Cited by 68Stress Responses and CortisolNeuroendocrine regulation and behaviorChild Abuse and Trauma

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

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Veenit, Vandana, Cordero, Maria I., Tzanoulinou, Stamatina, Sandi, Carmen·2013·Frontiers in Behavioral Neuroscience

Abstract

Stress during childhood and adolescence enhances the risk of psychopathology later in life. We have previously shown that subjecting male rats to stress during the peripubertal period induces long-lasting effects on emotion and social behaviors. As corticosterone is increased by stress and known to exert important programming effects, we reasoned that increasing corticosterone might mimic the effects of peripubertal stress. To this end, we injected corticosterone (5 mg/kg) on 7 scattered days during the peripuberty period (P28-P30, P34, P36, P40, and P42), following the same experimental schedule as for stress administration in our peripubertal paradigm. We measured play behavior in the homecage and, at adulthood, the corticosterone response to novelty and behavioral responses in tests for anxiety- and depression-like behaviors, aggression, and social exploration. As compared to vehicle, corticosterone-treated animals exhibit more aggressive play behavior during adolescence, increased aggressive behavior in a resident-intruder (RI) test while reduced juvenile exploration and corticosterone reactivity at adulthood. Whereas the corticosterone treatment mimicked alterations induced by the peripuberty stress protocol in the social domain, it did not reproduce previously observed effects of peripuberty stress on increasing anxiety-like and depression-like behaviors, respectively evaluated in the elevated plus maze (EPM) and the forced swim tests. Our findings indicate that increasing corticosterone levels during peripuberty might be instrumental to program alterations in the social domain observed following stress, whereas other factors might need to be recruited for the programming of long-term changes in emotionality. Our study opens the possibility that individual differences on the degree of glucocorticoid activation during peripuberty might be central to defining differences in vulnerability to develop psychopathological disorders coursing with alterations in the social realm.

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Research works printed but not linked: 53

