Adolescent social stress does not necessarily lead to a compromised adaptive capacity during adulthood: A study on the consequences of social stress in rats

Neuroscience

Volumn 249, Issue , 2013, Pages 258-270

  Buwalda, B ^a   Stubbendorff, C ^a,b   Zickert, N ^a   Koolhaas, J M ^a  

^a UNIVERSITY OF GRONINGEN   (Netherlands)

^b UNIVERSITY OF LEICESTER   (United Kingdom)

Author keywords

Adolescence; Match mismatch hypothesis; Neurogenesis; Play behavior; Social defeat; Social housing

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR;

ADAPTIVE BEHAVIOR; ADOLESCENT; AGGRESSION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANXIETY; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; COPING BEHAVIOR; HIPPOCAMPUS; MALE; NERVE CELL PLASTICITY; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PLAY; PRIORITY JOURNAL; RAT; SOCIAL INTERACTION; SOCIAL STRESS;

5-BROMODEOXIURIDINE; ADOLESCENCE; ANALYSIS OF VARIANCE; ANOVA; BDNF; BRAIN-DERIVED NEUROTROPHIC FACTOR; BRDU; CORT; CORTICOSTERONE; DCX; DOUBLECORTIN; MATCH-MISMATCH HYPOTHESIS; NEUROGENESIS; PBS; PHOSPHATE-BUFFERED SALINE; PLAY BEHAVIOR; PND; POSTNATAL DAY; SD; SEM; SOCIAL DEFEAT; SOCIAL HOUSING; STANDARD ERROR OF THE MEAN; WILDTYPE GRONINGEN RATS; WTG;

ADAPTATION, PSYCHOLOGICAL; AGE FACTORS; ANIMALS; FEMALE; INTERPERSONAL RELATIONS; MALE; RATS; RATS, SPRAGUE-DAWLEY; RATS, WISTAR; STRESS, PSYCHOLOGICAL;

EID: 84881543405     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2012.12.050     Document Type: Article

References (57)

