Effects of excessive glucocorticoid receptor stimulation during early gestation on psychomotor and social behavior in the rat

Developmental Psychobiology

Volumn 52, Issue 2, 2010, Pages 121-132

  Kleinhaus, Karine ^a   Steinfeld, Sara ^b   Balaban, Jordan ^b   Goodman, Leora ^b   Craft, Tara S ^b,c   Malaspina, Dolores ^a,c   Myers, Michael M ^b,c   Moore, Holly ^b,c  

^a NEW YORK UNIVERSITY MEDICAL CENTER   (United States)

^b NEW YORK STATE PSYCHIATRIC INSTITUTE   (United States)

^c New York State Psychiatric Institute ^*  (United States)

Author keywords

Acoustic startle response; Autism; Dexamethasone; Hypothalamic pituitary adrenal axis; Prenatal stress; Psychomotor development; Rat; Schizophrenia; Sensorimotor gating; Social play; Stress hormones

Indexed keywords

AMPHETAMINE; DEXAMETHASONE; GLUCOCORTICOID; GLUCOCORTICOID RECEPTOR;

ANALYSIS OF VARIANCE; ANIMAL; ANIMAL BEHAVIOR; ARTICLE; CHEMICALLY INDUCED DISORDER; DRUG EFFECT; FEMALE; FETOMATERNAL TRANSFUSION; MALE; MATERNAL BEHAVIOR; MOTOR ACTIVITY; PHYSIOLOGY; PREGNANCY; PRENATAL EXPOSURE; RAT; RECREATION; SENSORY GATING; SOCIAL BEHAVIOR; STARTLE REFLEX; STEREOTYPY; WISTAR RAT;

AMPHETAMINE; ANALYSIS OF VARIANCE; ANIMALS; BEHAVIOR, ANIMAL; DEXAMETHASONE; FEMALE; GLUCOCORTICOIDS; MALE; MATERNAL BEHAVIOR; MATERNAL-FETAL EXCHANGE; MOTOR ACTIVITY; PLAY AND PLAYTHINGS; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RATS; RATS, WISTAR; RECEPTORS, GLUCOCORTICOID; SENSORY GATING; SOCIAL BEHAVIOR; STARTLE REACTION; STEREOTYPED BEHAVIOR;

RATTUS;

EID: 77749312988     PISSN: 00121630     EISSN: 10982302     Source Type: Journal    
DOI: 10.1002/dev.20419     Document Type: Article

References (62)

