Enhanced stress responses in adolescent versus adult rats exposed to cues of predation threat, and peer interaction as a predictor of adult defensiveness

Developmental Psychobiology

Volumn 54, Issue 1, 2012, Pages 47-69

  Wright, Lisa D ^a   Muir, Katherine E ^a   Perrot, Tara S ^a  

^a DALHOUSIE UNIVERSITY   (Canada)

Author keywords

Adolescent development; Corticosterone; Defensive behavior; Hypothalamic pituitary adrenal axis; Open field testing; Predator odor; Prefrontal cortex; Rat; Sex differences; Stress responding

Indexed keywords

CORTICOSTERONE;

AGE; ANIMAL; ANIMAL BEHAVIOR; ARTICLE; BLOOD; EXERCISE; FEAR; FEMALE; HYPOPHYSIS ADRENAL SYSTEM; HYPOTHALAMUS HYPOPHYSIS SYSTEM; LEARNING; LONG EVANS RAT; MALE; MENTAL STRESS; PATHOPHYSIOLOGY; PHYSIOLOGICAL STRESS; PHYSIOLOGY; PREDATION; RAT; SOCIAL BEHAVIOR;

AGE FACTORS; ANIMALS; BEHAVIOR, ANIMAL; CORTICOSTERONE; CRITICAL PERIOD (PSYCHOLOGY); FEAR; FEMALE; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; MALE; PITUITARY-ADRENAL SYSTEM; PREDATORY BEHAVIOR; RATS; RATS, LONG-EVANS; RESTRAINT, PHYSICAL; SOCIAL BEHAVIOR; STRESS, PHYSIOLOGICAL; STRESS, PSYCHOLOGICAL;

ANIMALIA; MAMMALIA; RATTUS;

EID: 83955165952     PISSN: 00121630     EISSN: 10982302     Source Type: Journal    
DOI: 10.1002/dev.20575     Document Type: Article

References (74)

