Direct and dam-mediated effects of prenatal dexamethasone on emotionality, cognition and HPA axis in adult Wistar rats

Hormones and Behavior

Volumn 56, Issue 4, 2009, Pages 364-375

  Hauser, Jonas ^a   Feldon, Joram ^a   Pryce, Christopher R ^a  

^a ETH ZURICH   (Switzerland)

Author keywords

Endocrinology; HPA axis; Learning; Memory; Prenatal programming

Indexed keywords

CORTICOSTERONE; CORTICOTROPIN; DEXAMETHASONE;

ANHEDONIA; ANIMAL EXPERIMENT; ARTICLE; AVOIDANCE BEHAVIOR; CHILD REARING; COGNITION; CONTROLLED STUDY; DEPRESSION; EMOTIONALITY; FEMALE; FORCED SWIMMING TEST; HELPLESSNESS; HOPELESSNESS; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; MALE; MAZE TEST; NONHUMAN; PARENTAL BEHAVIOR; PHYSICAL STRESS; PRENATAL EXPOSURE; PRIORITY JOURNAL; PROGENY; RAT; REINFORCEMENT; SEX DIFFERENCE; SPATIAL MEMORY; WISTAR RAT; WORKING MEMORY;

ANIMALS; BRAIN; COGNITION; DEPRESSION; DEXAMETHASONE; EMOTIONS; FEMALE; GLUCOCORTICOIDS; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; LEARNING; MALE; MEMORY; MOTHERS; NEUROPSYCHOLOGICAL TESTS; PITUITARY-ADRENAL SYSTEM; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RANDOM ALLOCATION; RATS; RATS, WISTAR; SEX CHARACTERISTICS;

EID: 70349737605     PISSN: 0018506X     EISSN: 10956867     Source Type: Journal    
DOI: 10.1016/j.yhbeh.2009.07.003     Document Type: Article

References (55)