1. Adams, L. A., & Geyer, M. A. (1981). Effects of 6-hydroxydopamine lesions of locus coeruleus on startle in rats. Psychopharmacology, 73(4), 394-398.
2. Arnold, J. L., & Siviy, S. M. (2002). Effects of neonatal handling and maternal separation on rough-and-tumble play in the rat. Developmental Psychobiology, 41(3), 205-215.
3. Baker, S., Chebli, M., Rees, S., Lemarec, N., Godbout, R., & Bielajew, C. (2008). Effects of gestational stress: 1. Evaluation of maternal and juvenile offspring behavior. Brain Research, 1213, 98-110.
4. Barros, V. G., Rodriguez, P., Martijena, I. D., Perez, A., Molina, V. A., & Antonelli, M. C. (2006). Prenatal stress and early adoption effects on benzodiazepine receptors and anxiogenic behavior in the adult rat brain. Synapse, 60(8), 609-618.
5. Beversdorf, D. Q., Manning, S. E., Hillier, A., Anderson, S. L., Nordgren, R. E., Walters, S. E., et al. (2005). Timing of prenatal stressors and autism. Journal of Autism and Developmental Disorders, 35(4), 471-478.
6. Braff, D. L., Geyer, M. A., & Swerdlow, N. R. (2001). Human studies of prepulse inhibition of startle: Normal subjects, patient groups, and pharmacological studies. Psychopharmacology (Berl), 156(2-3), 234-258.
7. Braff, D. L., Grillon, C., & Geyer, M. A. (1992). Gating and habituation of the startle reflex in schizophrenic patients. Archives of General Psychiatry, 49(3), 206-215.
8. Budge, H., Stephenson, T., & Symonds, M. E. (2007). Maternal nutrient restriction is not equivalent to maternal biological stress. Current Drug Targets, 8(8), 888-893.
9. Cannon, T. D., Cadenhead, K., Cornblatt, B., Woods, S. W., Addington, J., Walker, E., et al. (2008). Prediction of psychosis in youth at high clinical risk: A multisite longitudinal study in North America. Archives of General Psychiatry, 65(1), 28-37.
10. Champagne, F. A., & Meaney, M. J. (2006). Stress during gestation alters postpartum maternal care and the development of the offspring in a rodent model. Biological Psychiatry, 59(12), 1227-1235.
11. Estanislau, C., & Morato, S. (2006). Behavior ontogeny in the elevated plus-maze: Prenatal stress effects. International Journal of Developmental Neuroscience, 24(4), 255-262.
12. Hadamitzky, M., Harich, S., Koch, M., & Schwabe, K. (2007). Deficient prepulse inhibition induced by selective breeding of rats can be restored by the dopamine D2 antagonist haloperidol. Behavioural Brain Research, 177(2), 364-367.
13. Hauser, J., Dettling-Artho, A., Pilloud, S., Maier, C., Knapman, A., Feldon, J., et al. (2007). Effects of prenatal dexamethasone treatment on postnatal physical, endocrine, and social development in the common marmoset monkey. Endocrinology, 148(4), 1813-1822.
14. Hauser, J., Feldon, J., & Pryce, C. R. (2006). Prenatal dexamethasone exposure, postnatal development, and adulthood prepulse inhibition and latent inhibition in Wistar rats. Behavioural Brain Research, 175(1), 51-61.
15. Hawkins, P., Steyn, C., McGarrigle, H. H., Calder, N. A., Saito, T., Stratford, L. L., et al. (2000). Cardiovascular and hypothalamic-pituitary- adrenal axis development in late gestation fetal sheep and young lambs following modest maternal nutrient restriction in early gestation. Reproduction, Fertility, and Development, 12(7-8), 443-456. (Pubitemid 32694443)
16. Heller, C. L., Orti, E., & De Nicola, A. F. (1986). Regulatory factors of glucocorticoid binding in early and term rat placenta. Journal of Steroid Biochemistry, 25(1), 53-58.
17. Holmes, M. C., & Seckl, J. R. (2006). The role of 11beta-hydroxysteroid dehydrogenases in the brain. Molecular and Cellular Endocrinology, 248(1-2), 9-14.
18. Hossain, A., Hajman, K., Charitidi, K., Erhardt, S., Zimmermann, U., Knipper, M., & Canlon, B. (2008). Prenatal dexamethasone impairs behavior and the activation of the BDNF Exon IV promoter in the PVN in adult offspring. Endocrinology, 149, 6356-6365.
19. Hougaard, K. S., Andersen, M. B., Kjaer, S. L., Hansen, A. M., Werge, T., & Lund, S. P. (2005). Prenatal stress may increase vulnerability to life events: Comparison with the effects of prenatal dexamethasone. Brain Research Developmental Brain Research, 159(1), 55-63.
20. Kapoor, A., Dunn, E., Kostaki, A., Andrews, M. H., & Matthews, S. G. (2006). Fetal programming of hypothalamo-pituitary-adrenal function: Prenatal stress and glucocorticoids. Journal of Physiology, 572(PART 1), 31-44.
