Environmental insults in early life and submissiveness later in life in mouse models

Frontiers in Neuroscience

Volumn 9, Issue MAR, 2015, Pages

  Benner, Seico ^a   Endo, Toshihiro ^a   Kakeyama, Masaki ^a,b   Tohyama, Chiharu ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b NAGASAKI UNIVERSITY   (Japan)

Author keywords

Dominance behavior; Early life environment; IntelliCage based competition task; Mouse; Social behavior

Indexed keywords

DIOXIN;

ANIMAL EXPERIMENT; ARTICLE; COMPETITION; DOMINANCE BEHAVIOR; EARLY LIFE STRESS; ENVIRONMENTAL FACTOR; MOTHER; MOUSE; NONHUMAN; PHENOTYPE; SOCIAL BEHAVIOR; SOCIAL DOMINANCE; SUBMISSIVENESS; TASK PERFORMANCE;

EID: 84928008348     PISSN: 16624548     EISSN: 1662453X     Source Type: Journal    
DOI: 10.3389/fnins.2015.00091     Document Type: Article

References (93)

1. Adolphs, R. (2001). The neurobiology of social cognition. Curr. Opin. Neurobiol. 11, 231-239. doi: 10.1016/S0959-4388(00)00202-6
2. Akbaripasand, A., Krkosek, M., Lokman, P. M., and Closs, G. P. (2014). Does social status within a dominance hierarchy mediate individual growth, residency and relocation? Oecologia 176, 771-779. doi: 10.1007/s00442-014-3038-z
3. Babri, S., Doosti, M. H., and Salari, A. A. (2014). Strain-dependent effects of prenatal maternal immune activation on anxiety- and depression-like behaviors in offspring. Brain Behav. Immun. 37, 164-176. doi: 10.1016/j.bbi.2013.12.003
4. Bachevalier, J., and Loveland, K. A. (2006). The orbitofrontal-amygdala circuit and self-regulation of social-emotional behavior in autism. Neurosci. Biobehav. Rev. 30, 97-117. doi: 10.1016/j.neubiorev.2005.07.002
5. Balk, J. L., and Piper, W. N. (1984). Altered blood levels of corticosteroids in the rat after exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin. Biochem. Pharmacol. 33, 2531-2534. doi: 10.1016/0006-2952(84)90732-9
6. Benner, S., Endo, T., Endo, N., Kakeyama, M., and Tohyama, C. (2014). Early deprivation induces competitive subordinance in C57BL/6 male mice. Physiol. Behav. 137, 42-52. doi: 10.1016/j.physbeh.2014.06.018
7. Berman, A. K., Lott, R. B., and Donaldson, S. T. (2014). Periodic maternal deprivation may modulate offspring anxiety-like behavior through mechanisms involving neuroplasticity in the amygdala. Brain Res. Bull. 101, 7-11. doi: 10.1016/j.brainresbull.2013.12.005
8. Bestervelt, L. L., Pitt, J. A., Nolan, C. J., Cai, Y., Piper, D. W., Dybowski, J. A., et al. (1998). In vitro 2,3,7,8-tetrachlorodibenzo-p-dioxin interference with the anterior pituitary hormone adrenocorticortropin. Toxicol. Sci. 44, 107-115.