  1. Bazak N. Kozlovsky N. Kaplan Z. Matar M. Golan H. Zohar J. (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 10.1016/j.psyneuen.2008.12.018 19181453 · DOI
  2. Caspi A. McClay J. Moffitt T. E. Mill J. Martin J. Craig I. W. (2002). Role of genotype in the cycle of violence in maltreated children. Science 297, 851– 854 10.1126/science.1072290 12161658 · DOI · Paper page
  3. Coppens C. M. Siripornmongcolchai T. Wibrand K. Alme M. N. Buwalda B. De Boer S. F. (2011). Social defeat during adolescence and adulthood differentially induce BDNF-regulated immediate early genes. Front. Behav. Neurosci. 5: 72 10.3389/fnbeh.2011.00072 22065953 PMC3206404 · DOI · Paper page
  4. Cordero M. I. Poirier G. L. Marquez C. Veenit V. Fontana X. Salehi B. (2012). Evidence for biological roots in the transgenerational transmission of intimate partner violence. Transl. Psychiatry 2, e106 10.1038/tp.2012.32 22832906 PMC3337076 · DOI · Paper page
  5. David D. J. Samuels B. A. Rainer Q. Wang J. W. Marsteller D. Mendez I. (2009). Neurogenesis-dependent and -independent effects of fluoxetine in an animal model of anxiety/depression. Neuron 62, 479– 493 10.1016/j.neuron.2009.04.017 19477151 PMC2759281 · DOI · Paper page
  6. Diamantopoulou A. Raftogianni A. Stamatakis A. Alikaridis F. Oitzl M. S. Stylianopoulou F. (2012). Denial of reward in the neonate shapes sociability and serotonergic activity in the adult rat. PLoS ONE 7: e33793 10.1371/journal.pone.0033793 22479443 PMC3313948 · DOI
  7. Foilb A. R. Lui P. Romeo R. D. (2011). The transformation of hormonal stress responses throughout puberty and adolescence. J. Endocrinol. 210, 391– 398 10.1530/JOE-11-0206 21746793 · DOI · Paper page
  8. Giedd J. N. (2004). Structural magnetic resonance imaging of the adolescent brain. Ann. N.Y. Acad. Sci. 1021, 77– 85 10.1196/annals.1308.009 15251877 · DOI · Paper page
  9. Golier J. Yehuda R. (1998). Neuroendocrine activity and memory-related impairments in posttraumatic stress disorder. Dev. Psychopathol. 10, 857– 869 9886230
  10. Haller J. Albert I. Makara G. B. (1997). Acute behavioural effects of corticosterone lack specificity but show marked context-dependency. J. Neuroendocrinol. 9, 515– 518 15305568
  11. Haller J. Mikics E. 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. 10.1016/j.yfrne.2007.10.004 18054070 · DOI
  12. Hamilton L. D. Newman M. L. Delville C. L. Delville Y. (2008). Physiological stress response of young adults exposed to bullying during adolescence. Physiol. Behav. 95, 617– 624 10.1016/j.physbeh.2008.09.001 18809422 · DOI
  13. Heim C. 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 11430844
  14. Heim C. Newport D. J. Bonsall R. Miller A. H. 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 10.1176/appi.ajp.158.4.575 11282691 · DOI · Paper page
  15. Hong S. Flashner B. Chiu M. Ver Hoeve E. Luz S. 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 10.1016/j.physbeh.2011.08.036 21907226 PMC3260053 · DOI
  16. Jacobson-Pick S. 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 10.1016/j.bbr.2010.05.036 20561965 · DOI
  17. Joels M. Vreugdenhil E. (1998). Corticosteroids in the brain. Cellular and molecular actions. Mol. Neurobiol. 17, 87– 108 10.1007/BF02802026 9887448 · DOI
  18. Johnson S. A. Fournier N. M. 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 10.1016/j.bbr.2005.11.019 16386319 · DOI
  19. Jonson-Reid M. Presnall N. Drake B. Fox L. Bierut L. Reich W. (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. 20410725 PMC2878182
  20. Juarez J. 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 10.1016/j.brainres.2010.05.093 20553877 · DOI
  21. Lukkes J. L. Mokin M. V. Scholl J. L. Forster G. L. (2009). Adult rats exposed to early-life social isolation exhibit increased anxiety and conditioned fear behavior, and altered hormonal stress responses. Horm. Behav. 55, 248– 256 10.1016/j.yhbeh.2008.10.014 19027017 · DOI
  22. Marks W. Fournier N. M. 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 10.1016/j.physbeh.2009.04.014 19393673 · DOI
  23. Márquez C. Poirier G. L. Cordero M. I. Larsen M. H. Groner A. Marquis J. (2013). Peripuberty stress leads to abnormal aggression, altered amygdala and orbitofrontal reactivity and increased prefrontal MAOA gene expression. Transl. Psychiatry 3, e216 10.1038/tp.2012.144 23321813 PMC3566724 · DOI · Paper page
  24. McCormick C. M. Smith C. 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 10.1016/j.bbr.2007.09.005 17945360 · DOI
  25. Mikics E. Barsy B. Haller J. (2007). The effect glucocorticoids on aggressiveness in established colonies of rats. Psychoneuroendocrinology 32, 160– 170 10.1016/j.psyneuen.2006.12.002 17275197 · DOI
  26. Mikics E. Kruk M. R. Haller J. (2004). Genomic and non-genomic effects of glucocorticoids on aggressive behavior in male rats. Psychoneuroendocrinology 29, 618– 635 10.1016/S0306-4530(03)00090-8 15041085 · DOI
  27. Pellis S. M. 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 10.1002/dev.420230303 2379760 · DOI · Paper page
  28. Pellow S. 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 10.1016/0091-3057(86)90552-6 2871560 · DOI