21. Kelly, P. H., Seviour, P. W., & Iversen, S. D. (1975). Amphetamine and apomorphine responses in the rat following 6-OHDA lesions of the nucleus accumbens septi and corpus striatum. Brain Research, 94(3), 507-522.
22. Khashan, A. S., Abel, K. M., McNamee, R., Pedersen, M. G., Webb, R. T., Baker, P. N., et al. (2008). Higher risk of offspring schizophrenia following antenatal maternal exposure to severe adverse life events. Archives of General Psychiatry, 65(2), 146-152.
23. Kinney, D. K., Miller, A. M., Crowley, D. J., Huang, E., & Gerber, E. (2008). Autism prevalence following prenatal exposure to hurricanes and tropical storms in Louisiana. Journal of Autism and Developmental Disorders, 38(3), 481-488.
24. Kranendonk, G., Hopster, H., Fillerup, M., Ekkel, E. D., Mulder, E. J. H., & Taverne, M. A. M. (2006). Cortisol administration to pregnant sows affects novelty-induced locomotion, aggressive behaviour, and blunts gender differences in their offspring. Hormones & Behavior, 49(5), 663- 672.
25. Lajic, S., Nordenstrom, A., & Hirvikoski, T. (2008). Long-term outcome of prenatal treatment of congenital adrenal hyperplasia. Endocrine Development, 13, 82-98.
26. Laplante, D. P., Barr, R. G., Brunet, A., Galbaud du Fort, G., Meaney, M. L., Saucier, J. F., et al. (2004). Stress during pregnancy affects general intellectual and language functioning in human toddlers. Pediatric Research, 56(3), 400- 410.
27. Lee, P. R., Brady, D. L., Shapiro, R. A., Dorsa, D. M., & Koenig, J. I. (2007). Prenatal stress generates deficits in rat social behavior: Reversal by oxytocin. Brain Research, 1156, 152-167.
28. Lobel, M., Cannella, D. L., Graham, J. E., DeVincent, C., Schneider, J., & Meyer, B. A. (2008). Pregnancy-specific stress, prenatal health behaviors, and birth outcomes. Health Psychology, 27(5), 604-615.
29. Maccari, S., & Morley-Fletcher, S. (2007). Effects of prenatal restraint stress on the hypothalamus-pituitary-adrenal axis and related behavioural and neurobiological alterations. Psychoneuroendocrinology, 32(Suppl 1), S10-S15.
30. Malaspina, D., Corcoran, C., Kleinhaus, K. R., Perrin, M. C., Fennig, S., Nahon, D., et al. (2008). Acute maternal stress in pregnancy and schizophrenia in offspring: A cohort prospective study. BMC Psychiatry, 8, 71.
31. Mark, P. J., Augustus, S., Lewis, J. L., Hewitt, D. P., & Waddell, B. J. (2009). Changes in the placental glucocorticoid barrier during rat pregnancy: Impact on placental corticosterone levels and regulation by progesterone. Biology of Reproduction, 80, 1209-1215.
32. Martin-Iverson, M. T., & Stevenson, K. N. (2005). Apomorphine effects on emotional modulation of the startle reflex in rats. Psychopharmacology (Berl) 181, 60-70.
33. McMillen, I. C., Edwards, L. J., Duffield, J., & Muhlhausler, B. S. (2006). Regulation of leptin synthesis and secretion before birth: Implications for the early programming of adult obesity. Reproduction, 131(3), 415-427.
34. Meaney, M. J., Szyf, M., & Seckl, J. R. (2007). Epigenetic mechanisms of perinatal programming of hypothalamicpituitary-adrenal function and health. Trends in Molecular Medicine, 13(7), 269-277.
35. Meyer-Bahlburg, H. F. L., Dolezal, C., Baker, S. W., Carlson, A. D., Obeid, J. S., & New, M. I. (2004). Cognitive and motor development of children with and without congenital adrenal hyperplasia after early-prenatal dexamethasone. Journal of Clinical Endocrinology & Metabolism, 89(2), 610-614.
36. Michael, A. E., & Papageorghiou, A. T. (2008). Potential significance of physiological and pharmacological glucocorticoids in early pregnancy. Human Reproduction Update, 14(5), 497-517.
37. Moore, H., & Robbins, T. W. (2008). Modeling psychiatric disordersin experimental animals. In: Psychiatry. J. K. A. Tasman, J. A. Lieberman, M. B. First, & M. Maj (Eds.), (pp. 275-288). West Sussex: John Wiley & Sons.
38. Morley-Fletcher, S., Rea, M., Maccari, S., & Laviola, G. (2003). Environmental enrichment during adolescence reverses the effects of prenatal stress on play behaviour and HPA axis reactivity in rats. European Journal of Neuroscience, 18(12), 3367-3374.
39. Mueller, B. R., & Bale, T. L. (2008). Sex-specific programming of offspring emotionality after stress early in pregnancy. Journal of Neuroscience, 28(36), 9055-9065.
40. Nagano, M., Ozawa, H., & Suzuki, H. (2008). Prenatal dexamethasone exposure affects anxiety-like behaviour and neuroendocrine systems in an age-dependent manner. Neuroscience Research, 60(4), 364-371.