9. Bestervelt, L. L., Pitt, J. A., Nolan, C. J., and Piper, W. N. (1993). TCDD alters pituitary-adrenal function. II: evidence for decreased bioactivity of ACTH. Neurotoxicol. Teratol. 15, 371-376. doi: 10.1016/0892-0362(93)90053-Q
10. Biagini, G., Pich, E. M., Carani, C., Marrama, P., and Agnati, L. F. (1998). Postnatal maternal separation during the stress hyporesponsive period enhances the adrenocortical response to novelty in adult rats by affecting feedback regulation in the CA1 hippocampal field. Int. J. Dev. Neurosci. 16, 187-197. doi: 10.1016/S0736-5748(98)00019-7
11. Birnie, A. K., Taylor, J. H., Cavanaugh, J., and French, J. A. (2013). Quality of maternal and paternal care predicts later stress reactivity in the cooperatively-breeding marmoset (Callithrix geoffroyi). Psychoneuroendocrinology 38, 3003-3014. doi: 10.1016/j.psyneuen.2013.08.011
12. Blair, K. S., Geraci, M., Hollon, N., Otero, M., Devido, J., Majestic, C., et al. (2010). Social norm processing in adult social phobia: atypically increased ventromedial frontal cortex responsiveness to unintentional (embarrassing) transgressions. Am. J. Psychiatry 167, 1526-1532. doi: 10.1176/appi.ajp.2010.09121797
13. Blanchard, D. C., Sakai, R. R., McEwen, B., Weiss, S. M., and Blanchard, R. J. (1993). Subordination stress: behavioral, brain, and neuroendocrine correlates. Behav. Brain Res. 58, 113-121. doi: 10.1016/0166-4328(93)90096-9
14. Blanchard, D. C., Spencer, R. L., Weiss, S. M., Blanchard, R. J., McEwen, B., and Sakai, R. R. (1995). Visible burrow system as a model of chronic social stress: behavioral and neuroendocrine correlates. Psychoneuroendocrinology 20, 117-134. doi: 10.1016/0306-4530(94)E0045-B
15. Blanchard, R. J., Flannelly, K. J., and Blanchard, D. C. (1988). Life-span studies of dominance and aggression in established colonies of laboratory rats. Physiol. Behav. 43, 1-7. doi: 10.1016/0031-9384(88)90089-3
16. Branchi, I., Curley, J. P., D'Andrea, I., Cirulli, F., Champagne, F. A., and Alleva, E. (2013). Early interactions with mother and peers independently build adult social skills and shape BDNF and oxytocin receptor brain levels. Psychoneuroendocrinology 38, 522-532. doi: 10.1016/j.psyneuen.2012.07.010
17. Braw, Y., Malkesman, O., Dagan, M., Bercovich, A., Lavi-Avnon, Y., Schroeder, M., et al. (2006). Anxiety-like behaviors in pre-pubertal rats of the Flinders Sensitive Line (FSL) and Wistar-Kyoto (WKY) animal models of depression. Behav. Brain Res. 167, 261-269. doi: 10.1016/j.bbr.2005.09.013
18. Caldji, C., Tannenbaum, B., Sharma, S., Francis, D., Plotsky, P. M., and Meaney, M. J. (1998). Maternal care during infancy regulates the development of neural systems mediating the expression of fearfulness in the rat. Proc. Natl. Acad. Sci. U.S.A. 95, 5335-5340. doi: 10.1073/pnas.95.9.5335
19. Champagne, F. A., and Curley, J. P. (2005). How social experiences influence the brain. Curr. Opin. Neurobiol. 15, 704-709. doi: 10.1016/j.conb.2005.10.001
20. Chase, I. D., Tovey, C., Spangler-Martin, D., and Manfredonia, M. (2002). Individual differences versus social dynamics in the formation of animal dominance hierarchies. Proc. Natl. Acad. Sci. U.S.A. 99, 5744-5749. doi: 10.1073/pnas.082104199
21. Cordero, M. I., and Sandi, C. (2007). Stress amplifies memory for social hierarchy. Front. Neurosci. 1, 175-184. doi: 10.3389/neuro.01.1.1.013.2007