1. Aisa B., Tordera R., Lasheras B., Del Rio J., and Ramirez M.J. Cognitive impairment associated to HPA axis hyperactivity after maternal separation in rats. Psychoneuroendocrinology 32 3 (2007) 256-266
2. Akirav I., Kozenicky M., Tal D., Sandi C., Venero C., and Richter-Levin G. A facilitative role for corticosterone in the acquisition of a spatial task under moderate stress. Learn. Mem. 11 2 (2004) 188-195
3. Alonso S.J., Castellano M.A., Afonso D., and Rodriguez M. Sex differences in behavioral despair: relationships between behavioral despair and open field activity. Physiol. Behav. 49 1 (1991) 69-72
4. Barker D.J. The developmental origins of well-being. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 359 1449 (2004) 1359-1366
5. Belda X., Marquez C., and Armario A. Long-term effects of a single exposure to stress in adult rats on behavior and hypothalamic-pituitary-adrenal responsiveness: comparison of two outbred rat strains. Behav. Brain Res. 154 2 (2004) 399-408
6. Benediktsson R., Calder A.A., Edwards C.R., and Seckl J.R. Placental 11 beta-hydroxysteroid dehydrogenase: a key regulator of fetal glucocorticoid exposure. Clin. Endocrinol. (Oxf). 46 2 (1997) 161-166
7. Bertoglio L.J., and Carobrez A.P. Behavioral profile of rats submitted to session 1-session 2 in the elevated plus-maze during diurnal/nocturnal phases and under different illumination conditions. Behav. Brain Res. 132 2 (2002) 135-143
8. Blokland A., Rutten K., and Prickaerts J. Analysis of spatial orientation strategies of male and female Wistar rats in a Morris water escape task. Behav. Brain Res. 171 2 (2006) 216-224
9. Bowman R.E., MacLusky N.J., Sarmiento Y., Frankfurt M., Gordon M., and Luine V.N. Sexually dimorphic effects of prenatal stress on cognition, hormonal responses, and central neurotransmitters. Endocrinology 145 8 (2004) 3778-3787
10. Brabham T., Phelka A., Zimmer C., Nash A., Lopez J.F., and Vazquez D.M. Effects of prenatal dexamethasone on spatial learning and response to stress is influenced by maternal factors. Am. J. Physiol. Regul. Integr. Comp. Physiol. 279 5 (2000) 899-909
11. Dalla C., Edgecomb C., Whetstone A.S., and Shors T.J. Females do not express learned helplessness like males do. Neuropsychopharmacology 33 7 (2008) 1559-1569
12. De Kloet E.R., Vreugdenhil E., Oitzl M.S., and Joels M. Brain corticosteroid receptor balance in health and disease. Endocr. Rev. 19 3 (1998) 269-301
13. Diamond D.M., Bennett M.C., Fleshner M., and Rose G.M. Inverted-U relationship between the level of peripheral corticosterone and the magnitude of hippocampal primed burst potentiation. Hippocampus 2 4 (1992) 421-430
14. Emgard M., Paradisi M., Pirondi S., Fernandez M., Giardino L., and Calza L. Prenatal glucocorticoid exposure affects learning and vulnerability of cholinergic neurons. Neurobiol. Aging 28 1 (2007) 112-121
15. Erisman S., Carnes M., Takahashi L.K., and Lent S.J. The effects of stress on plasma ACTH and corticosterone in young and aging pregnant rats and their fetuses. Life. Sci. 47 17 (1990) 1527-1533
16. Estanislau C., and Morato S. Behavior ontogeny in the elevated plus-maze: prenatal stress effects. Int. J. Dev. Neurosci. 24 4 (2006) 255-262
17. Gallagher M., and Pelleymounter M.A. Spatial learning deficits in old rats: a model for memory decline in the aged. Neurobiol. Aging 9 5-6 (1988) 549-556
18. Ganong F.W. Review of Medical Physiology (1999), Appleton and Lange, Stanford
19. Garcia A.M., Cardenas F.P., and Morato S. Effect of different illumination levels on rat behavior in the elevated plus-maze. Physiol. Behav. 85 3 (2005) 265-270
20. Hauser J., Feldon J., and Pryce C.R. Prenatal dexamethasone exposure, postnatal development, and adulthood prepulse inhibition and latent inhibition in Wistar rats. Behav. Brain Res. 175 1 (2006) 51-61
21. Hauser J., Knapman A., Zurcher N.R., Pilloud S., Maier C., Diaz-Heijtz R., Forssberg H., Dettling A., Feldon J., and Pryce C.R. Effects of prenatal dexamethasone treatment on physical growth, pituitary-adrenal hormones, and performance of motor, motivational, and cognitive tasks in juvenile and adolescent common marmoset monkeys. Endocrinology 149 12 (2008) 6343-6355
22. Holmes P.V. Rodent models of depression: reexamining validity without anthropomorphic inference. Crit. Rev. Neurobiol. 15 2 (2003) 143-174
23. Johnston A.L., and File S.E. Sex differences in animal tests of anxiety. Physiol. Behav. 49 2 (1991) 245-250
24. Jonasson Z. Meta-analysis of sex differences in rodent models of learning and memory: a review of behavioral and biological data. Neurosci. Biobehav. Rev. 28 8 (2005) 811-825
25. Kreider M.L., Levin E.D., Seidler F.J., and Slotkin T.A. Gestational dexamethasone treatment elicits sex-dependent alterations in locomotor activity, reward-based memory and hippocampal cholinergic function in adolescent and adult rats. Neuropsychopharmacology 9 30 (2005) 1617-1623
26. Lehmann J., and Feldon J. Long-term biobehavioral effects of maternal separation in the rat: consistent or confusing?. Rev. Neurosci. 11 4 (2000) 383-408
27. Lehmann J., Pryce C.R., Bettschen D., and Feldon J. The maternal separation paradigm and adult emotionality and cognition in male and female Wistar rats. Pharmacol. Biochem. Behav. 64 4 (1999) 705-715
28. Leng A., Jongen-Relo A.L., Pothuizen H.H., and Feldon J. Effects of prenatal methylazoxymethanol acetate (MAM) treatment in rats on water maze performance. Behav. Brain. Res. 161 2 (2005) 291-298
29. Levitt N.S., Lindsay R.S., Holmes M.C., and Seckl J.R. Dexamethasone in the last week of pregnancy attenuates hippocampal glucocorticoid receptor gene expression and elevates blood pressure in the adult offspring in the rat. Neuroendocrinology 64 6 (1996) 412-418