41. O'Regan, D., Kenyon, C. J., Seckl, J. R., & Holmes, M. C. (2008). Prenatal dexamethasone 'programmes' hypotension, but stress-induced hypertension in adult offspring. Journal of Endocrinology, 196(2), 343-352.
42. Panksepp, J. (1981). The ontogeny of play in rats. Developmental Psychobiology, 14(4), 327-332.
43. Parent, C. I., & Meaney, M. J. (2008). The influence of natural variations in maternal care on play fighting in the rat. Developmental Psychobiology, 50(8), 767-776.
44. 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.
45. Plappert, C. F., & Pilz, P. K. (2001). The acoustic startle response as an effective model for elucidating the effect of genes on the neural mechanism of behavior in mice. Behavioural Brain Research, 125(1-2), 183-188.
46. Quednow, B. B., Frommann, I., Berning, J., Maier, K. U., & Wagner, M. (2008). Impaired sensorimotor gating of the acoustic startle response in the prodrome of schizophrenia. Biological Psychiatry, 64, 766-773.
47. Reul, J. M., van den Bosch, F. R., & de Kloet, E. R. (1987). Relative occupation of type-I and type-II corticosteroid receptors in rat brain following stress and dexamethasone treatment: Functional implications. Journal of Endocrinology, 115(3), 459-467.
48. Seckl, J. R. (2008). Glucocorticoids, developmental 'programming' and the risk of affective dysfunction. Progress in Brain Research, 167, 17-34.
49. Slotkin, T. A., Kreider, M. L., Tate, C. A., & Seidler, F. J. (2006). Critical prenatal and postnatal periods for persistent effects of dexamethasone on serotonergic and dopaminergic systems. Neuropsychopharmacology, 31(5), 904-911.
50. Smith, J. T., & Waddell, B. J. (2003). Leptin distribution and metabolism in the pregnant rat: Transplacental leptin passage increases in late gestation but is reduced by excess glucocorticoids. Endocrinology, 144(7), 3024-3030.
51. Smith, J.W., Seckl, J. R., Evans, A. T., Costall, B., & Smythe, J. W. (2004). Gestational stress induces post-partum depression-like behaviour and alters maternal care in rats. Psychoneuroendocrinology, 29(2), 227-244.
52. Spear, L. P. (2000). The adolescent brain and age-related behavioral manifestations. Neuroscience and Biobehavioral Reviews, 24(4), 417-463.
53. Speirs, H. J., Seckl, J. R., & Brown, R. W. (2004). Ontogeny of glucocorticoid receptor and 11beta-hydroxysteroid dehydrogenase type-1 gene expression identifies potential critical periods of glucocorticoid susceptibility during development. Journal of Endocrinology, 181(1), 105-116.
54. Spencer, R. L., Young, E. A., Choo, P. H., & McEwen, B. S. (1990). Adrenal steroid type I and type II receptor binding: Estimates of in vivo receptor number, occupancy, and activation with varying level of steroid. Brain Research, 514(1), 37-48.
55. Susser, E. S., & Lin, S. P. (1992). Schizophrenia after prenatal exposure to the Dutch Hunger Winter of 1944-1945. Archives of General Psychiatry, 49(12), 983-988.
56. Swerdlow, N. R., Braff, D. L., & Geyer, M. A. (2000). Animal models of deficient sensorimotor gating: What we know, what we think we know, and what we hope to know soon. Behavioural Pharmacology, 11(3-4), 185-204.
57. Takahashi, L. K., Turner, J. G., & Kalin, N. H. (1998). Prolonged stress-induced elevation in plasma corticosterone during pregnancy in the rat: Implications for prenatal stress studies. Psychoneuroendocrinology, 23(6), 571-581.
58. Tazumi, T., Hori, E., Uwano, T., Umeno, K., Tanebe, K., Tabuchi, E., et al. (2005). Effects of prenatal maternal stress by repeated cold environment on behavioral and emotional development in the rat offspring. Behavioural Brain Research, 162(1), 153-160.
59. Vanderschuren, L. J., Niesink, R. J., & Van Ree, J. M. (1997). The neurobiology of social play behavior in rats. Neuroscience and Biobehavioral Reviews, 21(3), 309- 326.
60. Weaver, I. C. G., Cervoni, N., Champagne, F. A., D'Alessio, A. C., Sharma, S., Seckl, J. R., et al. (2004). Epigenetic programming by maternal behavior [see comment]. Nature Neuroscience, 7(8), 847-854.
61. Woods, L. L., & Weeks, D. A. (2005). Prenatal programming of adult blood pressure: Role of maternal corticosteroids. American Journal of Physiology: Regulatory, Integrative and Comparative Physiology, 289(4), R955-R962.
62. Young, N. A., Teskey, G. C., Henry, L. C., & Edwards, H. E. (2006). Exogenous antenatal glucocorticoid treatment reduces susceptibility for hippocampal kindled and maximal electroconvulsive seizures in infant rats. Experimental Neurology, 198(2), 303-312.