22. Coura, R. S., Cressant, A., Xia, J., de Chaumont, F., Olivo-Marin, J. C., Pelloux, Y., et al. (2013). Nonaggressive and adapted social cognition is controlled by the interplay between noradrenergic and nicotinic receptor mechanisms in the prefrontal cortex. FASEB J. 27, 4343-4354. doi: 10.1096/fj.13-231084
23. Desjardins, C., Maruniak, J. A., and Bronson, F. H. (1973). Social rank in house mice: differentiation revealed by ultraviolet visualization of urinary marking patterns. Science 182, 939-941. doi: 10.1126/science.182.4115.939
24. Dewsbury, D. A. (1982). Dominance rank, copulatory behavior, and differential reproduction. Q. Rev. Biol. 57, 135-159. doi: 10.1086/412672
25. Dibartolomeis, M. J., Moore, R. W., Peterson, R. E., Christian, B. J., and Jefcoate, C. R. (1987). Altered regulation of adrenal steroidogenesis in 2,3,7,8-tetrachlorodibenzo-p-dioxin-treated rats. Biochem. Pharmacol. 36, 59-67. doi: 10.1016/0006-2952(87)90382-0
26. Disney, E. R., Iacono, W., McGue, M., Tully, E., and Legrand, L. (2008). Strengthening the case: prenatal alcohol exposure is associated with increased risk for conduct disorder. Pediatrics 122, e1225-e1230. doi: 10.1542/peds.2008-1380
27. Drickamer, L. C. (2001). Urine marking and social dominance in male house mice (Mus musculus domesticus). Behav. Processes 53, 113-120. doi: 10.1016/S0376-6357(00)00152-2
28. Endo, T., Kakeyama, M., Uemura, Y., Haijima, A., Okuno, H., Bito, H., et al. (2012). Executive function deficits and social-behavioral abnormality in mice exposed to a low dose of dioxin in utero and via lactation. PLoS ONE 7:e50741. doi: 10.1371/journal.pone.0050741
29. Feder, Y., Nesher, E., Ogran, A., Kreinin, A., Malatynska, E., Yadid, G., et al. (2010). Selective breeding for dominant and submissive behavior in Sabra mice. J. Affect. Disord. 126, 214-222. doi: 10.1016/j.jad.2010.03.018
30. Ferguson, J. N., Young, L. J., and Insel, T. R. (2002). The neuroendocrine basis of social recognition. Front. Neuroendocrinol. 23, 200-224. doi: 10.1006/frne.2002.0229
31. Fleming, A. S., O'Day, D. H., and Kraemer, G. W. (1999). Neurobiology of mother-infant interactions: experience and central nervous system plasticity across development and generations. Neurosci. Biobehav. Rev. 23, 673-685.
32. Freeman, J. B., Rule, N. O., Adams, R. B. Jr., and Ambady, N. (2009). Culture shapes a mesolimbic response to signals of dominance and subordination that associates with behavior. Neuroimage 47, 353-359. doi: 10.1016/j.neuroimage.2009.04.038
33. Freund, J., Brandmaier, A. M., Lewejohann, L., Kirste, I., Kritzler, M., Kruger, A., et al. (2013). Emergence of individuality in genetically identical mice. Science 340, 756-759. doi: 10.1126/science.1235294
34. Galsworthy, M. J., Amrein, I., Kuptsov, P. A., Poletaeva, I. I., Zinn, P., Rau, A., et al. (2005). A comparison of wild-caught wood mice and bank voles in the Intellicage: assessing exploration, daily activity patterns and place learning paradigms. Behav. Brain Res. 157, 211-217. doi: 10.1016/j.bbr.2004.06.021
35. Gee, D. G., Gabard-Durnam, L. J., Flannery, J., Goff, B., Humphreys, K. L., Telzer, E. H., et al. (2013). Early developmental emergence of human amygdala-prefrontal connectivity after maternal deprivation. Proc. Natl. Acad. Sci. U.S.A. 110, 15638-15643. doi: 10.1073/pnas.1307893110
36. Gesquiere, L. R., Learn, N. H., Simao, M. C., Onyango, P. O., Alberts, S. C., and Altmann, J. (2011). Life at the top: rank and stress in wild male baboons. Science 333, 357-360. doi: 10.1126/science.1207120