30. Liggins G.C., and Howie R.N. A controlled trial of antepartum glucocorticoid treatment for prevention of the respiratory distress syndrome in premature infants. Pediatrics 50 4 (1972) 515-525
31. Liu L., Li A., and Matthews S.G. Maternal glucocorticoid treatment programs HPA regulation in adult offspring: sex-specific effects. Am. J. Physiol. Endocrinol. Metab. 280 5 (2001) E729-E739
32. Lordache C., Drozdowski L., Clandinin T., Wild G., Todd Z., and Thomson A.B. Dexamethasone plus glucagon-like peptide 2 given to lactating rat dams has a late effect on intestinal lipid uptake in the weanling offspring. JPEN. J. Parenter. Enteral. Nutr. 28 5 (2004) 355-363
33. McCormick C.M., Smythe J.W., Sharma S., and Meaney M.J. Sex-specific effects of prenatal stress on hypothalamic-pituitary-adrenal responses to stress and brain glucocorticoid receptor density in adult rats. Brain Res. Dev. Brain Res. 84 1 (1995) 55-61
34. Muneoka K., Mikuni M., Ogawa T., Kitera K., Kamei K., Takigawa M., and Takahashi K. Prenatal dexamethasone exposure alters brain monoamine metabolism and adrenocortical response in rat offspring. Am. J. Physiol. 273 5 Pt. 2 (1997) 669-675
35. Nathanielsz P.W., and Padmanabhan V. Developmental origin of health and disease. J. Physiol. 572 Pt. 1 (2006) 3-4
36. National Institutes of Health Consensus Development Panel. Consensus development panel on the effect of corticosteroids for fetal maturation on perinatal outcomes: effect of corticosteroids for fetal maturation on perinatal outcomes. JAMA 273 5 (1995) 413-418
37. National Institutes of Health Consensus Development Panel. Consensus development conference statement: antenatal corticosteroids revisited: repeat courses. Obstet. Gynecol. 98 1 (2001) 144-150
38. Oliveira M., Bessa J.M., Mesquita A., Tavares H., Carvalho A., Silva R., Pego J.M., Cerqueira J.J., Palha J.A., Almeida O.F., and Sousa N. Induction of a hyperanxious state by antenatal dexamethasone: a case for less detrimental natural corticosteroids. Biol. Psychiatry 59 9 (2006) 844-852
39. Patin V., Lordi B., Vincent A., and Caston J. Effects of prenatal stress on anxiety and social interactions in adult rats. Brain Res. Dev. Brain Res. 160 2 (2005) 265-274
40. Porsolt R.D., Le Pichon M., and Jalfre M. Depression: a new animal model sensitive to antidepressant treatments. Nature 266 5604 (1977) 730-732
41. Porsolt R.D., Bertin A., and Jalfre M. "Behavioural despair" in rats and mice: strain differences and the effects of imipramine. Eur. J. Pharmacol. 51 3 (1978) 291-294
42. Pryce C.R., Palme R., and Feldon J. Development of pituitary-adrenal endocrine function in the marmoset monkey: infant hypercortisolism is the norm. J. Clin. Endocrinol. Metab. 87 2 (2002) 691-699
43. Pryce C.R., Bettschen D., Nanz-Bahr N.I., and Feldon J. Comparison of the effects of early handling and early deprivation on conditioned stimulus, context, and spatial learning and memory in adult rats. Behav. Neurosci. 117 5 (2003) 883-893
44. Pryce C.R., Ruedi-Bettschen D., Dettling A.C., Weston A., Russig H., Ferger B., and Feldon J. Long-term effects of early-life environmental manipulations in rodents and primates: potential animal models in depression research. Neurosci. Biobehav. Rev. 29 4-5 (2005) 649-674
45. Rayburn W.F., Christensen H.D., and Gonzalez C.L. A placebo-controlled comparison between betamethasone and dexamethasone for fetal maturation: differences in neurobehavioral development of mice offspring. Am. J. Obstet. Gynecol. 176 4 (1997) 842-850 discussion 850-1
46. Sanfacon R., Possmayer F., and Harding P.G. Dexamethasone treatment of the guinea pig fetus: its effects on the incorporation of 3H-thymidine into deoxyribonucleic acid. Am. J. Obstet. Gynecol. 127 7 (1977) 745-752
47. Seckl J.R. Prenatal glucocorticoids and long-term programming. Eur. J. Endocrinol. 151 Suppl. 3 (2004) 49-62
48. Smith J.W., Seckl J.R., Evans A.T., Costall B., and Smythe J.W. Gestational stress induces post-partum depression-like behaviour and alters maternal care in rats. Psychoneuroendocrinology 29 2 (2004) 227-244
49. Steenbergen H.L., Heinsbroek R.P., Van Haaren F., and Van de Poll N.E. Sex-dependent effects of inescapable shock administration on behavior and subsequent escape performance in rats. Physiol. Behav. 45 4 (1989) 781-787
50. van Hest A., van Haaren F., and van de Poll N.E. The behavior of male and female Wistar rats pressing a lever for food is not affected by sex differences in food motivation. Behav. Brain Res. 27 3 (1988) 215-221
51. Weinstock M. Behavioral and neurohormonal sequelae of prenatal stress: a suggested model of depression. Contemporary Issues in Modeling Psychopathology (2000), Kluwer Academic Publishers, Boston 45-54
52. Weinstock M. The potential influence of maternal stress hormones on development and mental health of the offspring. Brain Behav. Immun. 19 4 (2005) 296-308
53. Weinstock M., Matlina E., Maor G.I., Rosen H., and McEwen B.S. Prenatal stress selectively alters the reactivity of the hypothalamic-pituitary adrenal system in the female rat. Brain Res. 595 2 (1992) 195-200
54. Welberg L.A., Seckl J.R., and Holmes M.C. Prenatal glucocorticoid programming of brain corticosteroid receptors and corticotrophin-releasing hormone: possible implications for behaviour. Neuroscience 104 1 (2001) 71-79
55. Zagron G., and Weinstock M. Maternal adrenal hormone secretion mediates behavioural alterations induced by prenatal stress in male and female rats. Behav. Brain Res. 175 2 (2006) 323-328