1. Adriani, W., & Laviola, G. (2004). Windows of vulnerability to psychopathology and therapeutic strategy in the adolescent rodent model. Behavioural Pharmacology, 15(5-6), 341-352.
2. Andersen, S. L., & Teicher, M. H. (2000). Sex differences in dopamine receptors and their relevance to ADHD. Neuroscience and Biobehavioral Reviews, 24(1), 137-141.
3. Andersen, S. L., Thompson, A. P., Krenzel, E., & Teicher, M. H. (2002). Pubertal changes in gonadal hormones do not underlie adolescent dopamine receptor overproduction. Psychoneuroendocrinology, 27(6), 683-691.
4. Andersen, S. L., Thompson, A. T., Rutstein, M., Hostetter, J. C., & Teicher, M. H. (2000). Dopamine receptor pruning in prefrontal cortex during the periadolescent period in rats. Synapse, 37(2), 167-169.
5. Apfelbach, R., Blanchard, C. D., Blanchard, R. J., Hayes, R. A., & McGregor, I. S. (2005). The effects of predator odors in mammalian prey species: A review of field and laboratory studies. Neuroscience and Biobehavioral Reviews, 29(8), 1123-1144.
6. Atkinson, H. C., & Waddell, B. J. (1997). Circadian variation in basal plasma corticosterone and adrenocorticotropin in the rat: Sexual dimorphism and changes across the estrous cycle. Endocrinology, 138(9), 3842-3848.
7. Bland, S. T., Schmid, M. J., Der-Avakian, A., Watkins, L. R., Spencer, R. L., & Maier, S. F. (2005). Expression of c-fos and BDNF mRNA in subregions of the prefrontal cortex of male and female rats after acute uncontrollable stress. Brain Research, 1051(1-2), 90-99.
8. Bowen, S. E., Charlesworth, J. D., Tokarz, M. E., Wright, M. J., Jr., & Wiley, J. L. (2007). Decreased sensitivity in adolescent vs. adult rats to the locomotor activating effects of toluene. Neurotoxicology and Teratology, 29(6), 599-606.
9. Bowman, R. E., Beck, K. D., & Luine, V. N. (2003). Chronic stress effects on memory: Sex differences in performance and monoaminergic activity. Hormones and Behavior, 43(1), 48-59.
10. Caldwell, M. S., Rudolph, K. D., Troop-Gordon, W., & Kim, D. Y. (2004). Reciprocal influences among relational self-views, social disengagement, and peer stress during early adolescence. Child Development, 75(4), 1140-1154.
11. Cerqueira, J. J., Almeida, O. F., & Sousa, N. (2008). The stressed prefrontal cortex. Left? Right! Brain, Behavior, and Immunity. 22(5), 630-638.
12. Charmandari, E., Tsigos, C., & Chrousos, G. (2005). Endocrinology of the stress response. Annual Review of Physiology, 67, 259-284.
13. Coplan, J. D., Andrews, M. W., Rosenblum, L. A., Owens, M. J., Friedman, S., Gorman, J. M., & Nemeroff, C. B. (1996). Persistent elevations of cerebrospinal fluid concentrations of corticotropin-releasing factor in adult nonhuman primates exposed to early-life stressors: Implications for the pathophysiology of mood and anxiety disorders. Proceedings of the National Academy of Sciences of the United States of America, 93(4), 1619-1623.
14. Critchlow, V., Liebelt, R. A., Bar-Sela, M., Mountcastle, W., & Lipscomb, H. S. (1963). Sex difference in resting pituitary-adrenal function in the rat. American Journal of Physiology, 205(5), 807-815.
15. De Bellis, M. D., & Thomas, L. A. (2003). Biologic findings of post-traumatic stress disorder and child maltreatment. Current Psychiatry Reports, 5(2), 108-117.
16. Doremus-Fitzwater, T. L., Varlinskaya, E. I., & Spear, L. P. (2009). Social and non-social anxiety in adolescent and adult rats after repeated restraint. Physiology and Behavior, 97(3-4), 484-494.
17. Douglas, L. A., Varlinskaya, E. I., & Spear, L. P. (2003). Novel-object place conditioning in adolescent and adult male and female rats: Effects of social isolation. Physiology and Behavior, 80(2-3), 317-325.
18. Douglas, L. A., Varlinskaya, E. I., & Spear, L. P. (2004). Rewarding properties of social interactions in adolescent and adult male and female rats: Impact of social versus isolate housing of subjects and partners. Developmental Psychobiology, 45(3), 153-162.
19. Einon, D. F., & Morgan, M. J. (1977). A critical period for social isolation in the rat. Developmental Psychobiology, 10(2), 123-132.
20. Ferdman, N., Murmu, R. P., Bock, J., Braun, K., & Leshem, M. (2007). Weaning age, social isolation, and gender, interact to determine adult explorative and social behavior, and dendritic and spine morphology in prefrontal cortex of rats. Behavioural Brain Research, 180(2), 174-182.
21. Ferris, C. F., Messenger, T., & Sullivan, R. (2005). Behavioral and neuroendocrine consequences of social subjugation across adolescence and adulthood. Frontiers in Zoology, 2(1), 7.
22. Floresco, S. B., & Magyar, O. (2006). Mesocortical dopamine modulation of executive functions: Beyond working memory. Psychopharmacology (Berl), 188(4), 567-585.
23. Francis, D. D., Champagne, F. A., Liu, D., & Meaney, M. J. (1999). Maternal care, gene expression, and the development of individual differences in stress reactivity. Annals of the New York Academy of Sciences, 896, 66-84.