37. Glavas, M. M., Ellis, L., Yu, W. K., and Weinberg, J. (2007). Effects of prenatal ethanol exposure on basal limbic-hypothalamic-pituitary-adrenal regulation: role of corticosterone. Alcohol. Clin. Exp. Res. 31, 1598-1610. doi: 10.1111/j.1530-0277.2007.00460.x
38. Haijima, A., Endo, T., Zhang, Y., Miyazaki, W., Kakeyama, M., and Tohyama, C. (2010). In utero and lactational exposure to low doses of chlorinated and brominated dioxins induces deficits in the fear memory of male mice. Neurotoxicology 31, 385-390. doi: 10.1016/j.neuro.2010.04.004
39. Hamilton, D. A., Barto, D., Rodriguez, C. I., Magcalas, C. M., Fink, B. C., Rice, J. P., et al. (2014). Effects of moderate prenatal ethanol exposure and age on social behavior, spatial response perseveration errors and motor behavior. Behav. Brain Res. 269, 44-54. doi: 10.1016/j.bbr.2014.04.029
40. Hamilton, D. A., Candelaria-Cook, F. T., Akers, K. G., Rice, J. P., Maes, L. I., Rosenberg, M., et al. (2010). Patterns of social-experience-related c-fos and Arc expression in the frontal cortices of rats exposed to saccharin or moderate levels of ethanol during prenatal brain development. Behav. Brain Res. 214, 66-74. doi: 10.1016/j.bbr.2010.05.048
41. Hattori, Y., Takeda, T., Fujii, M., Taura, J., Ishii, Y., and Yamada, H. (2014). Dioxin-induced fetal growth retardation: the role of a preceding attenuation in the circulating level of glucocorticoid. Endocrine 47, 572-580. doi: 10.1007/s12020-014-0257-3
42. Huang, P., Ceccatelli, S., Håkansson, H., Grandison, L., and Rannug, A. (2002). Constitutive and TCDD-induced expression of ah receptor-responsive genes in the pituitary. Neurotoxicology 23, 783-793. doi: 10.1016/S0161-813X(02)00040-2
43. Huang, P., Rannug, A., Ahlbom, E., Hakansson, H., and Ceccatelli, S. (2000). Effect of 2,3,7,8-tetrachlorodibenzo-p-dioxin on the expression of cytochrome P450 1A1, the aryl hydrocarbon receptor, and the aryl hydrocarbon receptor nuclear translocator in rat brain and pituitary. Toxicol. Appl. Pharmacol. 169, 159-167. doi: 10.1006/taap.2000.9064
44. Kaliste-Korhonen, E., and Eskola, S. (2000). Fighting in NIH/S male mice: consequences for behaviour in resident-intruder tests and physiological parameters. Lab. Anim. 34, 189-198. doi: 10.1258/002367700780457626
45. Kiryanova, V., and Dyck, R. H. (2014). Increased aggression, improved spatial memory, and reduced anxiety-like behaviour in adult male mice exposed to fluoxetine early in life. Dev. Neurosci. 36, 396-408. doi: 10.1159/000363102
46. Kleinhans, N. M., Johnson, L. C., Richards, T., Mahurin, R., Greenson, J., Dawson, G., et al. (2009). Reduced neural habituation in the amygdala and social impairments in autism spectrum disorders. Am. J. Psychiatry 166, 467-475. doi: 10.1176/appi.ajp.2008.07101681
47. Koppensteiner, P., Aizawa, S., Yamada, D., Kabuta, T., Boehm, S., Wada, K., et al. (2014). Age-dependent sensitivity to glucocorticoids in the developing mouse basolateral nucleus of the amygdala. Psychoneuroendocrinology 46, 64-77. doi: 10.1016/j.psyneuen.2014.04.007
48. Laurent, H. K., Neiderhiser, J. M., Natsuaki, M. N., Shaw, D. S., Fisher, P. A., Reiss, D., et al. (2014). Stress system development from age 4.5 to 6: family environment predictors and adjustment implications of HPA activity stability versus change. Dev. Psychobiol. 56, 340-354. doi: 10.1002/dev.21103
49. Likhtik, E., Pelletier, J. G., Paz, R., and Pare, D. (2005). Prefrontal control of the amygdala. J. Neurosci. 25, 7429-7437. doi: 10.1523/JNEUROSCI.2314-05.2005
