The fetal hypothalamic–pituitary–adrenal axis: Relevance to developmental origins of health and disease

Developmental Origins of Health and Disease

Volumn , Issue , 2006, Pages 191-205

  Sloboda, Deborah M ^a   Newnham, John P ^a   Moss, Timothy J M ^a   Challis, John R G ^b  

^a UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 67650633583     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1017/CBO9780511544699.014     Document Type: Chapter

References (137)

1. Amaral, D. G. and Witter, M. P (1989). The three dimensional organization of the hippocampal formation: a review of anatomical data. Neuroscience, 31, 571-91.
2. Andrews, M. H., Kostaki, A., Setiawan, E. et al. (2004). Develop- mentalregulation of 5-HT7 receptor and NGFI-Ain the fetal limbic system: influence of glucocorticoid. J. Physiol., 555, 659-70.
3. Antonow-Schlorke, I., Schwab, M., Li, C. and Nathanielsz, P W. (2003). Glucocorticoid exposure at the dose used clinically alters cytoskeletal proteins and presynaptic terminals in the fetalbaboon brain. J. Physiol., 547, 117-23.
4. Anyaegbunam, W. I. and Adetona, A. B. (1997). Use of antenatal corticosteroids for fetal maturation in preterm infants. Am. Fam. Physician, 56, 1093-6.
5. Austin, M. P and Leader, L. (2000). Maternal stress and obstetric and infant outcomes: epidemiological findings and neuroendocrine mechanisms. Aust. NZ J. Obstet. Gynaecol., 40, 331-7.
6. Bakker, J. M., Schmidt, E. D., Kroes, H. et al. (1995). Effects of short-term dexamethasone treatment during pregnancy on the development of the immune system and the hypothalamo-pituitary adrenal axis in the rat. J. Neuroim- munol., 63, 183-91.
7. Ballard, R. A. and Ballard, P L. (1996). Antenatal hormone therapy for improving the outcome of the preterm infant. J. Perinatol., 16, 390-6.
8. Bamberger, C. M., Schulte, H. M. and Chrousos, G. P (1996). Molecular determinants of glucocorticoid receptor function and tissue sensitivity to glucocorticoids. Endocr. Rev., 17, 245-60.
9. Barker, D. J. P (1966). Low intelligence: its relation to length of gestation and rate of foetal growth. Br. J. Prev. Soc. Med., 20, 58-66.
10. Barker, D. J. P (1994a). The fetal origins of adult disease. Fetal Matern. Med. Rev., 6, 71-80.
11. Barker, D. J. P (1994b). Mothers, Babies and Disease in Later Life., London: BMJ Publishing Group.
12. Barker, D. J. P (1995). The fetal and infant origins of disease. Eur. J. Clini. Investiga., 25, 457-63.
13. Benediktsson, R., Lindsay, R. S., Noble, J. M., Seckl, J. R. and Edwards, C. R. W. (1993). Glucocorticoid exposure in utero: new model for adult hypertension. Lancet, 341, 339-41.
14. Bertram, C. E. and Hanson, M. A. (2002). Prenatalprogramming of postnatalendocrineresponsesbyglucocorticoids. Reproduction, 124, 459-67.
15. Bloomfield, F. H., Oliver, M. H., Hawkins, P et al. (2003).A peri- conceptional nutritional origin for noninfectious preterm birth. Science, 300, 606.
16. Boshier, D. P. and Holloway, H. (1989). Morphometric analyses of adrenal gland growth in fetal and neonatal sheep. I. The adrenal cortex. J. Anat., 167, 1-14.
17. Boshier, D. P. and Holloway, H. (1991). Morphometric analyses of adrenal gland growth in fetal and neonatal sheep. III. Volumes of the major organelles within the zona fasciculata steroidogenic cells. J.Anat., 178, 175-87.
18. Brooks, A. N. and Challis, J. R. G. (1989). Effectsof cRF, AVPand opioid peptides on pituitary-adrenal responses in sheep. Peptides, 10, 1291-3.
19. Challis, J. R. G., Lye, S. J. and Welsh, J. (1986). Ovinefetaladrenal maturation at term and during fetal ACTH administration: evidence that the modulating effect of cortisol mayinvolve cAMP. Can. J. Physiol. Pharmacol., 64, 1085-90.
20. Challis, J. R. G., Sloboda, D., Matthews, S. G. et al. (2001). The fetal placental hypothalamic-pituitary-adrenal (HPA) axis, parturition and post natal health. Mol. Cell. Endocrinol., 185, 135-44.
