent guinea pigs during exposure to novelty. Psychoneuroendocrinology 25, 619-632.
115. Herzog, C.J., Czéh, B., Corbach, S., Wuttke, W., Schulte-Herbrüggen, O., Hellweg, R., Flügge, G., Fuchs, E., 2009. Chronic social instability stress in female rats: a potential animal model for female depression. Neuroscience 159, 982-992.
116. Hofmann, H.A., Beery, A.K., Blumstein, D.T., Couzin, I.D., Earley, R.L., Hayes, L.D., Hurd, P.L., Lacey, E.A., Phelps, S.M., Solomon, N.G., Taborsky, M., Young, L.J., Rubenstein, D.R., 2014. An evolutionary framework for studying mechanisms of social behavior. Trends Ecol. Evol. Available at: http://linkinghub.elsevier.com/retrieve/pii/S0169534714001608 (accessed 25.08.14).
117. Holt-Lunstad, J., Smith, T.B., Layton, J.B., 2010. Social relationships and mortality risk: a meta-analytic review. PLoS Med. 7, e1000316.
118. Hostetler, C.M., Ryabinin, A.E., 2014. Social partners prevent alcohol relapse behavior in prairie voles. Psychoneuroendocrinology 39, 152-157.
119. Huhman, K.L., Solomon, M.B., Janicki, M., Harmon, A.C., Lin, S.M., Israel, J.E., Jasnow, A.M., 2003. Conditioned defeat in male and female syrian hamsters. Horm. Behav. 44, 293-299.
120. Jylhä, P., Isometsä, E., 2006. The relationship of neuroticism and extraversion to symptoms of anxiety and depression in the general population. Depress Anxiety 23, 281-289.
121. Kaiser, S., Kirtzeck, M., Hornschuh, G., Sachser, N., 2003. Sex-specific difference in social supportea study in female guinea pigs. Physiol. Behav. 79, 297-303.
122. Katz, P.S., Lillvis, J.L., 2014. Reconciling the deep homology of neuromodulation with the evolution of behavior. Curr. Opin. Neurobiol. 29, 39-47.
123. Kawachi, I., Kennedy, B.P., 1999. Income inequality and health: pathways and mechanisms. Health Serv. Res. 34, 215-227.
124. Kelly, A.M., Goodson, J.L., 2014. Social functions of individual vasopressineoxytocin cell groups in vertebrates: What do we really know? Front. Neuroendocrinol. 35, 512-529.
125. Kikusui, T., Winslow, J.T., Mori, Y., 2006. Social buffering: relief from stress and anxiety. Philos. Trans. R. Soc. B Biol. Sci. 361, 2215-2228.
126. King, J.A., 1956. Social relations of the domestic guinea pig living under seminatural conditions. Ecology 37, 221-228.
127. Kirby, E.D., Geraghty, A.C., Ubuka, T., Bentley, G.E., Kaufer, D., 2009. Stress increases putative gonadotropin inhibitory hormone and decreases luteinizing hormone in male rats. Proc. Natl. Acad. Sci. U.S.A. 106, 11324-11329.
128. Kirby, E.D., Muroy, S.E., Sun, W.G., Covarrubias, D., Leong, M.J., Barchas, L.A., Kaufer, D., 2013. Acute stress enhances adult rat hippocampal neurogenesis and activation of newborn neurons via secreted astrocytic FGF2. eLife 2, e00362.
129. Kirschbaum, C., Pirke, K.-M., Hellhammer, D.H., 1993. The "Trier Social Stress Test" e a tool for investigating psychobiological stress responses in a laboratory setting. Neuropsychobiology 28, 76-81.
130. Kiyokawa, Y., Kikusui, T., Takeuchi, Y., Mori, Y., 2004. Partner's stress status influences social buffering effects in rats. Behav. Neurosci. 118, 798-804.
