Behavioral effects of chronic adolescent stress are sustained and sexually dimorphic

Hormones and Behavior

Volumn 60, Issue 1, 2011, Pages 112-120

  Bourke, Chase H ^a   Neigh, Gretchen N ^a,b,c  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b EMORY UNIVERSITY   (United States)

^c Georgia State University   (United States)

Author keywords

Adolescent stress; Anhedonia; Anxiety; Depression; HPA; HPG; Sex differences

Indexed keywords

CORTICOSTERONE; SUCROSE;

ADOLESCENT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARBOHYDRATE INTAKE; CHILD BEHAVIOR; CHRONIC STRESS; CONTROLLED STUDY; DEPRESSION; FEMALE; FORCED SWIMMING TEST; HORMONE RESPONSE; HYPERACTIVITY; IMMOBILIZATION STRESS; MALE; MAZE TEST; NONHUMAN; PRIORITY JOURNAL; RAT; SEX DIFFERENCE; SOCIAL ISOLATION;

ADOLESCENT; ADOLESCENT BEHAVIOR; ANIMALS; CORTICOSTERONE; DOMINANCE-SUBORDINATION; FEMALE; HUMANS; MALE; MAZE LEARNING; RATS; RATS, LONG-EVANS; RATS, WISTAR; RESTRAINT, PHYSICAL; SEX CHARACTERISTICS; SEX FACTORS; SOCIAL BEHAVIOR; STRESS, PSYCHOLOGICAL; SWIMMING;

EID: 79958021241     PISSN: 0018506X     EISSN: 10956867     Source Type: Journal    
DOI: 10.1016/j.yhbeh.2011.03.011     Document Type: Article

References (58)

