Increased corticosterone in peripubertal rats leads to long-lasting alterations in social exploration and aggression

Frontiers in Behavioral Neuroscience

Volumn , Issue MAR, 2013, Pages

  Veenit, Vandana ^a   Cordero, Maria Isabel ^a,b   Tzanoulinou, Stamatina ^a   Sandi, Carmen ^a  

^a EPFL   (Switzerland)

^b GENEVA UNIVERSITY HOSPITALS   (Switzerland)

Author keywords

Adolescence; Aggressive behavior; Corticosterone; Emotion; Puberty; Sociability; Stress

Indexed keywords

CORTICOSTERONE;

AGGRESSION; ANIMAL EXPERIMENT; ANXIETY; ARTICLE; CONTROLLED STUDY; CORTICOSTERONE BLOOD LEVEL; DEPRESSION; EMOTIONALITY; EXPLORATORY BEHAVIOR; FORCED SWIMMING TEST; HORMONE RESPONSE; MALE; MOTIVATION; NERVE CELL PLASTICITY; NONHUMAN; PLAY; PUBERTY; RAT; SOCIAL BEHAVIOR; SOCIAL INTERACTION; SOCIAL PREFERENCE; SOCIAL STRESS;

EID: 84875483107     PISSN: 16625153     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnbeh.2013.00026     Document Type: Article

References (61)