131. Klein, S.L., Taymans, S.E., DeVries, A.C., Nelson, R.J., 1996. Cellular immunity is not compromised by high serum corticosterone concentrations in prairie voles. Am. J. Physiol-Regul. Integr. Comp. Physiol. 271, R1608-R1613.
132. Koolhaas, J.M., De Boer, S., De Rutter, A., Meerlo, P., Sgoifo, A., 1996. Social stress in rats and mice. Acta Physiol. Scand. Suppl. 640, 69-72.
133. Kotrschal, A., Ilmonen, P., Penn, D.J., 2007. Stress impacts telomere dynamics. Biol. Lett. 3, 128-130.
134. Krebs, H.A., 1975. The August Krogh principle: "For many problems there is an animal on which it can be most conveniently studied". J. Exp. Zool. 194, 221-226.
135. Krishnan, V., et al., 2007. Molecular adaptations underlying susceptibility and resistance to social defeat in brain reward regions. Cell 131, 391-404.
136. Lacey, E.A., Braude, S.H., Wieczorek, J.R., 1997. Burrow sharing by colonial tuco-tucos (Ctenomys sociabilis). J. Mammal. 78, 556-562.
137. Latané, B., 1969. Gregariousness and fear in laboratory rats. J. Exp. Soc. Psychol. 5, 61-69.
138. Latané, B., Eckman, J., Joy, V., 1966. Shared stress and interpersonal attraction. J. Exp. Soc. Psychol. 1 (Suppl. 1), 80-94.
139. Lee, A., Clancy, S., Fleming, A.S., 1999. Mother rats bar-press for pups: effects of lesions of the MPOA and limbic sites on maternal behavior and operant responding for pup-reinforcement. Behav. Brain Res. 100, 15-31.
140. Lepore, S.J., Allen, K.A., Evans, G.W., 1993. Social support lowers cardiovascular reactivity to an acute stressor. Psychosom. Med. 55, 518-524.
141. Lieberwirth, C., Wang, Z., 2012. The social environment and neurogenesis in the adult mammalian brain. Available at: Front. Hum. Neurosci. 6 http://www.ncbi. nlm.nih.gov/pmc/articles/PMC3347626/(accessed 01.08.14.).
142. Liu, D., Diorio, J., Tannenbaum, B., Caldji, C., Francis, D., Freedman, A., Sharma, S., Pearson, D., Plotsky, P.M., Meaney, M.J., 1997. Maternal care, hippocampal glucocorticoid receptors, and hypothalamic-pituitary-adrenal responses to stress. Science 277, 1659-1662.
143. Lucas, M., Ilin, Y., Anunu, R., Kehat, O., Xu, L., Desmedt, A., Richter-Levin, G., 2014. Long-term effects of controllability or the lack of it on coping abilities and stress resilience in the rat. Stress 1-8. http://dx.doi.org/10.3109/10253890.2014.930430.
144. Lukas, M., Toth, I., Reber, S.O., Slattery, D.A., Veenema, A.H., Neumann, I.D., 2011. The neuropeptide oxytocin facilitates pro-social behavior and prevents social avoidance in rats and mice. Neuropsychopharmacology 36, 2159-2168.
145. Lyons, D.M., Parker, K.J., Schatzberg, A.F., 2010. Animal models of early life stress: implications for understanding resilience. Dev. Psychobiol. 52, 616-624.
146. Mabry, K.E., Streatfeild, C.A., Keane, B., Solomon, N.G., 2011. avpr1a length polymorphism is not associated with either social or genetic monogamy in freeliving prairie voles. Anim. Behav. 81, 11-18.
147. Macdonald, D., Mathews, F., Berdoy, M., 1999. The behaviour and ecology of Rattus norvegicus: from opportunism to kamikaze tendencies. In: Ecologically-based Management of Rodent Pests. Australian Centre for International Agricultural Research, Canberra.
148. Madison, D.M., Fitzgerald, R.W., McShea, W.J., 1984. Dynamics of social nesting in overwintering meadow voles (Microtus pennsylvanicus): possible consequences for population cycling. Behav. Ecol. Sociobiol. 15, 9-17.