1. Adriani W., Laviola G. A unique hormonal and behavioral hyporesponsivity to both forced novelty and d-amphetamine in periadolescent mice. Neuropharmacology 2000, 39:334-346.
2. Andersen S.L., Teicher M.H. Stress, sensitive periods and maturational events in adolescent depression. Trends Neurosci. 2008, 31:183-191.
3. Apter S.J., Eriksson C.J.P. The role of social isolation in the effects of alcohol on corticosterone and testosterone levels of alcohol-preferring and non-preferring rats. Alcohol Alcohol 2006, 41:33-38.
4. Avital A., Richter-Levin G. Exposure to juvenile stress exacerbates the behavioural consequences of exposure to stress in the adult rat. Int. J. Neuropsychopharmacol. 2005, 8:163-173.
5. Bernal-Morales B., Contreras C.M., Cueto-Escobedo J. Acute restraint stress produces behavioral despair in weanling rats in the forced swim test. Behav. Processes 2009, 82:219-222.
6. Bolhuis J.J., Fitzgerald R.E., Dijk D.J., Koolhaas J.M. The corticomedial amygdala and learning in an agonistic situation in the rat. Physiol. Behav. 1984, 32:575-579.
7. Campbell T., Lin S., DeVries C., Lambert K. Coping strategies in male and female rats exposed to multiple stressors. Physiol. Behav. 2003, 78:495-504.
8. Cruz F.C., Leão R.M., Marin M.T., Planeta C.S. Stress-induced reinstatement of amphetamine-conditioned place preference and changes in tyrosine hydroxylase in the nucleus accumbens in adolescent rats. Pharmacol. Biochem. Behav. 2010, 96:160-165.
9. DeBold J.F., Miczek K.A. Aggression persists after ovariectomy in female rats. Horm. Behav. 1984, 18:177-190.
10. Desbonnet L., Garrett L., Daly E., McDermott K.W., Dinan T.G. Sexually dimorphic effects of maternal separation stress on corticotrophin-releasing factor and vasopressin systems in the adult rat brain. Int. J. Dev. Neurosci. 2008, 26:259-268.
11. Dhom G. The prepuberal and puberal growth of the adrenal (adrenarche). Beitr. Pathol. 1973, 150:357-377.
12. Doremus-Fitzwater T.L., Varlinskaya E.I., Spear L.P. Social and non-social anxiety in adolescent and adult rats after repeated restraint. Physiol. Behav. 2009, 97:484-494.
13. Ducharme J.R., Forest M.G., De Peretti E., Sempé M., Collu R., Bertrand J. Plasma adrenal and gonadal sex steroids in human pubertal development. J. Clin. Endocrinol. Metab. 1976, 42:468-476.
14. Faruzzi A.N., Solomon M.B., Demas G.E., Huhman K.L. Gonadal hormones modulate the display of submissive behavior in socially defeated female Syrian hamsters. Horm. Behav. 2005, 47:569-575.
15. Genazzani A.R., Bernardi F., Monteleone P., Luisi S., Luisi M. Neuropeptides, neurotransmitters, neurosteroids, and the onset of puberty. Ann. N.Y. Acad. Sci. 2000, 900:1-9.
16. Gutman D.A., Nemeroff C.B. Persistent central nervous system effects of an adverse early environment: clinical and preclinical studies. Physiol. Behav. 2003, 79:471-478.
17. Haller J., Fuchs E., Halász J., Makara G.B. 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. 1999, 50:33-39.
18. Holson R., Pearce B. Principles and pitfalls in the analysis of prenatal treatment effects in multiparous species. Neurotoxicol. Teratol. 1992, 14:221-228.
19. Huhman K.L., Solomon M.B., Janicki M., Harmon A.C., Lin S.M., Israel J.E., Jasnow A.M. Conditioned defeat in male and female Syrian hamsters. Horm. Behav. 2003, 44:293-299.
20. Iwasaki-Sekino A., Mano-Otagiri A., Ohata H., Yamauchi N., Shibasaki T. Gender differences in corticotropin and corticosterone secretion and corticotropin-releasing factor mRNA expression in the paraventricular nucleus of the hypothalamus and the central nucleus of the amygdala in response to footshock stress or psychological. Psychoneuroendocrinology 2009, 34:226-237.
21. Kessler R.C., Avenevoli S., Ries Merikangas K. Mood disorders in children and adolescents: an epidemiologic perspective. Biol. Psychiatry 2001, 49:1002-1014.
22. Kinkead B., Yan F., Owens M.J., Nemeroff C.B. Endogenous neurotensin is involved in estrous cycle related alterations in prepulse inhibition of the acoustic startle reflex in female rats. Psychoneuroendocrinology 2008, 33:178-187.
23. Kinsey-Jones J.S., Li X.F., Bowe J.E., Lightman S.L., O'Byrne K.T. Corticotrophin-releasing factor type 2 receptor-mediated suppression of gonadotrophin-releasing hormone mRNA expression in GT1-7 cells. Stress 2006, 9:215-222.
24. Kirby E.D., Geraghty A.C., Ubuka T., Bentley G.E., Kaufer D. Stress increases putative gonadotropin inhibitory hormone and decreases luteinizing hormone in male rats. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:11324-11329.
25. Ladd C.O., Huot R.L., Thrivikraman K.V., Nemeroff C.B., Meaney M.J., Plotsky P.M. Long-term behavioral and neuroendocrine adaptations to adverse early experience. Prog. Brain Res. 2000, 122:81-103.
26. Laviola G., Adriani W., Morley-Fletcher S., Terranova M.L. Peculiar response of adolescent mice to acute and chronic stress and to amphetamine: evidence of sex differences. Behav. Brain Res. 2002, 130:117-125.
27. Laviola G., Macrí S., Morley-Fletcher S., Adriani W. Risk-taking behavior in adolescent mice: psychobiological determinants and early epigenetic influence. Neurosci. Biobehav. Rev. 2003, 27:19-31.
28. Leussis M.P., Andersen S.L. Is adolescence a sensitive period for depression? Behavioral and neuroanatomical findings from a social stress model. Synapse 2008, 62:22-30.
29. Li X.F., Edward J., Mitchell J.C., Shao B., Bowes J.E., Coen C.W., Lightman S.L., O'Byrne K.T. Differential effects of repeated restraint stress on pulsatile lutenizing hormone secretion in female Fischer, Lewis and Wistar rats. J. Neuroendocrinol. 2004, 16:620-627.