1. Bazak, N., Kozlovsky, N., Kaplan, Z., Matar, M., Golan, H., Zohar, J., Richter-Levin, G., and Cohen, H. (2009). Pre-pubertal stress exposure affects adult behavioral response in association with changes in circulating corticosterone and brain-derived neurotrophic factor. Psychoneuroendocrinology 34, 844-858.
2. Caspi, A., Mcclay, J., Moffitt, T.E., Mill, J., Martin, J., Craig, I.W., Taylor, A., and Poulton, R. (2002). Role of genotype in the cycle of violence in maltreated children. Science 297, 851-854.
3. Cordero, M.I., Poirier, G.L., Marquez, C., Veenit, V., Fontana, X., Salehi, B., Ansermet, F., and Sandi, C. (2012). Evidence for biological roots in the transgenerational transmission of intimate partner violence. Transl Psychiatry 2, e106.
4. David, D.J., Samuels, B.A., Rainer, Q., Wang, J.W., Marsteller, D., Mendez, I., Drew, M., Craig, D.A., Guiard, B.P., Guilloux, J.P., Artymyshyn, R.P., Gardier, A.M., Gerald, C., Antonijevic, I.A., Leonardo, E.D., and Hen, R. (2009). Neurogenesis-dependent and -independent effects of fluoxetine in an animal model of anxiety/depression. Neuron 62, 479-493.
5. De Kloet, E.R., Karst, H., and Joels, M. (2008). Corticosteroid hormones in the central stress response: quick-and-slow. Front Neuroendocrinol 29, 268-272.
6. Giedd, J.N. (2004). Structural magnetic resonance imaging of the adolescent brain. Ann N Y Acad Sci 1021, 77-85.
7. Gogtay, N., Giedd, J.N., Lusk, L., Hayashi, K.M., Greenstein, D., Vaituzis, A.C., Nugent, T.F., 3rd, Herman, D.H., Clasen, L.S., Toga, A.W., Rapoport, J.L., and Thompson, P.M. (2004). Dynamic mapping of human cortical development during childhood through early adulthood. Proc Natl Acad Sci U S A 101, 8174-8179.
8. Foilb, A.R., Lui, P., and Romeo, R.D. (2011). The transformation of hormonal stress responses throughout puberty and adolescence. J Endocrinol 210, 391-398.
9. Golier, J., and Yehuda, R. (1998). Neuroendocrine activity and memory-related impairments in posttraumatic stress disorder. Dev Psychopathol 10, 857-869.
10. Haller, J., Albert, I., and Makara, G.B. (1997). Acute behavioural effects of corticosterone lack specificity but show marked context-dependency. J Neuroendocrinol 9, 515-518.
11. Haller, J., Mikics, E., and Makara, G.B. (2008). The effects of non-genomic glucocorticoid mechanisms on bodily functions and the central neural system. A critical evaluation of findings. Front Neuroendocrinol 29, 273-291.
12. Hamilton, L.D., Newman, M.L., Delville, C.L., and Delville, Y. (2008). Physiological stress response of young adults exposed to bullying during adolescence. Physiol Behav 95, 617-624.
13. Heim, C., and Nemeroff, C.B. (2001). The role of childhood trauma in the neurobiology of mood and anxiety disorders: preclinical and clinical studies. Biol Psychiatry 49, 1023-1039.
14. Heim, C., Newport, D.J., Bonsall, R., Miller, A.H., and Nemeroff, C.B. (2001). Altered pituitary-adrenal axis responses to provocative challenge tests in adult survivors of childhood abuse. Am J Psychiatry 158, 575-581.
15. Hong, S., Flashner, B., Chiu, M., Ver Hoeve, E., Luz, S., and Bhatnagar, S. (2012). Social isolation in adolescence alters behaviors in the forced swim and sucrose preference tests in female but not in male rats. Physiol Behav 105, 269-275.
16. Juarez, J., and Vazquez-Cortes, C. (2010). Corticosterone treatment before puberty sensitizes the effect of oral methylphenidate on locomotor activity in preadolescence and produces differential effects in adulthood. Brain Res 1346, 195-203.
17. Jacobson-Pick, S., and Richter-Levin, G. (2010). Differential impact of juvenile stress and corticosterone in juvenility and in adulthood, in male and female rats. Behav Brain Res 214, 268-276.
18. Joels, M., and Vreugdenhil, E. (1998). Corticosteroids in the brain. Cellular and molecular actions. Mol Neurobiol 17, 87-108.
19. Johnson, S.A., Fournier, N.M., and Kalynchuk, L.E. (2006). Effect of different doses of corticosterone on depression-like behavior and HPA axis responses to a novel stressor. Behav Brain Res 168, 280-288.