149. Madison, D.M., McShea, W., 1987. Seasonal changes in reproductive tolerance, spacing, and social organization in meadow voles: a microtine model. Am. Zool. 27, 899-908.
150. Magariños, A.M., McEwen, B.S., Flügge, G., Fuchs, E., 1996. Chronic psychosocial stress causes apical dendritic atrophy of hippocampal CA3 pyramidal neurons in subordinate tree shrews. J. Neurosci. 16, 3534-3540.
151. Maier, S.F., Watkins, L.R., 2005. Stressor controllability and learned helplessness: the roles of the dorsal raphe nucleus, serotonin, and corticotropin-releasing factor. Neurosci. Biobehav. Rev. 29, 829-841.
152. Marchleswska-Koj, A., 1997. Sociogenic stress and rodent reproduction. Neurosci. Biobehav. Rev. 21, 699-703.
153. Margerum, L., 2013. Effects of semi-natural environmental conditions on phenotypic plasticity in Rattus norvegicus. Available at: eScholarship http://escholarship.org/uc/item/60w8q88v (accessed 01.08.14.).
154. Martin, L.J., Tuttle, A.H., Mogil, J.S., 2014. The interaction between pain and social behavior in humans and rodents. Curr. Top. Behav. Neurosci. 1-18. Springer Berlin Heidelberg. Available at: http://link.springer.com/chapter/10.1007/7854_ 2014_287 (accessed 01.08.14).
155. Martinez, M., Calvo-Torrent, A., Pico-Alfonso, M.A., 1998. Social defeat and subordination as models of social stress in laboratory rodents: a review. Aggress. Behav. 24, 241-256.
156. McEwen, B.S., 2012. Brain on stress: how the social environment gets under the skin. Proc. Natl. Acad. Sci. U.S.A. 109 (Suppl. 2), 17180-17185.
157. McEwen, B.S., Magarinos, A.M., 2001. Stress and hippocampal plasticity: implications for the pathophysiology of affective disorders. Hum. Psychopharmacol. Clin. Exp. 16, S7-S19.
158. McNeal, N., Scotti, M.-A.L., Wardwell, J., Chandler, D.L., Bates, S.L., LaRocca, M., Trahanas, D.M., Grippo, A.J., 2014. Disruption of social bonds induces behavioral and physiological dysregulation in male and female prairie voles. Auton. Neurosci. 180, 9-16.
159. Meaney, M.J., 2001. Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations. Annu. Rev. Neurosci. 24, 1161-1192.
160. Meerlo, P., Overkamp, G.J.F., Daan, S., Van Den Hoofdakker, R.H., Koolhaas, J.M., 1996. Changes in behaviour and body weight following a single or double social defeat in rats. Stress 1, 21-32.
161. Mendoza, S.P., Coe, C.L., Lowe, E.L., Levine, S., 1978. The physiological response to group formation in adult male squirrel monkeys. Psychoneuroendocrinology 3, 221-229.
162. Meyerhoff, D.J., Mon, A., Metzler, T., Neylan, T.C., 2014. Cortical gammaaminobutyric acid and glutamate in posttraumatic stress disorder and their relationships to self-reported sleep quality. Sleep 37, 893-900.
163. Mirescu, C., Gould, E., 2006. Stress and adult neurogenesis. Hippocampus 16, 233-238.
164. Mogil, J.S., Chanda, M.L., 2005. The case for the inclusion of female subjects in basic science studies of pain. Pain 117, 1-5.
165. Morris, W.N., Worchel, S., Bois, J.L., Pearson, J.A., Alan, C., Samaha, G.M., Wachtler, J., Wright, S.L., 1976. Collective coping with stress: group reactions to fear, anxiety, and ambiguity. J. Pers. Soc. Psychol. 33, 674-679.