30. Macrí S., Granstrem O., Shumilina M., Gomes Antunes, dos Santos F.J., Berry A., Saso L., Laviola G. Resilience and vulnerability are dose-dependently related to neonatal stressors in mice. Horm. Behav. 2009, 56:391-398.
31. Macrí S., Zoratto F., Laviola G. Early-stress regulates resilience, vulnerability and experimental validity in laboratory rodents through mother-offspring hormonal transfer. Neurosci. Biobehav. Rev. 2011, 35:1534-1543.
32. Mastorakos G., Pavlatou M.G., Mizamtsidi M. The hypothalamic-pituitary-adrenal and the hypothalamic-pituitary-gonadal axes interplay. Pediatr. Endocrinol. Rev. 2006, 3(Suppl 1):172-181.
33. Mathews I.Z., Wilton A., Styles A., McCormick C.M. Increased depressive behaviour in females and heightened corticosterone release in males to swim stress after adolescent social stress in rats. Behav. Brain Res. 2008, 190:33-40.
34. McCormick C.M., Mathews I.Z. HPA function in adolescence: role of sex hormones in its regulation and the enduring consequences of exposure to stressors. Pharmacol. Biochem. Behav. 2007, 86:220-233.
35. McCormick C.M., Robarts D., Kopeikina K., Kelsey J.E. Long-lasting, sex- and age-specific effects of social stressors on corticosterone responses to restraint and on locomotor responses to psychostimulants in rats. Horm. Behav. 2005, 48:64-74.
36. McCormick C.M., Smith C., Mathews I.Z. Effects of chronic social stress in adolescence on anxiety and neuroendocrine response to mild stress in male and female rats. Behav. Brain Res. 2008, 187:228-238.
37. Nakayasu T., Ishii K. Effects of pair-housing after social defeat experience on elevated plus-maze behavior in rats. Behav. Processes 2008, 78:477-480.
38. Oldehinkel A.J., Bouma E.M.C. Sensitivity to the depressogenic effect of stress and HPA-axis reactivity in adolescence: a review of gender differences. Neurosci. Biobehav. Rev. 2010, 10.1016/j.neubiorev.2010.10.013.
39. Pellow S., Chopin P., File S., Briley M. Validation of open: closed arm entries in an elevated plus-maze as a measure of anxiety in the rat. J. Neurosci. Methods 1985, 14:149-167.
40. Pignatelli D., Xiao F., Gouveia A.M., Ferreira J.G., Vinson G.P. Adrenarche in the rat. J. Endocrinol. 2006, 191:301-308.
41. Porsolt R.D., Le Pichon M., Jalfre M. Depression: a new animal model sensitive to antidepressant treatments. Nature 1977, 266:730-732.
42. Rivest S., Plotsky P.M., Rivier C. CRF alters the infundibular LHRH secretory system from the medial preoptic area of female rats: possible involvement of opioid receptors. Neuroendocrinology 1993, 57:236-246.
43. Rodgers R.J., Haller J., Holmes A., Halasz J., Walton T.J., Brain P.F. Corticosterone response to the plus-maze: high correlation with risk assessment in rats and mice. Physiol. Behav. 1999, 68:47-53.
44. Romeo R.D., McEwen B.S. Stress and the adolescent brain. Ann. N. Y. Acad. Sci. 2006, 1094:202-214.
45. Ruis M.A., te Brake J.H., Buwalda B., De Boer S.F., Meerlo P., Korte S.M., Blokhuis H.J., Koolhaas J.M. Housing familiar male wildtype rats together reduces the long-term adverse behavioural and physiological effects of social defeat. Psychoneuroendocrinology 1999, 24:285-300.
46. Rygula R., Abumaria N., Flügge G., Fuchs E., Rüther E., Havemann-Reinecke U. Anhedonia and motivational deficits in rats: impact of chronic social stress. Behav. Brain Res. 2005, 162:127-134.
47. Sapolsky R.M., Meaney M.J. Maturation of the adrenocortical stress response: neuroendocrine control mechanisms and the stress hyporesponsive period. Brain Res. 1986, 396:64-76.
48. Scholtens J., Roozen M., Mirmiran M., van de Poll N.E. Role of noradrenaline in behavioral changes after defeat in male and female rats. Behav. Brain Res. 1990, 36:199-202.
49. Selye H. The general adaptation syndrome and the diseases of adaptation. J. Clin. Endocrinol. Metab. 1946, 6:117-230.
50. Solomon M.B., Karom M.C., Huhman K.L. Sex and estrous cycle differences in the display of conditioned defeat in Syrian hamsters. Horm. Behav. 2007, 52:211-219.
51. Sterlemann V., Rammes G., Wolf M., Liebl C., Ganea K., Müller M.B., Schmidt M.V. Chronic social stress during adolescence induces cognitive impairment in aged mice. Hippocampus 2010, 20:540-549.
52. Tamashiro K.L.K., Moran T.H. Perinatal environment and its influences on metabolic programming of offspring. Physiol. Behav. 2010, 100:560-566.
53. Terranova M.L., Cirulli F., Laviola G. Behavioral and hormonal effects of partner familiarity in periadolescent rat pairs upon novelty exposure. Psychoneuroendocrinology 1999, 24:639-656.
54. Tõnissaar M., Mällo T., Eller M., Häidkind R., Kõiv K., Harro J. Rat behavior after chronic variable stress and partial lesioning of 5-HT-ergic neurotransmission: effects of citalopram. Prog. Neuropsychopharmacol. Biol. Psychiatry 2008, 32:164-177.
55. Van den Berg C.L., Lamberts R.R., Wolterink G., Wiegant V.M., Van Ree J.M. Emotional and footshock stimuli induce differential long-lasting behavioural effects in rats; involvement of opioids. Brain Res. 1998, 799:6-15.
56. Vidal J., de Bie J., Granneman R.A., Wallinga A.E., Koolhaas J.M., Buwalda B. Social stress during adolescence in Wistar rats induces social anxiety in adulthood without affecting brain monoaminergic content and activity. Physiol. Behav. 2007, 92:824-830.
57. Weintraub A., Singaravelu J., Bhatnagar S. Enduring and sex-specific effects of adolescent social isolation in rats on adult stress reactivity. Brain Res. 2010, 1343:83-92.
58. Young E.A. Sex differences and the HPA axis: implications for psychiatric disease. J. Gend. Specif. Med. 1998, 1:21-27.