1. 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.
2. Belsky J., Jonassaint C., Pluess M., Stanton M., Brummett B., Williams R. Vulnerability genes or plasticity genes?. Mol Psychiatry 2009, 14:746-754.
3. Bingham B., McFadden K., Zhang X., Bhatnagar S., Beck S., Valentino R. Early adolescence as a critical window during which social stress distinctly alters behavior and brain norepinephrine activity. Neuropsychopharmacology 2011, 36:896-909.
4. Bjorkqvist K. Social defeat as a stressor in humans. Physiol Behav 2001, 73:435-442.
5. Brown G.W., Prudo R. Psychiatric disorder in a rural and an urban population: 1. Aetiology of depression. Psychol Med 1981, 11:581-599.
6. Burgdorf J., Kroes R.A., Moskal J.R., Pfaus J.G., Brudzynski S.M., Panksepp J. Ultrasonic vocalizations of rats (Rattus norvegicus) during mating, play, and aggression: behavioral concomitants, relationship to reward, and self-administration of playback. J Comp Psychol 2008, 122:357-367.
7. Buwalda B., de Boer S.F., Schmidt E.D., Felszeghy K., Nyakas C., Sgoifo A., Van der Vegt B.J., Tilders F.J., Bohus B., Koolhaas J.M. Long-lasting deficient dexamethasone suppression of hypothalamic-pituitary-adrenocortical activation following peripheral CRF challenge in socially defeated rats. J Neuroendocrinol 1999, 11:513-520.
8. Buwalda B., Blom W.A., Koolhaas J.M., Van Dijk G. Behavioral and physiological responses to stress are affected by high-fat feeding in male rats. Physiol Behav 2001, 73:371-377.
9. Buwalda B., Geerdink M., Vidal J., Koolhaas J.M. Social behavior and social stress in adolescence: A focus on animal models. Neurosci Biobehav Rev 2011, 35:1713-1721.
10. Chechik G., Meilijson I., Ruppin E. Neuronal regulation: a mechanism for synaptic pruning during brain maturation. Neural Comput 1999, 11:2061-2080.
11. Cherng C.G., Lin P.S., Chuang J.Y., Chang W.T., Lee Y.S., Kao G.S., Lai Y.T., Yu L. Presence of conspecifics and their odor-impregnated objects reverse stress-decreased neurogenesis in mouse dentate gyrus. J Neurochem 2010, 112:1138-1146.
12. Cosley B.J., McCoy S.K., Saslow L.R., Epel E.S. Is compassion for others stress buffering? Consequences of compassion and social support for physiological reactivity to stress. J Exp Social Psychology 2010, 46:816-823.
13. Cutrona C.E., Russell D.W., Brown P.A., Clark L.A., Hessling R.M., Gardner K.A. Neighborhood context, personality, and stressful life events as predictors of depression among African American women. J Abnorm Psychol 2005, 114:3-15.
14. Daskalakis N.P., Oitzl M.S., Schachinger H., Champagne D.L., de Kloet E.R. Testing the cumulative stress and mismatch hypotheses of psychopathology in a rat model of early-life adversity. Physiol Behav 2012, 106:707-721.
15. de Boer S.F., Koolhaas J.M. Defensive burying in rodents: ethology, neurobiology and psychopharmacology. Eur J Pharmacol 2003, 463:145-161.
16. de Boer S.F., Van der Vegt B.J., Koolhaas J.M. Individual variation in aggression of feral rodent strains: a standard for the genetics of aggression and violence?. Behav Genet 2003, 33:485-501.
17. de Jong J.G., Van der Vegt B.J., Buwalda B., Koolhaas J.M. Social environment determines the long-term effects of social defeat. Physiol Behav 2005, 84:87-95.
18. Dunbar R.I. The social role of touch in humans and primates: behavioural function and neurobiological mechanisms. Neurosci Biobehav Rev 2010, 34:260-268.
19. Einon D.F., Morgan M.J. A critical period for social isolation in the rat. Dev Psychobiol 1977, 10:123-132.
20. Ellis B.J., Boyce W.T., Belsky J., Bakermans-Kranenburg M.J., van Ijzendoorn M.H. Differential susceptibility to the environment: an evolutionary-neurodevelopmental theory. Dev Psychopathol 2011, 23:7-28.
21. Franks P., Campbell T.L., Shields C.G. Social relationships and health: the relative roles of family functioning and social support. Soc Sci Med 1992, 34:779-788.
22. Frisen A., Jonsson A.K., Persson C. Adolescents' perception of bullying: who is the victim? Who is the bully? What can be done to stop bullying?. Adolescence 2007, 42:749-761.
23. Hemphill S.A., Kotevski A., Tollit M., Smith R., Herrenkohl T.I., Toumbourou J.W., Catalano R.F. Longitudinal predictors of cyber and traditional bullying perpetration in Australian secondary school students. J Adolesc Health 2012, 51:59-65.
24. Hennessy M.B., Kaiser S., Sachser N. Social buffering of the stress response: diversity, mechanisms, and functions. Front Neuroendocrinol 2009, 30:470-482.
25. Hol T., Van Den Berg C.L., van Ree J.M., Spruijt B.M. Isolation during the play period in infancy decreases adult social interactions in rats. Behav Brain Res 1999, 100:91-97.
26. Jacobson-Pick S., Audet M.-C., Nathoo N., Anisman H. Stressor experiences during the juvenile period increase stressor responsivity in adulthood: transmission of stressor experiences. Behav Brain Res 2011, 216:365-374.
27. Jankord R., Solomon M.B., Albertz J., Flak J.N., Zhang R., Herman J.P. Stress vulnerability during adolescent development in rats. Endocrinology 2011, 152:629-638.
