Prenatal stress effects on emotion regulation differ by genotype and sex in prepubertal rats

Developmental Psychobiology

Volumn 55, Issue 2, 2013, Pages 176-192

  Schroeder, Mariana ^a   Sultany, Tom ^a   Weller, Aron ^a  

^a BAR ILAN UNIVERSITY   (Israel)

Author keywords

Animal model of depression; Anxiety; Prenatal stress; Prepubertal rats; Sex differences

Indexed keywords

CORTICOSTERONE;

ANIMAL; ARTICLE; BLOOD; DEPRESSION; EMOTION; EXERCISE; FEMALE; GENOTYPE; MALE; MENTAL STRESS; PATHOPHYSIOLOGY; PHYSIOLOGY; PREGNANCY; PRENATAL EXPOSURE; PSYCHOLOGICAL ASPECT; RAT; SOCIAL BEHAVIOR; SPECIES DIFFERENCE; WISTAR KYOTO RAT; WISTAR RAT;

ANIMALS; CORTICOSTERONE; DEPRESSION; EMOTIONS; FEMALE; GENOTYPE; MALE; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RATS; RATS, INBRED WKY; RATS, WISTAR; RESTRAINT, PHYSICAL; SOCIAL BEHAVIOR; SPECIES SPECIFICITY; STRESS, PSYCHOLOGICAL;

ANIMALIA; RATTUS; RATTUS NORVEGICUS;

EID: 84872651377     PISSN: 00121630     EISSN: 10982302     Source Type: Journal    
DOI: 10.1002/dev.21010     Document Type: Article

References (90)