166. Moy, S.S., Nadler, J.J., Young, N.B., Perez, A., Holloway, L.P., Barbaro, R.P., Barbaro, J.R., Wilson, L.M., Threadgill, D.W., Lauder, J.M., Magnuson, T.R., Crawley, J.N., 2007. Mouse behavioral tasks relevant to autism: phenotypes of 10 inbred strains. Behav. Brain Res. 176, 4-20.
167. Nakayasu, T., Ishii, K., 2008. Effects of pair-housing after social defeat experience on elevated plus-maze behavior in rats. Behav. Process. 78, 477-480.
168. Naragon-Gainey, K., Rutter, L.A., Brown, T.A., 2014. The interaction of extraversion and anxiety sensitivity on social anxiety: evidence of specificity relative to depression. Behav. Ther. 45, 418-429.
169. Neumann, I.D., 2008. Brain oxytocin: a key regulator of emotional and social behaviours in both females and males. J. Neuroendocrinol 20, 858-865.
170. Nyuyki, K.D., Beiderbeck, D.I., Lukas, M., Neumann, I.D., Reber, S.O., 2012. Chronic subordinate colony housing (CSC) as a model of chronic psychosocial stress in male rats. PLoS ONE 7, e52371.
171. Ophir, A.G., Gessel, A., Zheng, D.-J., Phelps, S.M., 2012. Oxytocin receptor density is associated with male mating tactics and social monogamy. Horm. Behav. 61, 445-453.
172. Ophir, A.G., Phelps, S.M., Sorin, A.B., Wolff, J.O., 2008. Social but not genetic monogamy is associated with greater breeding success in prairie voles. Anim. Behav. 75, 1143-1154.
173. Palanza, P., 2001. Animal models of anxiety and depression: how are females different? Neurosci. Biobehav. Rev. 25, 219-233.
174. Palanza, P., Gioiosa, L., Parmigiani, S., 2001. Social stress in mice: gender differences and effects of estrous cycle and social dominance. Physiol. Behav. 73, 411-420.
175. Panksepp, J.B., Lahvis, G.P., 2007. Social reward among juvenile mice. Genes Brain Behav. 6, 661-671.
176. Parent, C.I., Del Corpo, A., Cameron, N.M., Meaney, M.J., 2013. Maternal care associates with play dominance rank among adult female rats. Dev. Psychobiol. 55, 745-756.
177. Parent, C.I., Meaney, M.J., 2008. The influence of natural variations in maternal care on play fighting in the rat. Dev. Psychobiol. 50, 767-776.
178. Parker, K.J., Buckmaster, C.L., Lindley, S.E., Schatzberg, A.F., Lyons, D.M., 2012. Hypothalamic- pituitary-adrenal axis physiology and cognitive control of behavior in stress inoculated monkeys. Int. J. Behav. Dev. 36.
179. Payne, A.P., Swanson, H.H., 1970. Agonistic behaviour between pairs of hamsters of the same and opposite sex in a neutral observation area. Behaviour 36, 260-269.
180. Peña, C.J., Neugut, Y.D., Calarco, C.A., Champagne, F.A., 2014. Effects of maternal care on the development of midbrain dopamine pathways and reward-directed behavior in female offspring. Eur. J. Neurosci. 39, 946-956.
181. Perkeybile, A.M., Griffin, L.L., Bales, K.L., 2013. Natural variation in early parental care correlates with social behaviors in adolescent prairie voles (Microtus ochrogaster). Front. Behav. Neurosci. 7, 21.
182. Peters, S., Grunwald, N., Rümmele, P., Endlicher, E., Lechner, A., Neumann, I.D., Obermeier, F., Reber, S.O., 2011. Chronic psychosocial stress increases the risk for inflammation-related colon carcinogenesis in male mice. Stress 15, 403-415.
183. Peuler, J.D., Scotti, M.-A.L., Phelps, L.E., McNeal, N., Grippo, A.J., 2012. Chronic social isolation in the prairie vole induces endothelial dysfunction: implications for depression and cardiovascular disease. Physiol. Behav. 106, 476-484.