28. Juvonen J., Graham S., Schuster M.A. Bullying among young adolescents: the strong, the weak, and the troubled. Pediatrics 2003, 112:1231-1237.
29. Kessler R.C., McLaughlin K.A., Green J.G., Gruber M.J., Sampson N.A., Zaslavsky A.M., Aguilar-Gaxiola S., Alhamzawi A.O., Alonso J., Angermeyer M., Benjet C., Bromet E., Chatterji S., de Girolamo G., Demyttenaere K., Fayyad J., Florescu S., Gal G., Gureje O., Haro J.M., Hu C.Y., Karam E.G., Kawakami N., Lee S., Lepine J.P., Ormel J., Posada-Villa J., Sagar R., Tsang A., Ustun T.B., Vassilev S., Viana M.C., Williams D.R. Childhood adversities and adult psychopathology in the WHO World Mental Health Surveys. Br J Psychiatry 2010, 197:378-385.
30. Kiyokawa Y., Kikusui T., Takeuchi Y., Mori Y. Partner's stress status influences social buffering effects in rats. Behav Neurosci 2004, 118:798-804.
31. Koolhaas J.M., Meerlo P., de Boer S.F., Strubbe J.H., Bohus B. The temporal dynamics of the stress response. Neurosci Biobehav Rev 1997, 21:775-782.
32. Kudryavtseva N.N., Bakshtanovskaya I.V., Koryakina L.A. Social model of depression in mice of C57BL/6J strain. Pharmacol Biochem Behav 1991, 38:315-320.
33. 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.
34. Macone B.W., O'Malley M., Datta S. Sharing stressful experiences attenuates anxiety-related cognitive and sleep impairments. Behav Brain Res 2011, 222:351-356.
35. Martinez M., Calvo-Torrent A., Pico-Alfonso M.A. Social defeat and subordination as models of social stress in laboratory rodents: A review. Aggressive Behav 1998, 24:241-256.
36. McCormick C.M. An animal model of social instability stress in adolescence and risk for drugs of abuse. Physiol Behav 2010, 99:194-203.
37. Meerlo P., de Boer S.F., Koolhaas J.M., Daan S., Van Den Hoofdakker R.H. Changes in daily rhythms of body temperature and activity after a single social defeat in rats. Physiol Behav 1996, 59:735-739.
38. Meerlo P., Sgoifo A., de Boer S.F., Koolhaas J.M. Long-lasting consequences of a social conflict in rats: behavior during the interaction predicts subsequent changes in daily rhythms of heart rate, temperature, and activity. Behav Neurosci 1999, 113:1283-1290.
39. 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.
40. Neumann I.D. The advantage of social living: brain neuropeptides mediate the beneficial consequences of sex and motherhood. Front Neuroendocrinol 2009, 30:483-496.
41. Paxinos G, Watson C (2008) The rat brain in stereotaxix coordinates. Sixth Edition.
42. Pellis S.M., Pellis V.C. Juvenilized play fighting in subordinate male rats. Aggressive Behav 1992, 18:449-457.
43. Pellis S.M., Pellis V.C. Rough-and-tumble play and the development of the social brain. Curr Dir Psychol Sci 2007, 16:95-98.
44. Post R.M. Transduction of psychosocial stress into the neurobiology of recurrent affective disorder. Am J Psychiatry 1992, 149:999-1010.
45. Ren X.S., Skinner K., Lee A., Kazis L. Social support, social selection and self-assessed health status: results from the veterans health study in the United States. Soc Sci Med 1999, 48:1721-1734.
46. Romeo R.D. Adolescence: a central event in shaping stress reactivity. Dev Psychobiol 2010, 52:244-253.
47. 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.
48. Schmidt M.V. Animal models for depression and the mismatch hypothesis of disease. Psychoneuroendocrinology 2011, 36:330-338.
49. Stranahan A.M. Putting age-associated changes in neurogenesis in their place. Neurobiol Aging 2010, 31:2179-2180.
50. Tornatzky W., Miczek K.A. Long-term impairment of autonomic circadian rhythms after brief intermittent social stress. Physiol Behav 1993, 53:983-993.
51. van den Berg C.L., Hol T., Van Ree J.M., Spruijt B.M., Everts H., Koolhaas J.M. Play is indispensable for an adequate development of coping with social challenges in the rat. Dev Psychobiol 1999, 34:129-138.
52. Vidal J., 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.
53. Watt M.J., Burke A.R., Renner K.J., Forster G.L. Adolescent male rats exposed to social defeat exhibit altered anxiety behavior and limbic monoamines as adults. Behav Neurosci 2009, 123:564-576.
54. Weidt A., Hofmann S.E., Konig B. Not only mate choice matters: fitness consequences of social partner choice in female house mice. Anim Behav 2012, 75:801-808.
55. Weihs K.L., Simmens S.J., Mizrahi J., Enright T.M., Hunt M.E., Siegel R.S. Dependable social relationships predict overall survival in stages II and III breast carcinoma patients. J Psychosom Res 2005, 59:299-306.
56. Wilson J.H. Prolactin in rats is attenuated by conspecific touch in a novel environment. Cogn Affect Behav Neurosci 2001, 1:199-205.
57. Zaias J., Queeney T.J., Kelley J.B., Zakharova E.S., Izenwasser S. Social and physical environmental enrichment differentially affect growth and activity of preadolescent and adolescent male rats. J Am Assoc Lab Anim Sci 2008, 47:30-34.