1. Adriani, W., Zoratto, F., Romano, E., & Laviola, G. (2010). Cognitive impulsivity in animal models: Role of response time and reinforcing rate in delay intolerance with two-choice operant tasks. Neuropharmacology, 58, 694-701.
2. American Psychiatric Association. (2000). Diagnostic and statistical manual of mental disorders, Fourth edition (DSM-IV). Washington, DC: American Psychiatric Association.
3. Anisman, H., & Matheson, K. (2005). Stress, depression, and anhedonia: Caveats concerning animal models. Neuroscience and Biobehavioral Reviews, 29, 525-546.
4. Anisman, H., & Zacharko, R. M. (1982). Depression-The predisposing influence of stress. Behavioral and Brain Sciences, 5, 89-122.
5. Barha, C. K., Brummelte, S., Lieblich, S. E., & Galea, L. A. (2011). Chronic restraint stress in adolescence differentially influences hypothalamic-pituitary-adrenal axis function and adult hippocampal neurogenesis in male and female rats. Hippocampus, 21, 1216-1227.
6. Barker, D. J. P. (2001). Fetal and infant origins of adult disease. Monatsschrift Kinderheilkunde, 149(13), 2-6.
7. Biala, Y. N., Bogoch, Y., Bejar, C., Linial, M., & Weinstock, M. (2010). Prenatal stress diminishes gender differences in behavior and in expression of hippocampal synaptic genes and proteins in rats. Hippocampus, 21, 1114-1125.
8. Bosch, O. J., Krömer, S. A., & Neumann, I. D. (2006). Prenatal stress: Opposite effects on anxiety an hypothalamic expression of vasopressin and corticotropin-releasing hormone in rats selectively bred for high and low anxiety. European Journal of Neuroscience, 23, 541-551.
9. Braw, Y., Malkesman, O., Bercovich, A., Dagan, M., Lavi-Avnon, Y., Schroeder, M., Weller, A. (2006). Anxiety-like behaviors in pre-pubertal rats of the Flinders Sensitive Line (FSL) and Wistar-Kyoto (WKY) animal models of depression. Behavioural Brain Research, 167, 261-269.
10. Braw, Y., Malkesman, O., Merenlender, A., Bercovich, A., Dagan, M., Overstreet, D. H., & Weller, A. (2008). Withdrawal emotional-regulation in infant rats from genetic animal models of depression. Behavioural Brain Research, 193(1), 94-100.
11. Brunton, P. J., & Russell, J. A. (2010). Prenatal social stress in the rat programmes neuroendocrine and behavioural responses to stress in the adult offspring: Sex-specific effects. J Neuroendocrinology, 22, 258-271.
12. Burke, H. M., Davis, M. C., Otte, C., & Mohr, D. C. (2005). Depression and cortisol responses to psychological stress: A meta-analysis. Psychoneuroendocrinology, 30, 846-856.
13. Calcagnetti, D. J., & Schechter, M. D. (1992). Place conditioning reveals the rewarding aspect of social interaction in juvenile rats. Physiology and Behavior, 51, 667-672.
14. Cannizzaroa, C., Plesciaa, F., Martireb, M., Gaglianoa, M., Cannizzaroa, G., Mantiaa, G., & Cannizzaro, E. (2006). Single, intense prenatal stress decreases emotionality and enhances learning performance in the adolescent rat offspring: Interaction with a brief, daily maternal separation. Behavioral Brain Research, 169, 128-136.
15. Charmandari, E., Kino, T., Souvatzoglou, E., & Chrousos, G. P. (2003). Pediatric stress: Hormonal mediators and human development. Hormone Research, 59, 161-179.
16. Clarke, A. S., & Schneider, M. L. (1993). Prenatal stress has long-term effects on behavioral responses to stress in juvenile rhesus monkeys. Developmental Psychobiology, 26, 293-304.
17. Cruz, F. C., Marin, M. T., Leão, R. M., & Planeta, C. S. (2012). Behavioral and neuroendocrine effects of the exposure to chronic restraint or variable stress in early adolescent rats. International Journal of Developmental Neuroscience, 30, 19-23.
18. Cryan, J. F., Markou, A., & Lucki, I. (2002). Assessing antidepressant activity in rodents: Recent developments and future needs. Trends in Pharmacological Sciences, 23, 238-245.
19. Darnaudéry, M., & Maccari, S. (2008). Epigenetic programming of the stress response in male and female rats by prenatal restraint stress. Brain Research Reviews, 57, 571-585.
20. Dela Peña, I., Yoon, S. Y., Lee, J. C., Dela Peña, J. B., Sohn, A. R., Ryu, J. H., Cheong, J. H. (2011). Methylphenidate treatment in the spontaneously hypertensive rat: Influence on methylphenidate self-administration, reinstatement in comparison with Wistar rats. Psychopharmacology (Berlin), PMID: 22086360.
21. 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, 484-494.
22. Foa, E. B., Zinbarg, R., & Rothbaum, B. O. (1992). Uncontrollability and unpredictability in post-traumatic stress disorder: An animal model. Psychological Bulletin, 112, 218-238.