184. Phelps, S.M., Campbell, P., Zheng, D.-J., Ophir, A.G., 2010. Beating the boojum: comparative approaches to the neurobiology of social behavior. Neuropharmacology 58, 17-28.
185. Puzserova, A., Slezak, P., Balis, P., Bernatova, I., 2013. Long-term social stress induces nitric oxide-independent endothelial dysfunction in normotensive rats. Stress Amst. Neth. 16, 331-339.
186. Pyter, L.M., Weil, Z.M., Nelson, R.J., 2005. Latitude affects photoperiod-induced changes in immune response in meadow voles (Microtus pennsylvanicus). Can. J. Zool 83, 1271-1278.
187. Quirici, V., Faugeron, S., Hayes, L.D., Ebensperger, L.A., 2011. The influence of group size on natal dispersal in the communally rearing and semifossorial rodent, Octodon degus. Behav. Ecol. Sociobiol. 65, 787-798.
188. Reiss, D., Wolter-Sutter, A., Krezel, W., Ouagazzal, A.-M., 2007. Effects of social crowding on emotionality and expression of hippocampal nociceptin/orphanin FQ system transcripts in mice. Behav. Brain Res. 184, 167-173.
189. Resendez, S.L., Kuhnmuench, M., Krzywosinski, T., Aragona, B.J., 2012. -Opioid receptors within the nucleus accumbens shell mediate pair bond maintenance. J. Neurosci. 32, 6771-6784.
190. Ross, H.E., Young, L.J., 2009. Oxytocin and the neural mechanisms regulating social cognition and affiliative behavior. Front. Neuroendocr 30, 534-547.
191. Ruis, M.A.W., te Brake, J.H.A., Buwalda, B., De Boer, S.F., Meerlo, P., Korte, S.M., Blokhuis, H.J., Koolhaas, J.M., 1999. Housing familiar male wildtype rats together reduces the long-term adverse behavioural and physiological effects of social defeat. Psychoneuroendocrinology 24, 285-300.
192. Ruscio, M.G., Sweeny, T., Hazelton, J., Suppatkul, P., Sue Carter, C., 2007. Social environment regulates corticotropin releasing factor, corticosterone and vasopressin in juvenile prairie voles. Horm. Behav. 51, 54-61.
193. Sapolsky, R.M., 1989. Hypercortisolism among socially subordinate wild baboons originates at the CNS level. Arch. Gen. Psychiatry 46, 1047-1051.
194. Sapolsky, R.M., 2005. The influence of social hierarchy on primate health. Science 308, 648-652.
195. Sapolsky, R.M., Meaney, M.J., McEwen, B.S., 1985. The development of the glucocorticoid receptor system in the rat limbic brain. III. Negative-feedback regulation. Brain Res. 350, 169-173.
196. Sapolsky, R.M., Romero, L.M., Munck, A.U., 2000. How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocr. Rev. 21, 55-89.
197. Schmidt, M.V., Trümbach, D., Weber, P., Wagner, K., Scharf, S.H., Liebl, C., Datson, N., Namendorf, C., Gerlach, T., Kühne, C., Uhr, M., Deussing, J.M., Wurst, W., Binder, E.B., Holsboer, F., Müller, M.B., 2010. Individual stress vulnerability is predicted by short-term memory and AMPA receptor subunit ratio in the hippocampus. J. Neurosci. Off. J. Soc. Neurosci. 30, 16949-16958.
198. Seney, M., Goldman, B.D., Forger, N.G., 2006. Breeding status affects motoneuron number and muscle size in naked mole-rats: recruitment of perineal motoneurons? J. Neurobiol. 66, 1354-1364.
199. Sgoifo, A., Carnevali, L., Grippo, A.J., 2014. The socially stressed heart. Insights from studies in rodents. Neurosci. Biobehav. Rev. 39, 51-60.