50. Likhtik, E., Stujenske, J. M. A., Topiwala, M., Harris, A. Z., and Gordon, J. A. (2014). Prefrontal entrainment of amygdala activity signals safety in learned fear and innate anxiety. Nat. Neurosci. 17, 106-113. doi: 10.1038/nn.3582
51. Lindzey, G., Winston, H., and Manosevitz, M. (1961). Social dominance in inbred mouse strains. Nature 191, 474-476. doi: 10.1038/191474a0
52. Maheu, F. S., Dozier, M., Guyer, A. E., Mandell, D., Peloso, E., Poeth, K., et al. (2010). A preliminary study of medial temporal lobe function in youths with a history of caregiver deprivation and emotional neglect. Cogn. Affect. Behav. Neurosci. 10, 34-49. doi: 10.3758/CABN.10.1.34
53. Malatynska, E., and Knapp, R. J. (2005). Dominant-submissive behavior as models of mania and depression. Neurosci. Biobehav. Rev. 29, 715-737. doi: 10.1016/j.neubiorev.2005.03.014
54. Malkesman, O., Maayan, R., Weizman, A., and Weller, A. (2006). Aggressive behavior and HPA axis hormones after social isolation in adult rats of two different genetic animal models for depression. Behav. Brain Res. 175, 408-414. doi: 10.1016/j.bbr.2006.09.017
55. Marmendal, M., Eriksson, C. J., and Fahlke, C. (2006). Early deprivation increases exploration and locomotion in adult male Wistar offspring. Pharmacol. Biochem. Behav. 85, 535-544. doi: 10.1016/j.pbb.2006.10.005
56. Marusak, H. A., Martin, K. R., Etkin, A., and Thomason, M. E. (2014). Childhood trauma exposure disrupts the automatic regulation of emotional processing. Neuropsychopharmacology. doi: 10.1038/npp.2014.311. [Epub ahead of print].
57. Matthews, S. G. (2002). Early programming of the hypothalamo-pituitary-adrenal axis. Trends Endocrinol. Metab. 13, 373-380. doi: 10.1016/S1043-2760(02)00690-2
58. Mikics, E., Barsy, B., and Haller, J. (2007). The effect glucocorticoids on aggressiveness in established colonies of rats. Psychoneuroendocrinology 32, 160-170. doi: 10.1016/j.psyneuen.2006.12.002
59. Mikics, E., Kruk, M. R., and Haller, J. (2004). Genomic and non-genomic effects of glucocorticoids on aggressive behavior in male rats. Psychoneuroendocrinology 29, 618-635. doi: 10.1016/S0306-4530(03)00090-8
60. Millstein, R. A., Ralph, R. J., Yang, R. J., and Holmes, A. (2006). Effects of repeated maternal separation on prepulse inhibition of startle across inbred mouse strains. Genes Brain Behav. 5, 346-354. doi: 10.1111/j.1601-183X.2005.00172.x
61. Moore, R. W., Parsons, J. A., Bookstaff, R. C., and Peterson, R. E. (1989). Plasma concentrations of pituitary hormones in 2,3,7,8-tetrachlorodibenzo-p-dioxin-treated male rats. J. Biochem. Toxicol. 4, 165-172. doi: 10.1002/jbt.2570040305
62. Murray, E. A. (2007). The amygdala, reward and emotion. Trends Cogn. Sci. 11, 489-497. doi: 10.1016/j.tics.2007.08.013
63. Mustoe, A. C., Taylor, J. H., Birnie, A. K., Huffman, M. C., and French, J. A. (2014). Gestational cortisol and social play shape development of marmosets' HPA functioning and behavioral responses to stressors. Dev. Psychobiol. 56, 1229-1243. doi: 10.1002/dev.21203
64. Nelson, R. J., and Trainor, B. C. (2007). Neural mechanisms of aggression. Nat. Rev. Neurosci. 8, 536-546. doi: 10.1038/nrn2174
65. Ohayon, S., Avni, O., Taylor, A. L., Perona, P., and Roian Egnor, S. E. (2013). Automated multi-day tracking of marked mice for the analysis of social behaviour. J. Neurosci. Methods 219, 10-19. doi: 10.1016/j.jneumeth.2013.05.013
66. Pitt, J. A., Buckalew, A. R., House, D. E., and Abbott, B. D. (2000). Adrenocorticotropin (ACTH) and corticosterone secretion by perifused pituitary and adrenal glands from rodents exposed to 2,3,7, 8-tetrachlorodibenzo-p-dioxin (TCDD). Toxicology 151, 25-35. doi: 10.1016/S0300-483X(00)00257-2