  29. Perepletchikova F. Kaufman J. (2010). Emotional and behavioral sequelae of childhood maltreatment. Curr. Opin. Pediatr. 22, 610– 615 10.1097/MOP.0b013e32833e148a 20736837 PMC4113480 · DOI
  30. Porsolt R. D. Bertin A. Jalfre M. (1977). Behavioral despair in mice: a primary screening test for antidepressants. Arch. Int. Pharmacodyn. Ther. 229, 327– 336 596982
  31. Resnick H. S. Yehuda R. Pitman R. K. Foy D. W. (1995). Effect of previous trauma on acute plasma cortisol level following rape. Am. J. Psychiatry 152, 1675– 1677 7485635
  32. Romeo R. D. (2003). Puberty: a period of both organizational and activational effects of steroid hormones on neurobehavioural development. J. Neuroendocrinol. 15, 1185– 1192 10.1111/j.1365-2826.2003.01106.x 14636181 · DOI · Paper page
  33. Romeo R. D. (2005). Neuroendocrine and behavioral development during puberty: a tale of two axes. Vitam. Horm. 71, 1– 25 10.1016/S0083-6729(05)71001-3 16112263 · DOI
  34. Ros-Simo C. Valverde O. (2012). Early-life social experiences in mice affect emotional behaviour and hypothalamic-pituitary-adrenal axis function. Pharmacol. Biochem. Behav. 102, 434– 441 10.1016/j.pbb.2012.06.001 22691868 · DOI
  35. Sandi C. (2011). Glucocorticoids act on glutamatergic pathways to affect memory processes. Trends Neurosci. 34, 165– 176 10.1016/j.tins.2011.01.006 21377221 · DOI
  36. Schmidt M. V. Sterlemann V. Ganea K. Liebl C. Alam S. Harbich D. (2007). Persistent neuroendocrine and behavioral effects of a novel, etiologically relevant mouse paradigm for chronic social stress during adolescence. Psychoneuroendocrinology 32, 417– 429 10.1016/j.psyneuen.2007.02.011 17449187 · DOI
  37. Schmidt M. V. Wang X. D. Meijer O. C. (2011). Early life stress paradigms in rodents: potential animal models of depression? Psychopharmacology (Berl.) 214, 131– 140 10.1007/s00213-010-2096-0 21086114 · DOI
  38. Spear L. P. (2000). The adolescent brain and age-related behavioral manifestations. Neurosci. Biobehav. Rev. 24, 417– 463 10.1016/S0149-7634(00)00014-2 10817843 · DOI · Paper page
  39. Suzuki M. Hagino H. Nohara S. Zhou S. Y. Kawasaki Y. Takahashi T. (2005). Male-specific volume expansion of the human hippocampus during adolescence. Cereb. Cortex 15, 187– 193 10.1093/cercor/bhh121 15238436 · DOI
  40. Tarullo A. R. Gunnar M. R. (2006). Child maltreatment and the developing HPA axis. Horm. Behav. 50, 632– 639 10.1016/j.yhbeh.2006.06.010 16876168 · DOI · Paper page
  41. Toledo-Rodriguez M. Pitiot A. Paus T. 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 10.1016/j.nlm.2012.05.006 22664720 · DOI
  42. Trezza V. Vanderschuren L. J. (2008). Bidirectional cannabinoid modulation of social behavior in adolescent rats. Psychopharmacology (Berl.) 197, 217– 227 10.1007/s00213-007-1025-3 18058088 · DOI · Paper page
  43. Tsoory M. Cohen H. 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 10.1016/j.euroneuro.2006.06.007 16889944 · DOI
  44. Veenema A. H. Blume A. Niederle D. Buwalda B. Neumann I. D. (2006). Effects of early life stress on adult male aggression and hypothalamic vasopressin and serotonin. Eur. J. Neurosci. 24, 1711– 1720 10.1111/j.1460-9568.2006.05045.x 17004935 · DOI · Paper page
  45. Veenema A. H. Neumann I. D. (2009). Maternal separation enhances offensive play-fighting, basal corticosterone and hypothalamic vasopressin mRNA expression in juvenile male rats. Psychoneuroendocrinology 34, 463– 467 10.1016/j.psyneuen.2008.10.017 19056182 · DOI · Paper page
  46. Venero C. Guaza C. Sandi C. (1996). Regional and temporal modulation of brain glycoprotein synthesis by corticosterone. Neuroreport 7, 2819– 2822 8981474
  47. Watt M. J. Burke A. R. Renner K. J. 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 10.1037/a0015752 19485563 PMC2771678 · DOI
  48. Wommack J. C. 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 10.1016/j.yhbeh.2006.11.007 17258746 · DOI
  49. Wommack J. C. Salinas A. Delville Y. (2005). Glucocorticoids and the development of agonistic behaviour during puberty in male golden hamsters. J. Neuroendocrinol. 17, 781– 787 10.1111/j.1365-2826.2005.01369.x 16280025 · DOI
  50. Wommack J. C. Salinas A. Melloni R. H. Jr. Delville Y. (2004). Behavioural and neuroendocrine adaptations to repeated stress during puberty in male golden hamsters. J. Neuroendocrinol. 16, 767– 775 10.1111/j.1365-2826.2004.01233.x 15344915 · DOI
  51. Yehuda R. Southwick S. M. Nussbaum G. Wahby V. Giller E. L. Jr. Mason J. W. (1990). Low urinary cortisol excretion in patients with posttraumatic stress disorder. J. Nerv. Ment. Dis. 178, 366– 369 2348190
  52. Yehuda R. Teicher M. H. Trestman R. L. Levengood R. A. Siever L. J. (1996). Cortisol regulation in posttraumatic stress disorder and major depression: a chronobiological analysis. Biol. Psychiatry 40, 79– 88 10.1016/0006-3223(95)00451-3 8793040 · DOI
  53. Zhao Y. Ma R. Shen J. Su H. Xing D. Du L. (2008). A mouse model of depression induced by repeated corticosterone injections. Eur. J. Pharmacol. 581, 113– 120 10.1016/j.ejphar.2007.12.005 18184609 · DOI