200. Sgoifo, A., Koolhaas, J., De Boer, S., Musso, E., Stilli, D., Buwalda, B., Meerlo, P., 1999. Social stress, autonomic neural activation, and cardiac activity in rats. Neurosci. Biobehav Rev. 23, 915-923.
201. Sgoifo, A., Pozzato, C., Meerlo, P., Costoli, T., Manghi, M., Stilli, D., Olivetti, G., Musso, E., 2002. Intermittent exposure to social defeat and open-field test in rats: acute and long-term effects on ECG, body temperature and physical activity. Stress Int. J. Biol. Stress 5, 23-35.
202. Sherman, P.W., Jarvis, J.U.M., Alexander, R.D., 1991. The Biology of the Naked Molerat. Princeton University Press, Princeton, New Jersey.
203. Siegrist, J., Marmot, M., 2004. Health inequalities and the psychosocial environmentdtwo scientific challenges. Soc. Sci. Med. 58, 1463-1473.
204. Silk, J.B., Beehner, J.C., Bergman, T.J., Crockford, C., Engh, A.L., Moscovice, L.R., Wittig, R.M., Seyfarth, R.M., Cheney, D.L., 2010. Strong and consistent social bonds enhance the longevity of female baboons. Curr. Biol. 20, 1359-1361.
205. Simpson, J., Kelly, J.P., 2011. The impact of environmental enrichment in laboratory ratsdbehavioural and neurochemical aspects. Behav. Brain Res. 222, 246-264.
206. Singh-Manoux, A., Marmot, M.G., Adler, N.E., 2005. Does subjective social status predict health and change in health status better than objective status? Psychosom. Med. 67, 855-861.
207. Smith, A.S., Wang, Z., 2014. Hypothalamic oxytocin mediates social buffering of the stress response. Biol. Psychiatry 76, 281-288.
208. Sorge, R.E., et al., 2014. Olfactory exposure to males, including men, causes stress and related analgesia in rodents. Nat. Methods. Available at: http://www. nature.com/doifinder/10.1038/nmeth.2935 (accessed 13.05.14.).
209. Späni, D., Arras, M., König, B., Rülicke, T., 2003. Higher heart rate of laboratory mice housed individually vs in pairs. Lab. Anim. 37, 54-62.
210. Stanton, M.A., Mann, J., 2012. Early social networks predict survival in wild bottlenose dolphins. PLoS ONE 7, e47508.
211. Starr-Phillips, E.J., Beery, A.K., 2014. Natural variation in maternal care shapes adult social behavior in rats. Dev. Psychobiol. 56, 1017-1026.
212. Stranahan, A.M., Khalil, D., Gould, E., 2006. Social isolation delays the positive effects of running on adult neurogenesis. Nat. Neurosci. 9, 526-533.
213. Sztainberg, Y., Chen, A., 2010. An environmental enrichment model for mice. Nat. Protoc. 5, 1535-1539.
214. Szyf, M., Weaver, I., Meaney, M., 2007. Maternal care, the epigenome and phenotypic differences in behavior. Reprod. Toxicol. Elmsford. N. 24, 9-19.
215. Taylor, G.T., 1981. Fear and affiliation in domesticated male rats. J. Comp. Physiol. Psychol. 95, 685-693.
216. Taylor, S.E., 2006. Tend and befriend: biobehavioral bases of affiliation under stress. Curr. Dir. Psychol. Sci. 15, 273-277.
217. Taylor, S.E., Klein, L.C., Lewis, B.P., Gruenewald, T.L., Gurung, R.A., Updegraff, J.A., 2000. Biobehavioral responses to stress in females: tend-and-befriend, not fight-or-flight. Psychol. Rev. 107, 411-429.
218. Taymans, S.E., DeVries, A.C., DeVries, M.B., Nelson, R.J., Friedman, T.C., Castro, M., Detera-Wadleigh, S., Carter, C.S., Chrousos, G.P., 1997. The hypothalamic-pituitary- adrenal axis of prairie voles (Microtus ochrogaster): evidence for target tissue glucocorticoid resistance. Gen. Comp. Endocrinol. 106, 48-61.