67. Poimenova, A., Markaki, E., Rahiotis, C., and Kitraki, E. (2010). Corticosterone-regulated actions in the rat brain are affected by perinatal exposure to low dose of bisphenol A. Neuroscience 167, 741-749. doi: 10.1016/j.neuroscience.2010.02.051
68. Pryce, C. R., Aubert, Y., Maier, C., Pearce, P. C., and Fuchs, E. (2011). The developmental impact of prenatal stress, prenatal dexamethasone and postnatal social stress on physiology, behaviour and neuroanatomy of primate offspring: studies in rhesus macaque and common marmoset. Psychopharmacology (Berl) 214, 33-53. doi: 10.1007/s00213-010-1989-2
69. Pryce, C. R., and Feldon, J. (2003). Long-term neurobehavioural impact of the postnatal environment in rats: manipulations, effects and mediating mechanisms. Neurosci. Biobehav. Rev. 27, 57-71. doi: 10.1016/S0149-7634(03)00009-5
70. Rees, S. L., Akbari, E., Steiner, M., and Fleming, A. S. (2008). Effects of early deprivation and maternal separation on pup-directed behavior and HPA axis measures in the juvenile female rat. Dev. Psychobiol. 50, 315-321. doi: 10.1002/dev.20292
71. Rees, S. L., Steiner, M., and Fleming, A. S. (2006). Early deprivation, but not maternal separation, attenuates rise in corticosterone levels after exposure to a novel environment in both juvenile and adult female rats. Behav. Brain Res. 175, 383-391. doi: 10.1016/j.bbr.2006.09.013
72. Rincon-Cortes, M., and Sullivan, R. M. (2014). Early life trauma and attachment: immediate and enduring effects on neurobehavioral and stress axis development. Front. Endocrinol. (Lausanne) 5:33. doi: 10.3389/fendo.2014.00033
73. Rowell, T. E. (1974). The concept of social dominance. Behav. Biol. 11, 131-154. doi: 10.1016/S0091-6773(74)90289-2
74. Ruedi-Bettschen, D., Feldon, J., and Pryce, C. R. (2004). Circadian- and temperature-specific effects of early deprivation on rat maternal care and pup development: short-term markers for long-term effects? Dev. Psychobiol. 45, 59-71. doi: 10.1002/dev.20014
75. Ruedi-Bettschen, D., Zhang, W., Russig, H., Ferger, B., Weston, A., Pedersen, E. M., et al. (2006). Early deprivation leads to altered behavioural, autonomic and endocrine responses to environmental challenge in adult Fischer rats. Eur. J. Neurosci. 24, 2879-2893. doi: 10.1111/j.1460-9568.2006.05158.x
76. Sapolsky, R. M., Alberts, S. C., and Altmann, J. (1997). Hypercortisolism associated with social subordinance or social isolation among wild baboons. Arch. Gen. Psychiatry 54, 1137-1143. doi: 10.1001/archpsyc.1997.01830240097014
77. Savonenko, A., Filipkowski, R. K., Werka, T., Zielinski, K., and Kaczmarek, L. (1999). Defensive conditioning-related functional heterogeneity among nuclei of the rat amygdala revealed by c-Fos mapping. Neuroscience 94, 723-733. doi: 10.1016/S0306-4522(99)00331-0
78. Shang, J., Fu, Y., Ren, Z., Zhang, T., Du, M., Gong, Q., et al. (2014). The common traits of the ACC and PFC in anxiety disorders in the DSM-5: meta-analysis of voxel-based morphometry studies. PLoS ONE 9:e93432. doi: 10.1371/journal.pone.0093432
79. Shridhar, S., Farley, A., Reid, R. L., Foster, W. G., and Van Vugt, D. A. (2001). The effect of 2,3,7,8-tetrachlorodibenzo-p-dioxin on corticotrophin-releasing hormone, arginine vasopressin, and pro-opiomelanocortin mRNA levels in the hypothalamus of the cynomolgus monkey. Toxicol. Sci. 63, 181-188. doi: 10.1093/toxsci/63.2.181