Cited by

Sorted by citations

Authors
Veenit, V., Cordero, M. I., Tzanoulinou, S., & Sandi, C.
Affiliations
  • École Polytechnique Fédérale de Lausanne (CH)
  • University of Geneva (CH)
Corresponding author
Sandi, Carmen
Venue
Frontiers in Behavioral Neuroscience
Published
2013
Volume
7
Pages
26-26
ISSN
1662-5153 (ISSN-L)
OpenAlex
W2120642714
Cited by
68
References
10
Citations by year
2026: 1 · 2025: 1 · 2024: 4 · 2023: 5 · 2022: 4 · 2021: 7 · 2020: 1 · 2019: 5 · 2018: 8 · 2017: 7 · 2016: 7 · 2015: 8 · 2014: 9 · 2013: 1
FWCI
3.80
Type
journal article
Language
en
Open access
Licence
cc-by
Locations
  • Frontiers in Behavioral Neuroscience (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • e-space (Manchester Metropolitan University) (submittedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Infoscience (Ecole Polytechnique Fédérale de Lausanne) (submittedVersion)
  • Infoscience (Ecole Polytechnique Fédérale de Lausanne) (submittedVersion, cc-by-nc-nd)
Funders
  • National Science Foundation
  • École Polytechnique Fédérale de Lausanne (31003AB-135710)
  • Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (122691, 120791, 135710, 310000)
Topics
  • Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
  • Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
  • Social Sciences › Psychology › Clinical Psychology › Child Abuse and Trauma
Keywords
corticosterone, social exploration, aggression, play behavior, resident-intruder test, anxiety-like behavior, depression-like behavior, adolescence, vulnerability to psychopathology, individual differences

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