24. Frisone, D. F., Frye, C. A., & Zimmerberg, B. (2002). Social isolation stress during the third week of life has age-dependent effects on spatial learning in rats. Behavioural Brain Research, 128(2), 153-160.
25. Giedd, J. N. (2004). Structural magnetic resonance imaging of the adolescent brain. Annals of the New York Academy of Sciences, 1021, 77-85.
26. Hall, F. S. (1998). Social deprivation of neonatal, adolescent, and adult rats has distinct neurochemical and behavioral consequences. Critical Reviews in Neurobiology, 12(1-2), 129-162.
27. Herman, J. P., Ostrander, M. M., Mueller, N. K., & Figueiredo, H. (2005). Limbic system mechanisms of stress regulation: Hypothalamo-pituitary-adrenocortical axis. Progress in Neuro-Psychopharmacology & Biological Psychiatry, 29(8), 1201-1213.
28. Hodes, G. E., & Shors, T. J. (2005). Distinctive stress effects on learning during puberty. Hormones and Behavior, 48(2), 163-171.
29. Hubbard, D. T., Blanchard, D. C., Yang, M., Markham, C. M., Gervacio, A., Chun, I. L., & Blanchard, R. J. (2004). Development of defensive behavior and conditioning to cat odor in the rat. Physiology and Behavior, 80(4), 525-530.
30. Karelina, K., Walton, J. C., Weil, Z. M., Norman, G. J., Nelson, R. J., & Devries, A. C. (2010). Estrous phase alters social behavior in a polygynous but not a monogamous Peromyscus species. Hormones and Behavior, 58(2), 193-199.
31. Klein, Z. A. Padow, V. A., & Romeo R. D. (2010). The effects of stress on play and home cage behaviors in adolescent male rats. Developmental Psychobiology, 52(1), 62-70.
32. Leussis, M. P., Lawson, K., Stone, K., & Andersen, S. L. (2008). The enduring effects of an adolescent social stressor on synaptic density, part II: Poststress reversal of synaptic loss in the cortex by adinazolam and MK-801. Synapse, 62(3), 185-192.
33. Liu, D., Diorio, J., Tannenbaum, B., Caldji, C., Francis, D., Freedman, A., Meaney, M. J. (1997). Maternal care, hippocampal glucocorticoid receptors, and hypothalamic-pituitary-adrenal responses to stress. Science, 277(5332), 1659-1662.
34. Maldonado, A. M., & Kirstein, C. L. (2005a). Cocaine-induced locomotor activity is increased by prior handling in adolescent but not adult female rats. Physiology and Behavior, 86(4), 568-572.
35. Maldonado, A. M., & Kirstein, C. L., (2005b). Handling alters cocaine-induced activity in adolescent but not adult male rats. Physiology and Behavior, 84(2), 321-326.
36. Marquardt, A. R., Ortiz-Lemos, L., Lucion, A. B., & Barros, H. M. (2004). Influence of handling or aversive stimulation during rats' neonatal or adolescence periods on oral cocaine self-administration and cocaine withdrawal. Behavioural Pharmacology, 15(5-6), 403-412.
37. Mashoodh, R., Wright, L. D., Hebert, K., & Perrot-Sinal, T. S. (2008). Investigation of sex differences in behavioural, endocrine, and neural measures following repeated psychological stressor exposure. Behavioural Brain Research, 188(2), 368-379.
38. Masini, C. V., Sauer, S., & Campeau, S. (2005). Ferret odor as a processive stress model in rats: Neurochemical, behavioral, and endocrine evidence. Behavioral Neuroscience, 119(1), 280-292.
39. Matsumoto, M., Togashi, H., Kaku, A., Kanno, M., Tahara, K., & Yoshioka, M. (2005). Cortical GABAergic regulation of dopaminergic responses to psychological stress in the rat dorsolateral striatum. Synapse, 56(2), 117-121.
40. McCormick, C. M., & Mathews, I. Z. (2007). HPA function in adolescence: Role of sex hormones in its regulation and the enduring consequences of exposure to stressors. Pharmacology, Biochemistry, and Behavior, 86(2), 220-233.
41. McCormick, C. M., Robarts, D., Kopeikina, K., & Kelsey, J. E. (2005). Long-lasting, sex- and age-specific effects of social stressors on corticosterone responses to restraint and on locomotor responses to psychostimulants in rats. Hormones and Behavior, 48(1), 64-74.
42. McEwen, B., & Lasley, E. N. (2003). Allostatic load: When protection gives way to damage. Advances in Mind-Body Medicine, 19(1), 28-33.
43. McEwen, B. S. (2004). Protection and damage from acute and chronic stress: Allostasis and allostatic overload and relevance to the pathophysiology of psychiatric disorders. Annals of the New York Academy of Sciences, 1032, 1-7.
44. McEwen, B. S., & Stellar, E. (1993). Stress and the individual. Mechanisms leading to disease. Archives of Internal Medicine, 153(18), 2093-2101.
45. McGregor, I. S., Schrama, L., Ambermoon, P., & Dielenberg, R. A. (2002). Not all 'predator odours' are equal: Cat odour but not 2, 4, 5 trimethylthiazoline (TMT; fox odour) elicits specific defensive behaviours in rats. Behavioural Brain Research, 129(1-2), 1-16.
46. Meaney, M. J., Sapolsky, R. M., & McEwen, B. S. (1985). The development of the glucocorticoid receptor system in the rat limbic brain. I. Ontogeny and autoregulation. Brain Research, 350(1-2), 159-164.
47. Meaney, M. J., & Szyf, M. (2005). Environmental programming of stress responses through DNA methylation: Life at the interface between a dynamic environment and a fixed genome. Dialogues in Clinical Neuroscience, 7(2), 103-123.