20. Jonson-Reid, M., Presnall, N., Drake, B., Fox, L., Bierut, L., Reich, W., Kane, P., Todd, R.D., and Constantino, J.N. (2010). Effects of child maltreatment and inherited liability on antisocial development: an official records study. J Am Acad Child Adolesc Psychiatry 49, 321-332; quiz 431.
21. Lukkes, J.L., Mokin, M.V., Scholl, J.L., and Forster, G.L. (2009). Adult rats exposed to earlylife social isolation exhibit increased anxiety and conditioned fear behavior, and altered hormonal stress responses. Horm Behav 55, 248-256.
22. Marks, W., Fournier, N.M., and Kalynchuk, L.E. (2009). Repeated exposure to corticosterone increases depression-like behavior in two different versions of the forced swim test without altering nonspecific locomotor activity or muscle strength. Physiol Behav 98, 67-72.
23. Marquez, C., Poirier, G.L., Cordero, M.I., Larsen, M.H., Groner, A., Marquis, J., Magistretti, P.J., Trono, D., and Sandi, C. (2013). Peripuberty stress leads to abnormal aggression, altered amygdala and orbitofrontal reactivity and increased prefrontal MAOA gene expression. Transl Psychiatry 3, e216.
24. Mccormick, C.M., Smith, C., and Mathews, I.Z. (2008). Effects of chronic social stress in adolescence on anxiety and neuroendocrine response to mild stress in male and female rats. Behav Brain Res 187, 228-238.
25. 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.
26. Mikics, E., Barsy, B., and Haller, J. (2007). The effect glucocorticoids on aggressiveness in established colonies of rats. Psychoneuroendocrinology 32, 160-170.
27. Moy, S.S., Nadler, J.J., Perez, A., Barbaro, R.P., Johns, J.M., Magnuson, T.R., Piven, J., and Crawley, J.N. (2004). Sociability and preference for social novelty in five inbred strains: an approach to assess autistic-like behavior in mice. Genes Brain Behav 3, 287-302.
28. Pellis, S.M., and Pellis, V.C. (1990). Differential rates of attack, defense, and counterattack during the developmental decrease in play fighting by male and female rats. Dev Psychobiol 23, 215-231.
29. Pellow, S., and File, S.E. (1986). Anxiolytic and anxiogenic drug effects on exploratory activity in an elevated plus-maze: a novel test of anxiety in the rat. Pharmacol Biochem Behav 24, 525-529.
30. Perepletchikova, F., and Kaufman, J. (2010). Emotional and behavioral sequelae of childhood maltreatment. Curr Opin Pediatr 22, 610-615.
31. Porsolt, R.D., Bertin, A., and Jalfre, M. (1977). Behavioral despair in mice: a primary screening test for antidepressants. Arch Int Pharmacodyn Ther 229, 327-336.
32. Resnick, H.S., Yehuda, R., Pitman, R.K., and Foy, D.W. (1995). Effect of previous trauma on acute plasma cortisol level following rape. Am J Psychiatry 152, 1675-1677.
33. Rinne, T., De Kloet, E.R., Wouters, L., Goekoop, J.G., Derijk, R.H., and Van Den Brink, W. (2002). Hyperresponsiveness of hypothalamic-pituitary-adrenal axis to combined dexamethasone/corticotropin-releasing hormone challenge in female borderline personality disorder subjects with a history of sustained childhood abuse. Biol Psychiatry 52, 1102-1112.
34. Romeo, R.D., Richardson, H.N., and Sisk, C.L. (2002). Puberty and the maturation of the male brain and sexual behavior: recasting a behavioral potential. Neurosci Biobehav Rev 26, 381-391.
35. Romeo, R.D. (2003). Puberty: a period of both organizational and activational effects of steroid hormones on neurobehavioural development. J Neuroendocrinol 15, 1185-1192.
36. Romeo, R.D. (2005). Neuroendocrine and behavioral development during puberty: a tale of two axes. Vitam Horm 71, 1-25.
37. Ros-Simo, C., and Valverde, O. (2012). Early-life social experiences in mice affect emotional behaviour and hypothalamic-pituitary-adrenal axis function. Pharmacol Biochem Behav 102, 434-441.
38. Sandi, C. (2011). Glucocorticoids act on glutamatergic pathways to affect memory processes. Trends Neurosci 34, 165-176.
39. Schmidt, M.V., Sterlemann, V., Ganea, K., Liebl, C., Alam, S., Harbich, D., Greetfeld, M., Uhr, M., Holsboer, F., and Muller, M.B. (2007). Persistent neuroendocrine and behavioral effects of a novel, etiologically relevant mouse paradigm for chronic social stress during adolescence. Psychoneuroendocrinology 32, 417-429.