80. Suzuki, H., Luby, J. L., Botteron, K. N., Dietrich, R., McAvoy, M. P., and Barch, D. M. (2014). Early life stress and trauma and enhanced limbic activation to emotionally valenced faces in depressed and healthy children. J. Am. Acad. Child Adolesc. Psychiatry 53, 800.e10-813.e10. doi: 10.1016/j.jaac.2014.04.013
81. Takeda, T., Taura, J., Hattori, Y., Ishii, Y., and Yamada, H. (2014). Dioxin-induced retardation of development through a reduction in the expression of pituitary hormones and possible involvement of an aryl hydrocarbon receptor in this defect: a comparative study using two strains of mice with different sensitivities to dioxin. Toxicol. Appl. Pharmacol. 278, 220-229. doi: 10.1016/j.taap.2014.04.022
82. Timmer, M., Cordero, M. I., Sevelinges, Y., and Sandi, C. (2011). Evidence for a role of oxytocin receptors in the long-term establishment of dominance hierarchies. Neuropsychopharmacology 36, 2349-2356. doi: 10.1038/npp.2011.125
83. Toth, M., Tulogdi, A., Biro, L., Soros, P., Mikics, E., and Haller, J. (2012). The neural background of hyper-emotional aggression induced by post-weaning social isolation. Behav. Brain Res. 233, 120-129. doi: 10.1016/j.bbr.2012.04.025
84. Tottenham, N. (2012). Human amygdala development in the absence of species-expected caregiving. Dev. Psychobiol. 54, 598-611. doi: 10.1002/dev.20531
85. Truitt, W., Sajdyk, T., Dietrich, A., Oberlin, B., McDougle, C., and Shekhar, A. (2007). From anxiety to autism: spectrum of abnormal social behaviors modeled by progressive disruption of inhibitory neuronal function in the basolateral amygdala in Wistar rats. Psychopharmacology(Berl) 191, 107-118. doi: 10.1007/s00213-006-0674-y
86. Tzanoulinou, S., Riccio, O., de Boer, M. W., and Sandi, C. (2014). Peripubertal stress-induced behavioral changes are associated with altered expression of genes involved in excitation and inhibition in the amygdala. Transl. Psychiatry 4, e410. doi: 10.1038/tp.2014.54
87. Veenema, A. H. (2012). Toward understanding how early-life social experiences alter oxytocin- and vasopressin-regulated social behaviors. Horm. Behav. 61, 304-312. doi: 10.1016/j.yhbeh.2011.12.002
88. Veenit, V., Cordero, M. I., Tzanoulinou, S., and Sandi, C. (2013). Increased corticosterone in peripubertal rats leads to long-lasting alterations in social exploration and aggression. Front. Behav. Neurosci. 7:26. doi: 10.3389/fnbeh.2013.00026
89. Wang, F., Zhu, J., Zhu, H., Zhang, Q., Lin, Z., and Hu, H. (2011). Bidirectional control of social hierarchy by synaptic efficacy in medial prefrontal cortex. Science 334, 693-697. doi: 10.1126/science.1209951
90. Wedig, M. M., Rauch, S. L., Albert, M. S., and Wright, C. I. (2005). Differential amygdala habituation to neutral faces in young and elderly adults. Neurosci. Lett. 385, 114-119. doi: 10.1016/j.neulet.2005.05.039
91. Weissbrod, A., Shapiro, A., Vasserman, G., Edry, L., Dayan, M., Yitzhaky, A., et al. (2013). Automated long-term tracking and social behavioural phenotyping of animal colonies within a semi-natural environment. Nat. Commun. 4, 2018. doi: 10.1038/ncomms3018
92. Xu, X., Hong, X., Xie, L., Li, T., Yang, Y., Zhang, Q., et al. (2012). Gestational and lactational exposure to bisphenol-A affects anxiety- and depression-like behaviors in mice. Horm. Behav. 62, 480-490. doi: 10.1016/j.yhbeh.2012.08.005
93. Zink, C. F., Tong, Y., Chen, Q., Bassett, D. S., Stein, J. L., and Meyer-Lindenberg, A. (2008). Know your place: neural processing of social hierarchy in humans. Neuron 58, 273-283. doi: 10.1016/j.neuron.2008.01.025