21. Clark, E M. S., Hindmarsh, E C., Shiell, A. W., Law, C. M., Honour, J. W. and Barker, D. J. P. (1996). Size at birth and adreno- corticalfunction in childhood. Clin. Endocrinol., 45, 721-6.
22. Clarke, A. S., Wittwer, D. J., Abbott, D. H. and Schneider, M. L. (1994). Long-term effects of prenatal stress on HPA axis activity in juvenile rhesus monkeys. Dev. Psychobiol., 27, 257-69.
23. Cox, D. B., Brubaker, P., Fraser, M., Whittle, W. and Challis, J. R. G. (1999). The effect of maternal dexamethasone during early pregnancy on fetal growth, HPA development and the control of glucose homeostasis. J. Soc. Gynecol. Investig., 6, 110A.
24. Crowley, P. (2003). Antenatal corticosteroids: current thinking. BJOG, 110 (Suppl. 20), 77-8.
25. Dean, F. and Matthews, S. G. (1999). Maternal dexametha- sone treatment in late gestation alters glucocorticoid and mineralocorticoid receptor mRNA in the fetal guinea pig brain. Brain Res., 846, 253-9.
26. De Kloet, E. R., Vreugdenhil, E., Oitzl, M. S. and Joels, M. (1998). Brain corticosteroids receptor balance in health and disease. Endocr. Rev., 19, 269-301.
27. Dinan, T. G. (1996). Serotonin and the regulation of hypothalamic-pituitary-adrenal axis function. Life Sci., 58, 1683-94.
28. Dobbing, J. and Sands, J. (1979). Comparative aspects of the brain growth spurt. EarlyHum. Dev., 3, 79-83.
29. Dodic, M. and Wintour, E. M. (1994). Effects of prolonged (48 h) infusion of cortisol on blood pressure, renal function and fetal fluids in the immature ovine foetus. Clin. Exp. Pharmacol. Physiol., 21, 971-80.
30. Dunlop, S. A., Archer, M. A., Quinlivan, J. A., Beazley, L. D. and Newnham, J. P (1997). Repeated prenatal corticosteroids delay myelination in the ovine central nervous system. J. Matern. Fetal Med., 6, 309-13.
31. Durand, P (1979). ACTH receptor levels in lamb adrenals at late gestation and early neonatal stages. Biol. Reprod., 20, 837-45.
32. Durand, P., Bosc, M. J. and Locatelli, A. (1980). Adrenal maturation of the sheep fetus during late pregnancy. Reprod. Nutr. Dev., 20, 339-47.
33. Durand, P., Locatelli, A., Cathiard, A. M., Dazord, A. and Saez, J. M. (1981). ACTH induction of the maturation of ACTH-sensitive adenylate cyclase system in the ovine fetal adrenal. J. SteroidBiochem., 15, 445-8.
34. Edwards, C. R. W., Benediktsson, R., Lindsay, R. S. and Seckl, J. R. (1993).Dysfunction of placental glucocorticoid barrier:link between fetal environment and adult hypertension? Lancet, 341, 355-7.
35. Feldman, S. and Conforti, N. (1980). Participation of the dorsal hippocampus in the glucocorticoid feedback effect on adrenocortical activity. Neuroendocrinology, 30, 52-5.
36. Fernald, L. C. and Grantham-McGregor, S. M. (2002). Growth retardation is associatedwith changes in the stress response system and behavior in school-aged Jamaican children. J. Nutr., 132, 3674-9.
37. Field, T., Diego, M., Hernandez-Reif, M. et al. (2003). Pregnancy anxiety and comorbid depression and anger: effects on the fetus and neonate. Depress. Anxiety, 17, 140-51.
38. Fowden, A. L. and Forhead, A. J. (2004). Endocrine mechanisms of intrauterine programming. Reproduction, 127, 515-26.
39. Fowden, A. L., Li, J. and Forhead, A. J. (1998). Glucocorticoids and the preparation for life after birth: are there long-term consequences of the life insurance? Proc. Nutr Soc., 57, 113-22.
40. Fraser, M., Braems, G. and Challis, J. R. G. (2001a).Developmen- tal regulation of corticotrophin receptor gene expression in the adrenal gland of the ovine fetus and newborn lamb: effects of hypoxia during late pregnancy. J. Endocrinol., 169, 1-10.