40. Schmidt, M.V., Wang, X.D., and Meijer, O.C. (2011). Early life stress paradigms in rodents: potential animal models of depression? Psychopharmacology (Berl) 214, 131-140.
41. Spear, L.P. (2000). The adolescent brain and age-related behavioral manifestations. Neurosci Biobehav Rev 24, 417-463.
42. Stein-Behrens, B., Mattson, M.P., Chang, I., Yeh, M., and Sapolsky, R. (1994). Stress exacerbates neuron loss and cytoskeletal pathology in the hippocampus. J Neurosci 14, 5373-5380.
43. Suzuki, M., Hagino, H., Nohara, S., Zhou, S.Y., Kawasaki, Y., Takahashi, T., Matsui, M., Seto, H., Ono, T., and Kurachi, M. (2005). Male-specific volume expansion of the human hippocampus during adolescence. Cereb Cortex 15, 187-193.
44. Tarullo, A.R., and Gunnar, M.R. (2006). Child maltreatment and the developing HPA axis. Horm Behav 50, 632-639.
45. Toledo-Rodriguez, M., and Sandi, C. (2011). Stress during Adolescence Increases Novelty Seeking and Risk-Taking Behavior in Male and Female Rats. Front Behav Neurosci 5, 17
46. Toledo-Rodriguez, M., Pitiot, A., Paus, T., and Sandi, C. (2012). Stress during puberty boosts metabolic activation associated with fear-extinction learning in hippocampus, basal amygdala and cingulate cortex. Neurobiol Learn Mem 98, 93-101.
47. Trezza, V., and Vanderschuren, L.J. (2008). Bidirectional cannabinoid modulation of social behavior in adolescent rats. Psychopharmacology (Berl) 197, 217-227.
48. Trickett, P.K., Noll, J.G., Susman, E.J., Shenk, C.E., and Putnam, F.W. (2010). Attenuation of cortisol across development for victims of sexual abuse. Dev Psychopathol 22, 165-175.
49. Tsoory, M., Cohen, H., and Richter-Levin, G. (2007). Juvenile stress induces a predisposition to either anxiety or depressive-like symptoms following stress in adulthood. Eur Neuropsychopharmacol 17, 245-256.
50. Veenema, A.H., Blume, A., Niederle, D., Buwalda, B., and Neumann, I.D. (2006). Effects of early life stress on adult male aggression and hypothalamic vasopressin and serotonin. Eur J Neurosci 24, 1711-1720.
51. Veenema, A.H., and Neumann, I.D. (2009). Maternal separation enhances offensive playfighting, basal corticosterone and hypothalamic vasopressin mRNA expression in juvenile male rats. Psychoneuroendocrinology 34, 463-467.
52. Venero, C., Guaza, C., and Sandi, C. (1996). Regional and temporal modulation of brain glycoprotein synthesis by corticosterone. Neuroreport 7, 2819-2822.
53. Watt, M.J., Burke, A.R., Renner, K.J., and Forster, G.L. (2009). Adolescent male rats exposed to social defeat exhibit altered anxiety behavior and limbic monoamines as adults. Behav Neurosci 123, 564-576.
54. Wommack, J.C., and Delville, Y. (2003). Repeated social stress and the development of agonistic behavior: individual differences in coping responses in male golden hamsters. Physiol Behav 80, 303-308.
55. Wommack, J.C., Salinas, A., Melloni, R.H., Jr., and Delville, Y. (2004). Behavioural and neuroendocrine adaptations to repeated stress during puberty in male golden hamsters. J Neuroendocrinol 16, 767-775.
56. Wommack, J.C., Salinas, A., and Delville, Y. (2005). Glucocorticoids and the development of agonistic behaviour during puberty in male golden hamsters. J Neuroendocrinol 17, 781-787.
57. Wommack, J.C., and Delville, Y. (2007). Cortisol controls the pubertal development of agonistic behavior in male golden hamsters via type II corticosteroid receptors. Horm Behav 51, 306-312.
58. Yehuda, R., Teicher, M.H., Trestman, R.L., Levengood, R.A., and Siever, L.J. (1996). Cortisol regulation in posttraumatic stress disorder and major depression: a chronobiological analysis. Biol Psychiatry 40, 79-88.
59. Yehuda, R., Kahana, B., Binder-Brynes, K., Southwick, S.M., Mason, J.W., and Giller, E.L. (1995). Low urinary cortisol excretion in Holocaust survivors with posttraumatic stress disorder. Am J Psychiatry 152, 982-986.
60. Yehuda, R., Southwick, S.M., Nussbaum, G., Wahby, V., Giller, E.L., Jr., and Mason, J.W. (1990). Low urinary cortisol excretion in patients with posttraumatic stress disorder. J Nerv Ment Dis 178, 366-369.
61. Zhao, Y., Ma, R., Shen, J., Su, H., Xing, D., and Du, L. (2008). A mouse model of depression induced by repeated corticosterone injections. Eur J Pharmacol 581, 113-120.