219. Teichman, Y., 1974. Predisposition for anxiety and affiliation. J. Pers. Soc. Psychol. 29, 405-410.
220. Thorsteinsson, E.B., James, J.E., Elizabeth, M., 1998. Effects of video-relayed social support on hemodynamic reactivity and salivary cortisol during laboratorybased behavioral challenge. Health Psychol. 17, 436-444.
221. Tornatzky, W., Miczek, K.A., 1993. Long-term impairment of autonomic circadian rhythms after brief intermittent social stress. Physiol. Behav. 53, 983-993.
222. Tramullas, M., Dinan, T.G., Cryan, J.F., 2012. Chronic psychosocial stress induces visceral hyperalgesia in mice. Stress Amst. Neth. 15, 281-292.
223. Tzanoulinou, S., Riccio, O., de Boer, M.W., Sandi, C., 2014. Peripubertal stressinduced behavioral changes are associated with altered expression of genes involved in excitation and inhibition in the amygdala. Transl. Psychiatry 4, e410. Valzelli, L., 1973. The "isolation syndrome" in mice. Psychopharmacologia 31, 305-320.
224. Valzelli, L., 1973. The "isolation syndrome" in mice. Psychopharmacologia 31, 305-320
225. Van Hasselt, F.N., Tieskens, J.M., Trezza, V., Krugers, H.J., Vanderschuren, L.J.M.J., Joëls, M., 2012. Within-litter variation in maternal care received by individual pups correlates with adolescent social play behavior in male rats. Physiol. Behav. 106, 701-706.
226. Veenema, A.H., 2012. Toward understanding how early-life social experiences alter oxytocin- and vasopressin-regulated social behaviors. Horm. Behav. 61, 304-312.
227. Veenema, A.H., Meijer, O.C., de Kloet, E.R., Koolhaas, J.M., Bohus, B.G., 2003. Differences in basal and stress-induced HPA regulation of wild house mice selected for high and low aggression. Horm. Behav. 43, 197-204.
228. Veenema, A.H., Reber, S.O., Selch, S., Obermeier, F., Neumann, I.D., 2008. Early life stress enhances the vulnerability to chronic psychosocial stress and experimental colitis in adult mice. Endocrinology 149, 2727-2736.
229. Veeraiah, P., Noronha, J.M., Maitra, S., Bagga, P., Khandelwal, N., Chakravarty, S., Kumar, A., Patel, A.B., 2014. Dysfunctional glutamatergic and g-aminobutyric acidergic activities in prefrontal cortex of mice in social defeat model of depression. Biol. Psychiatry 76, 231-238.
230. Virgin, C.E., Sapolsky, R.M., 1997. Styles of male social behavior and their endocrine correlates among low-ranking baboons. Am. J. Primatol. 42, 25-39.
231. Ward, I.L., Ward, O.B., Winn, R.J., Bielawski, D., 1994. Male and female sexual behavior potential of male rats prenatally exposed to the influence of alcohol, stress, or both factors. Behav. Neurosci. 108, 1188-1195.
232. Weaver, I.C.G., Cervoni, N., Champagne, F.A., D'Alessio, A.C., Sharma, S., Seckl, J.R., Dymov, S., Szyf, M., Meaney, M.J., 2004. Epigenetic programming by maternal behavior. Nat. Neurosci. 7, 847-854.
233. Westenbroek, C., Snijders, T.A.B., den Boer, J.A., Gerrits, M., Fokkema, D.S., Ter Horst, G.J., 2005. Pair-housing of male and female rats during chronic stress exposure results in gender-specific behavioral responses. Horm. Behav. 47, 620-628.