48. Morrow, B. A., Elsworth, J. D., & Roth, R. H. (2002). Fear-like biochemical and behavioral responses in rats to the predator odor, TMT, are dependent on the exposure environment. Synapse, 46(1), 11-18.
49. Nappi, R. E., Bonneau, M. J., & Rivest, S. (1997). Influence of the estrous cycle on c-fos and CRH gene transcription in the brain of endotoxin-challenged female rats. Neuroendocrinology, 65(1), 29-46.
50. Nemeroff, C. B., & Vale, W. W. (2005). The neurobiology of depression: Inroads to treatment and new drug discovery. Journal of Clinical Psychiatry 66 (Suppl 7), 5-13.
51. Palanza, P., Gioiosa, L., & Parmigiani, S. (2001). Social stress in mice: Gender differences and effects of estrous cycle and social dominance. Physiology and Behavior, 73(3), 411-420.
52. Pellis, S. M., Pellis, V. C., & Whishaw, I. Q. (1992). The role of the cortex in play fighting by rats: Developmental and evolutionary implications. Brain, Behavior and Evolution, 39(5), 270-284.
53. Raap, D. K., Morin, B., Medici, C. N., & Smith, R. F. (2000). Adolescent cocaine and injection stress effects on the estrous cycle. Physiology and Behavior, 70(5), 417-424.
54. Rees, S. L., Steiner, M., & 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. Behavioural Brain Research, 175(2), 383-391.
55. Romeo, R. D. (2010a). Adolescence: A central event in shaping stress reactivity. Developmental Psychobiology, 52(3), 244-253.
56. Romeo, R. D. (2010b). Pubertal maturation and programming of hypothalamic-pituitary-adrenal reactivity. Frontiers in Neuroendocrinology, 31(2), 232-240.
57. Romeo, R. D., Bellani, R., Karatsoreos, I. N., Chhua, N., Vernov, M., Conrad, C. D., & McEwen, B. S. (2006). Stress history and pubertal development interact to shape hypothalamic-pituitary-adrenal axis plasticity. Endocrinology, 147(4), 1664-1674.
58. Romeo, R. D., Karatsoreos, I. N., & McEwen, B. S. (2006). Pubertal maturation and time of day differentially affect behavioral and neuroendocrine responses following an acute stressor. Hormones and Behavior, 50(3), 463-468.
59. Romeo, R. D., Lee, S. J., Chhua, N., McPherson, C. R., & McEwen, B. S. (2004). Testosterone cannot activate an adult-like stress response in prepubertal male rats. Neuroendocrinology, 79(3), 125-132.
60. Sapolsky, R. M. (2000). Stress hormones: Good and bad. Neurobiology of Disease, 7(5), 540-542.
61. Sapolsky, R. M., Meaney, M. J., & McEwen, B. S. (1985). The development of the glucocorticoid receptor system in the rat limbic brain. III. Negative-feedback regulation. Brain Research, 350(1-2), 169-173.
62. Simon, P., Dupuis, R., & Costentin, J. (1994). Thigmotaxis as an index of anxiety in mice. Influence of dopaminergic transmissions. Behavioural Brain Research, 61(1), 59-64.
63. Siviy, S. M., Harrison, K. A., & McGregor, I. S. (2006). Fear, risk assessment, and playfulness in the juvenile rat. Behavioral Neuroscience, 120(1), 49-59.
64. Spear, L. P. (2000). The adolescent brain and age-related behavioral manifestations. Neuroscience and Biobehavioral Reviews, 24(4), 417-463.
65. Spear, L. P. (2004). Adolescent brain development and animal models. Annals of the New York Academy of Sciences, 1021, 23-26.
66. Spencer, S. J., Buller, K. M., & Day, T. A. (2005). Medial prefrontal cortex control of the paraventricular hypothalamic nucleus response to psychological stress: Possible role of the bed nucleus of the stria terminalis. Journal of Comparative Neurology, 481(4), 363-376.
67. Sullivan, R. M. (2004). Hemispheric asymmetry in stress processing in rat prefrontal cortex and the role of mesocortical dopamine. Stress, 7(2), 131-143.
68. Sullivan, R. M., & Gratton, A. (2002). Prefrontal cortical regulation of hypothalamic-pituitary-adrenal function in the rat and implications for psychopathology: Side matters. Psychoneuroendocrinology, 27(1-2), 99-114.
69. Treit, D., & Fundytus, M. (1988). Thigmotaxis as a test for anxiolytic activity in rats. Pharmacology, Biochemistry, and Behavior, 31(4), 959-962.
70. Varlinskaya, E. I., & Spear, L. P. (2008). Social interactions in adolescent and adult Sprague-Dawley rats: Impact of social deprivation and test context familiarity. Behavioural Brain Research, 188(2), 398-405.
71. Vidal, J., Bie, J., Granneman, R. A., Wallinga, A. E., Koolhaas, J. M., & Buwalda, B. (2007). Social stress during adolescence in Wistar rats induces social anxiety in adulthood without affecting brain monoaminergic content and activity. Physiology and Behavior, 92(5), 824-830.
72. 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. Behavioral Neuroscience, 123(3), 564-576.
73. Weaver, I. C., Cervoni, N., Champagne, F. A., D'Alessio, A. C., Sharma, S., Seckl, J. R., Meaney, M. J. (2004). Epigenetic programming by maternal behavior. Nature Neuroscience, 7(8), 847-854.
74. Wright, L. D., Hebert, K. E., & Perrot-Sinal, T. S. (2008). Periadolescent stress exposure exerts long-term effects on adult stress responding and expression of prefrontal dopamine receptors in male and female rats. Psychoneuroendocrinology, 33(2), 130-142.