41. Fraser, M., Oliver, M. H., Harding, J. E., Gluckman, P. D. and Challis, J. R. G. (2001b). Alterations in ovine fetal adrenal corticotropin receptor and steroidogenic enzyme mRNA expresssion following maternal undernutrition in late pregnancy. J. Soc. Gynecol. Investig., 6, 116A.
42. French, N. P, Evans, S. F, Godfrey, K. M. and Newnham, J. P (1999). Repeated antenatalcorticosteroids: size atbirth and subsequentdevelopment. Am.J. Obstet. Gynecol., 180, 114-21.
43. French, N. P., Hagan, R., Evans, S. F., Mullan, A. and Newnham, J. P (2004). Repeated antenatal corticosteroids: effects on cerebral palsy and childhood behaviour. Am. J. Obstet. Gynecol., 190, 588-95.
44. Gale, C. R., Walton, S. and Martyn, C. N. (2003). Foetal and postnatal head growth and risk of cognitive decline in old age Brain, 126, 2273-8.
45. Glickman, J. A. and Challis, J. R. G. (1980). The changing response pattern of sheep fetal adrenal cells throughout the course of gestation. Endocrinology, 106, 1371-6.
46. Glover, V, O’Connor, T. G., Heron, J. and Golding, J. (2004). Antenatal maternal anxiety is linked with atypical handedness in the child. Early Hum. Dev., 79, 107-18.
47. Goland, R. S., Jozak, S., Warren, W. B., Conwell, I. M., Stark, R. I. and Tropper, P J. (1993). Elevated levels of umbilical cord plasma corticotropin-releasing hormone in growth retarded fetuses. J. Clin. Endocrinol. Metab., 77, 1174-9.
48. Habib, M. and Galaburda, A. M. (1986). [Biological determinants of cerebral dominance]. Rev. Neurol. (Paris), 142, 869-94.
49. Haussmann, M. F., Carroll, J. A., Weesner, G. D., Daniels, M. J., Matteri, R. L. and Lay, D. C. Jr. (2000). Administration of ACTH to restrained, pregnant sows alters their pigs’ hypothalamic-pituitary-adrenal (HPA) axis. J. Anim. Sci., 78, 2399-411.
50. Hawkins, P, Steyn, C., McGarrigle, H. H. G. et al. (1999). Effect of maternal nutrient restiction in early gestation on development of the hypothalamic pituitary adrenal axis in fetal sheep at 0.8-0.9 of gestation. J. Endocrinol., 163, 553-61.
51. Hawkins, P, Steyn, C., McGarrigle, H. H. G. et al. (2000). Effect of maternal nutrient restriction in early gestation on hypothalamic pituitary adrenal axis responses during acute hypoxemia in late gesation fetal sheep. Exp. Physiol., 85, 85-96.
52. Hawkins, P., Hanson, M. A. and Matthews, S. G. (2001). Maternal undernutrition in early gestation alters molecular regulation of the hypothalamic-pituitary-adrenal axis in the ovine fetus. J. Neuroendocrinol., 13, 855-61.
53. Herrick, K., Phillips, D. I., Haselden, S., Shiell, A. W., Campbell- Brown, M. and Godfrey, K. M. (2003). Maternal consumption of a high-meat, low-carbohydrate diet in late pregnancy: relation to adult cortisol concentrations in the offspring. J. Clin. Endocrinol. Metab., 88, 3554-60.
54. Holmes, M. C., French, K. L. and Seckl, J. R. (1997). Dysregulation of diurnal rhythms of serotonin 5-HT2C and corticosteroid receptor gene expression in the hippocampus with food restriction and glucocorticoids. J. Neurosci., 17, 4056-65.
55. Huang, W. L., Beazley, L. D., Quinlivan, J. A., Evans, S., Newnham, J. and Dunlop, S. A. (1999). Effect of corticosteroids on brain growth in fetal sheep Obstet. Gynecol., 94, 213-18.
56. Jacobson, L. and Sapolsky, R. M. (1991). The role of the hippocampus in feedback regulation of the hypothalamic- pituitary-adrenocortical axis. Endocr. Rev., 12, 118-34.
57. Jacobson, L., Zurakowski, D. and Majzoub, J. A. (1997). Protein malnutrition increases plasma adrenocorticotropin and anterior pituitary proopiomelanocortin messenger ribonucleic acid in the rat. Endocrinology, 138, 1048-57.