23. Foilb, A. R., Lui, P., & Romeo, R. D. (2011). The transformation of hormonal stress responses throughout puberty and adolescence. Journal of Endocrinology, 210, 391-398.
24. Fride, E., & Weinstock, M. (1984). The effects of prenatal exposure to predictable or unpredictable stress on early development in the rat. Developmental Psychobiology, 17, 651-660.
25. García-Cáceres, C., Lagunas, N., Calmarza-Font, I., Azcoitia, I., Diz-Chaves, Y., García-Segura, L. M., Chowen, J. A. (2010). Gender differences in the long-term effects of chronic prenatal stress on the HPA axis and hypothalamic structure in rats. Psychoneuroendocrinology, 35, 1525-1535.
26. Goodwin, G. A., & Yacko, H. (1984). Emergence of the exploratory motive in rats. Developmental Psychobiology, 45, 34-48.
27. Grippo, A. J., Sullivan, N. R., Damjanoska, K. J., Crane, J. W., Carrasco, G. A., Shi, J., Van de Kar, L. D. (2004). Chronic mild stress induces behavioral and physiological changes, and may alter serotonin 1A receptor function, in male and cycling female rats. Psychopharmacology, 179, 769-780.
28. Hammen, C., & Gitlin, M. (1997). Stress reactivity in bipolar patients and its relation to prior history of disorder. American Journal of Psychiatry, 154, 856-857.
29. Hauger, R. L., Lorang, M., Irwin, M., & Aguilera, G. (1990). CRF receptor regulation and sensitization of ACTH responses to acute ether stress during chronic intermittent immobilization stress. Brain Research, 532, 34-40.
30. Jacobson, S. W., & Jacobson, J. L. (2000). Teratogenic insult and neurobehavioural function in infancy and childhood. In C. A. Nelson (Ed.), The effects of early adversity on neurobehavioral development. The Minnesota Symposia on Child Psychology, 31 (pp. 61-112). Mahwah, NJ: Erlbaum.
31. Jaio, X., Paré, W. P., & Tejani-Butt, S. (2003). Strain differences in the distribution of dopamine transporter sites in rat brain. Progress in Neuro-Psychopharmacology and Biological Psychology, 27, 913-919.
32. Jesberger, J. A., & Richardson, J. S. (1985). Animal models of depression: parallels and correlates to severe depression in humans. Biological Psychiatry, 20, 764-784.
33. Kalin, N. H., Weiler, S. J., & Shelton, S. E. (1982). Plasma ACTH and cortisol concentrations before and after dexamethasone. Psychiatry Research, 7, 87-92.
34. Kioukia-Fougia, N., Antoniou, K., Bekris, S., Liapi, C., Christofidis, I., & Papadopoulou-Daifoti, Z. (2002). The effects of stress exposure on the hypothalamicpituitary adrenal axis, thymus, thyroid hormones and glucose levels. Progress in Neuro-Psychopharmacology and Biological Psychiatry, 26, 823-830.
35. Koenig, J. I., Elmer, G. I., Shepard, P. D., Lee, P. R., Mayo, C., Joy, B., Brady, D. L. (2005). Prenatal exposure to a repeated variable stress paradigm elicits behavioral and neuroendocrinological changes in the adult offspring: potential relevance to schizophrenia. Behavioural Brain Research, 156, 251-261.
36. Lahmame, A., del Arco, C., Pazos, A., Yritia, M., & Armario, A. (1997). Are Wistar-Kyoto rats a genetic animal model of depression resistant to antidepressants? European Journal of Pharmacology, 337, 115-123.
37. Langen, B., & Dost, R. (2011). Comparison of SHR, WKY and Wistar rats in different behavioural animal models: Effect of dopamine D1 and alpha2 agonists. Attention Deficit Hyperactive Disorder, 3, 1-12.
38. Lavi-Avnon, Y., Shayit, M., Yadid, G., Overstreet, H. D., & Weller, A. (2005). Immobility in the swim test and observations of maternal behavior in lactating Flinders Sensitive Line rats. Behavioral Brain Research, 161, 155-163.
39. Laviola, G., Adriani, W., Morley-Fletcher, S., & Terranova, M. L. (2002). Peculiar response of adolescent mice to acute and chronic stress and to amphetamine: Evidence of sex differences. Behavioural Brain Research, 130, 117-125.
40. Laviola, G., Rea, M., Morley-Fletcher, S., Di Carlo, S., Bacosi, A., De Simone, R., Pacific, R. (2004). Beneficial effects of enriched environment on adolescent rats from stressed pregnancies. European Journal of Neuroscience, 20(6), 1655-1664.
41. Lupien, S. J., McEwen, B. S., Gunnar, M. R., & Heim, C. (2009). Effects of stress throughout the lifespan on the brain, behaviour and cognition. Nature Reviews Neuroscience, 10, 434-445.
42. Ma, X. M., & Lightman, S. L. (1998). The arginine vasopressin and corticotrophinreleasing hormone gene transcription responses to varied frequencies of repeated stress in rats. The Journal of Physiology, 510, 605-614.