234. Wilkinson, M.B., Dias, C., Magida, J., Mazei-Robison, M., Lobo, M., Kennedy, P., Dietz, D., Covington, H., Russo, S., Neve, R., Ghose, S., Tamminga, C., Nestler, E.J., 2011. A novel role of the WNT-dishevelled-GSK3b signaling cascade in the mouse nucleus accumbens in a social defeat model of depression. J. Neurosci. Off. J. Soc. Neurosci. 31, 9084-9092.
235. Williams, J.R., Catania, K.C., Carter, C.S., 1992. Development of partner preferences in female prairie voles (Microtus ochrogaster): the role of social and sexual experience. Horm. Behav. 26, 339-349.
236. Wilson, J.H., 2000. A conspecific attenuates prolactin responses to open-field exposure in rats. Horm. Behav. 38, 39-43.
237. Wohleb, E.S., Hanke, M.L., Corona, A.W., Powell, N.D., Stiner, L.M., Bailey, M.T., Nelson, R.J., Godbout, J.P., Sheridan, J.F., 2011. b-Adrenergic receptor antagonism prevents anxiety-like behavior and microglial reactivity induced by repeated social defeat. J. Neurosci. Off. J. Soc. Neurosci. 31, 6277-6288.
238. Wood, G.E., Shors, T.J., 1998. Stress facilitates classical conditioning in males, but impairs classical conditioning in females through activational effects of ovarian hormones. Proc. Natl. Acad. Sci. U.S.A. 95, 4066-4071.
239. Wood, S.K., Walker, H.E., Valentino, R.J., 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.
240. Woodruff, J.A., Lacey, E.A., Bentley, G.E., Kriegsfeld, L.J., 2013. Effects of social environment on baseline glucocorticoid levels in a communally breeding rodent, the colonial tuco-tuco (Ctenomys sociabilis). Horm. Behav. 64, 566-572.
241. Woodruff, T.K., Kibbe, M.R., Paller, A.S., Turek, F.W., Woolley, C.S., 2014. Commentary: "Leaning in" to support sex differences in basic science and clinical research. Endocrinology 155, 1181-1183.
242. Wu, M.V., Shamy, J.L., Bedi, G., Choi, C.-W.J., Wall, M.M., Arango, V., Boldrini, M., Foltin, R.W., Hen, R., 2014. Impact of social status and antidepressant treatment on neurogenesis in the baboon hippocampus. Neuropsychopharmacol. Off. Publ. Am. Coll. Neuropsychopharmacol. 39, 1861-1871.
243. Wynne-Edwards, K.E., Lisk, R.D., 1989. Differential effects of paternal presence on pup survival in two species of dwarf hamster (Phodopus sungorus and Phodopus campbelli). Physiol. Behav. 45, 465-469.
244. Yee, J.R., Cavigelli, S.A., Delgado, B., McClintock, M.K., 2008. Reciprocal affiliation among adolescent rats during a mild group stressor predicts mammary tumors and lifespan. Psychosom. Med. 70, 1050-1059.
245. Young, K.A., Liu, Y., Wang, Z., 2008. The neurobiology of social attachment: a comparative approach to behavioral, neuroanatomical, and neurochemical studies. Comp. Biochem. Physiol. C. Toxicol. Pharmacol. 148, 401-410.
246. Young, L.J., 1999. Frank A. Beach Award. Oxytocin and vasopressin receptors and species-typical social behaviors. Horm. Behav. 36, 212-221.
247. Young, L.J., Wang, Z., 2004. The neurobiology of pair bonding. Nat. Neurosci. 7, 1048-1054.
248. Zucker, I., Beery, A.K., 2010. Males still dominate animal studies. Nature 465, 690. Zucker, R.A., Manosevitz, M., Lanyon, R.I., 1968. Birth order, anxiety, and affiliation during a crisis. J. Pers. Soc. Psychol. 8, 354-359.
249. Zucker, R.A., Manosevitz, M., Lanyon, R.I., 1968. Birth order, anxiety, and affiliation during a crisis. J. Pers. Soc. Psychol. 8, 354-359