58. Kajantie, E., Dunkel, L., Turpeinen, U. et al. (2003). Placental 11p-hydroxysteroid dehydrogenase-2 and fetal corti- sol/cortisone shuttle in small preterm infants. J. Clin. Endocrinol. Metab., 88, 493-500.
59. Kari, M. A., Hallman, M., Eronen, M. et al. (1994). Prenatal dexa- methasone treatment in conjunction with rescue therapy of human surfactant: a randomized placebo-controlled multicenter study. Pediatrics, 93, 730-6.
60. Koehl, M., Barbazanges, A., Le Moal, M. and Maccari, S. (1997). Prenatal stress induces a phase advance of circadian corticosterone rhythm in adult rats which is prevented by postnatal stress. Brain Res., 759, 317-20.
61. Kof man, O. (2002). The role of prenatal stress in the etiology of developmental behavioural disorders. Neurosci. Biobehav. Rev., 26, 457-70.
62. Kupfermann, I. (1991). Hypothalamus and limbic system: peptidergic neurons, homeostasis, and emotional behavior. In Principlesof neuralScience (ed. E. R. Kandel, J. H. Schwartz and T. M. Jessell). New York, NY: Elsevier, pp. 735-49.
63. Langley-Evans, S. C., Gardner, D. S. and Jackson, A. A. (1996a). Maternal protein restriction influences the programming of the rat hypothalamic-pituitary-adrenal axis. J. Nutr., 126, 1578-85.
64. Langley-Evans, S. C., Phillips, G. J., Benediktsson, R. et al. (1996b). Protein intake in pregnancy, placental glucocorticoid metabolism and the programming of hypertension in the rat. Placenta, 17, 169-72.
65. Laplante, P., Diorio, J. and Meaney, M. J. (2002). Serotonin regulates hippocampal glucocorticoid receptor expression via a 5-HT7 receptor. Brain Res. Dev. Brain Res., 139, 199-203.
66. Lemaire, V, Koehl, M., LeMoal, M. and Abrous, D. N. (2000). Prenatal stress produces learning deficits associated with an inhibition of neurogenesis in the hippocampus. Proc. Natl. Acad. Sci. USA, 97, 11032-7.
67. Leon, D. A. (2001). Commentary. Getting to grips with fetal programming: aspects of a rapidly evolving agenda. Int. J. Epidemiol., 30, 96-8.
68. Levidiotis, M. L., Oldfield, B. J. and Wintour, E. M. (1987). Corticotropin-releasing factor and arginine vasopressin fibre projections to the median eminence of fetal sheep. Neuroendocrinology, 46, 453-6.
69. Levitt, N. S., Lindsay, R. S., Holmes, M. C. and Seckl, J. R. (1996). 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, 412-19.
70. Levitt, N. S., Lambert, E. V., Woods, D., Hales, C. N., Andrew, R. and Seckl, J. R. (2000). Impaired glucose tolerance and elevated blood pressure in low birth weight, nonobese, young south african adults: early programming of cortisol axis. J. Clin. Endocrinol. Metab., 85, 4611-18.
71. Liakos, P., Chambaz, E. M., Feige, J. J. and Defaye, G. (1998). Expression of ACTH receptors (MC2-R and MC5-R) in the glomerulosa and the fasciculata-reticularis zones of bovine adrenal cortex. Endocr. Res., 24, 427-32.
72. Liggins, G. C. (1969). Premature delivery of fetal lambs infused with glucocorticoids. J. Endocrinol., 45, 515-23.
73. Liggins, G. C. (1994). The role of cortisol in preparing the fetus for birth. Reprod., Fertil Dev., 6, 141-50.
74. Liggins, G. C. and Howie, R. N. (1972). A controlled trial of antepartum glucocorticoid treatment for prevention of the respiratory distress syndrome in premature infants. Pediatrics, 50, 515-25.
75. Liggins, G. C. and Kennedy, P. C. (1968). Effects of electrocoagulation of the fetal lamb hypophysis on growth and development. J. Endocrinol., 40, 371-81.
76. Lindsay, R. S., Lindsay, R. M., Waddell, B. J. and Seckl, J. R. (1996). Prenatal glucocorticoid exposure leads to offspring hyper- glycaemia in the rat: studies with the 11p-hydroxysteroid dehydrogenase inhibitor carbenoxolone. Diabetologia, 39, 1299-305.