43. Ma, X. M., Lightman, S. L., & Aguilera, G. (1999). Vasopressin and corticotropin-releasing hormone gene responses to novel stress in rats adapted to repeated restraint. Endocrinology, 140, 3623-3632.
44. Malkesman, O., Braw, Y., Zagoory-Sharon, O., Golan, O., Lavi-Avnon, Y., Schroeder, M., Weller, A. (2005). Reward and anxiety behavior in genetic animal models of childhood depression. Behavioural Brain Research, 164, 1-10.
45. Malkesman, O., & Weller, A. (2009). Two different putative genetic animal models of childhood depression-A review. Progress in Neurobiology, 88, 153-169.
46. Markham, J. A., & Koenig, J. I. (2011). Prenatal stress: role in psychotic and depressive diseases. Psychopharmacology (Berlin), 214, 89-106.
47. Mathews, I. Z., Wilton, A., Styles, A., & McCormick, C. M. (2008). Increased depressive behaviour in females and heightened corticosterone release in males to swim stress after adolescent social stress in rats. Behavioural Brain Research, 190, 33-40.
48. McCormick, C. M., Merrick, A., Secen, J., & Helmreich, D. L. (2007). Social instability in adolescence alters the central and peripheral hypothalamic-pituitary-adrenal responses to a repeated homotypic stressor in male and female rats. Journal of Neuroendocrinology, 19, 116-126.
49. Meaney, M. J., & Stewart, J. (1981). A descriptive study of social development in the rat (Rattus norvegicus). Animal Behavior, 29, 34-45.
50. Meijer, A. (1985). Child psychiatric sequelae of maternal war stress. Acta Psychiatrica Scandinavica, 72, 505-511.
51. Mueller, B. R., & Bale, T. L. (2008). Sex-specific programming of offspring emotionality after stress early in pregnancy. Journal of Neuroscience, 28, 9055-9065.
52. Newnham J. P. & Ross M. G. (Eds.). (2009). Early life origins of human health and disease. Basel: S Karger.
53. O'Connor, T. G., Heron, J., & Glover, V. (2002). Antenatal anxiety predicts child behavioral/emotional problems independently of postnatal depression. Journal of the American Academy of Child and Adolescent Psychiatry, 41(12), 1470-1477.
54. O'Donnell, K., O'Connor, T. G., & Glover, V. (2009). Prenatal stress and neurodevelopment of the child: Focus on the HPA axis and role of the placenta. Developmental Neuroscience, 31, 285-292.
55. Offord, D. R., & Cross, L. A. (1969). Behavioral antecedents of adult schizophrenia. Archives of General Psychiatry, 21, 267-283.
56. Ottoni, E. B. (2000). EthoLog 2.2: A tool for the transcription and timing of behavior observation sessions. Behavior Research Methods, Instruments, and Computers, 32, 446-449.
57. Overstreet, D. H. (1993). The flinders sensitive line rats: A genetic animal model of depression. Neuroscience and Biobehavioral Review, 17, 51-68.
58. Paré, W. P. (1989a). Stress ulcer susceptibility and depression in Wistar Kyoto (WKY) rats. Physiology and Behavior, 46, 993-998.
59. Paré, W. P. (1989b). "Behavioral despair" test predict stress ulcer in WKY rats. Physiology and Behavior, 46, 483-487.
60. Paré, W. P. (1992). The performance of WKY rats on three tests of emotional behavior. Physiology and Behavior, 51, 1051-1056.
61. Paré, W. P. (1993). Passive-avoidance behavior in Wistar-Kyoto (WKY), Wistar and Fischer-344 rats. Physiology and Behavior, 54, 845-852.
62. Paré, W. P., & Redei, E. (1993). Depressive behavior and stress ulcer in Wistar Kyoto rats. Journal of Physiology (Paris), 87, 229-238.
63. Paré, W. P. (1994). Open field, learned helplessness, conditioned defensive burying, and forced-swim tests in WKY rats. Physiology and Behavior, 55, 433-439.
64. Paré, W. P. (2000). Investigatory behavior of a novel conspecific by Wistar Kyoto, Wistar and Sprague-Dawley rats. Brain Research Bulletin, 53, 759-765.
65. Paré, W. P., Blair, G. R., Kluczynski, J., & Tejani-Butt, S. (1999). Gender differences in acute and chronic stress in Wistar Kyoto (WKY) rats. Integrative Psychological and Behavioral Science, 34(4), 227-241.
66. Peters, D. A. (1988). Effects of maternal stress during different gestational periods on the serotonergic system in adult rat offspring. Pharmacology Biochemistry and Behavior, 31, 839-843.
67. Pryce, C. R., Bettschen, D., & Feldon, J. (2001). Comparison of the effects f early handling and early deprivation on maternal care in the rat. Developmental Psychobiology, 38, 239-251.
68. Quirce, C. M., Odio, M., & Solano, J. M. (1981). The effects of predictable and unpredictable schedules of physical restraint upon rats. Life Sciences, 28, 1897-1902.
69. Redei, E., Paré, W. P., Aird, F., & Kluczynski, J. (1994). Strain differences in hypothalamic-pituitary-adrenal activity and stress ulcer. The American Journal of Physiology-Regulatory, Integrative and Comparative Physiology, 266, 353-360.
70. Salomon, S., Bejar, C., Schorer-Apelbaum, D., & Weinstock, M. (2011). Corticosterone mediates some but not other behavioural changes induced by prenatal stress in rats. Neuroendocrinology, 23, 118-128.
71. Schenberg, L. C., Bittencourt, A. S., Sudré, E. C., & Vargas, L. C. (2001). Modeling panic attacks. Neuroscience and Biobehavioral Reviews, 25, 647-659.
72. Schroeder, M., Zagoory-Sharon, O., Lavi-Avnon, Y., Moran, T. H., & Weller, A. (2006). Weight gain and maternal behavior in CCK1 deficient rats. Physiology and Behavior, 89(3), 402-409.
73. Schulz, K. M., Pearson, J. N., Neeley, E. W., Berger, R., Leonard, S., Adams, C. E., & Stevens, K. E., (2011). Maternal stress during pregnancy causes sex-specific alterations in offspring memory performance, social interactions, indices of anxiety, and body mass. Physiology and Behavior, 104, 340-347.
74. Shepard, J. D., & Myers, D. A. (2008). Strain differences in anxiety-like behavior: Association with corticotropin-releasing factor. Behavioural Brain Research, 186, 239-245.
75. Simpkiss, J. L., & Devine, D. P. (2003). Responses of the HPA axis after chronic variable stress: Effects of novel and familiar stressors. Neuroendocrinology Letters, 24, 97-103.
76. Solberg, L. C., Olson, S. L., Turek, F. W., & Redei, E. (2001). Altered hormone levels and circadian rhythm of activity in the WKY rat, a putative animal model of depression. American Journal of Physiology Regulatory Integrative Comparative Physiology, 281, 786-794.
77. Stohr, T., Wermeling, D. S., Szuran, T., Pliska, V., Domeney, A., Welzl, H., Feldon, J. (1998). Differential effects of prenatal stress in two inbred strains of rats. Pharmacology Biochemistry and Behavior, 59, 799-805.
78. Szuran, T. F., Pliska, V., Pokorny, J., & Welzl, H. (2000). Prenatal stress in rats effects on plasma corticosterone, hippocampal glucocorticoid receptors, and maze performance. Physiology and Behavior, 71, 353-362.
79. Terranova, M. L., Cirulli, F., & Laviola, G. (1999). Behavioral and hormonal effects of partner familiarity in periadolescent rat pairs upon novelty exposure. Psychoneuroendocrinology, 24, 639-656.
80. Toledo-Rodriguez, M., & Sandi, C. (2011). Stress during adolescence increases novelty seeking and risk-taking behavior in male and female rats. Frontiers in Behavioral Neuroscience, 5, 17.
81. Van den Bergh, B. R., & Marcoen, A. (2004). High antenatal maternal anxiety is related to ADHD symptoms, externalizing problems, and anxiety in 8- and 9-year-olds. Child Development, 75(4), 1085-1097.
82. Vanderschuren, L. J. M. J., Niesink, R. J. M., & Van Pee, J. M. (1997). The neurobiology of social play behavior in rats. Neuroscience and Biobehavioral Reviews, 21(3), 309-326.
83. Weinstock, M. (2007). Gender differences in the effects of prenatal stress on brain development and behaviour. Neurochemical Research, 32, 1730-1740.
84. Weinstock, M. (2010). Intrauterine factors as determinants of depressive disorder. Israel Journal of Psychiatry and Related Sciences, 47, 36-45.
85. Weinstock, M., Matlina, E., Maor, G. I., Rosen, H., & McEwen, B. S. (1992). Prenatal stress selectively alters the reactivity of the hypothalamic-pituitary adrenal system in the female rat. Brain Research, 595, 195-200.
86. Welberg, L. A. M., & Seckl, J. R. (2001). Prenatal stress, glucocorticoids and the programming of the brain. Journal of Neuroendocrinology, 13, 113-128.
87. Weller, A., Glaubman, H., Yehuda, S., Caspy, T., & Ben-Uria, Y. (1988). Acute and repeated gestational stress affect offspring learning and activity in rats. Physiology and Behavior, 43, 139-143.
88. Willner, P. (1997). Validity, reliability and utility of the chronic mild stress model of depression: A 10-year review and evaluation. Psychopharmacology, 134, 319-329.
89. Zohar, I., & Weinstock, M. (2011). Differential effect of prenatal stress on the expression of cortiocotrophin-releasing hormone and its receptors in the hypothalamus and amygdala in male and female rats. Neuroendocrinology, 23, 320-328.
90. Zuena, A. R., Mairesse, J., Casolini, P., Cinque, C., Alemà, G. S., Morley-Fletcher, S., Maccari, S. (2008). Prenatal restraint stress generates two distinct behavioral and neurochemical profiles in male and female rats. PLoS ONE, 3, e2170.