77. Lingas, R., Dean, F. and Matthews, S. G. (1999).Maternalnutient restriction (48h) modifies brain corticosteorid receptor expression and endocrine function in the fetal guinea pig. Brain Res., 846, 236-42.
78. Lu, F. and Challis, J. R. G. (1994). Regulation of ovine fetal pituitary function by corticotrophin-releasing hormone, arginine vasopressin and cortisol in vitro. J. Endocrinol., 143, 199-208.
79. Lunblad, J. R. and Roberts, J. L. (1988). Regulation of proopiomelanocortin gene expression in pituitary. Endocr. Rev., 9, 135-58.
80. Mandell, A. J., Chapman, L. F, Rand, R. W and Walter, R. D. (1963). Plasma corticosteroids: changes in concentration after stimulation of hippocampus and amygdala. Science, 139, 1212.
81. Matthews, S. G. (2001).Antenatalglucocorticoidsandthe developing brain: mechanisms of action. Semin. Neonatol., 6, 309-17.
82. Matthews, S. G. and Challis, J. R. G. (1995). Levels of proopiomelanocortin and prolactin mRNA in the fetal sheep pituitary following hypoxemia and glucocorticoid treatment in late gestation. J. Endocrinol., 147, 139-46.
83. Matthews, S. G., Owen, D., Kalabis, G. et al. (2004). Fetal glucocorticoid exposure and hypothalamo-pituitary-adrena! (HPA) function after brith. Endocr. res., 30, 827-36.
84. McCormick, C. M., Smythe, J. W., Sharma, S. and Meaney, M. (1995). Sex specific effects of prenatal stress on hypothalamic-pituitary adrenal responses to stress and brain gluccocorticoid receptors density in rats. Dev. Brain Res., 84, 55-61.
85. McDonald, T. J., Hoffman, G. E. and Nathaneilsz, P W. (1992). Hypothalamic paraventricular nuclear lesions delay cor- ticotroph maturation in the fetal sheep anterior pituitary. Endocrinology, 131, 1101-6.
86. McLaughlin, K. J. and Crowther, C. A. (2003). Repeat prenatal corticosteroids: who still recommends their use and why? Aust. NZ J. Obstet. Gynaecol., 43, 199-202.
87. McMullen, S., Osgerby, J. C., Thurston, L. M. et al. (2004).Alter- ations in placental 11 beta-hydroxysteroid dehydrogenase (11 betaHSD) activities and fetal cortisol: cortisone ratios induced by nutritional restriction prior to conception and at defined stages of gestation in ewes. Reproduction, 127, 717-25.
88. Meaney, M., Sapolsky, R. M. and McEwen, B. S. (1985).The development of the glucocorticoid receptor system in the rat limbic brain. I. Ontogeny and autoregulation. Dev. Brain Res., 18, 159-164.
89. Modi, N., Lewis, H., Al-Naqeeb, N., Ajayi-Obe, M., Dore, C. J. and Rutherford, M. (2001). The effects of repeated antenatal glucocorticoid therapy on the developing brain. Pediatr. Res., 50, 581-5.
90. Moss, T. J. M., Doherty, D., Nitsos, I., Sloboda, D. M., Harding, R. and Newnham, J. P (2005). Effects into adulthood of single or repeated antenatalcorticosteroids in sheep. Am. J. Obstet. Gynecol., 192, 146-52.
91. Mulchahey, J. J., DiBlasio, A. M., Martin, M. C., Blumenfeld, Z. and Jaffe, R. B. (1987). Hormone production and peptide regulation of the human fetal pituitary gland. Endocr Rev., 8, 406-425.
92. Muneoka, K., Mikuni, M., Ogawa, T. et al. (1997). Prenataldexa- methasone exposure alters brain monoamine metabolism and adrenocortical response in rat offspring. Am. J. Physiol., 273, R1669-75.
93. Newnham, J. P, Evans, S. F, Godfrey, M., Huang, W., Ikegami, M. and Jobe, A. (1999). Maternal, but not fetal, administration of corticosteroids restrictsfetalgrowth. J. Matern. Fetal Med., 8, 81-7.
94. NIH (1995).Effectof corticosteroidsforfetalmaturationonperi- natal outcomes, NIH Consensus Development Panel on the Effect of Corticosteroids for Fetal Maturation on Perinatal Outcomes. JAMA, 273, 413-18.
95. NIH (2001). Antenatal corticosteroids revisited: repeat courses. National Institutes of Health Consensus Development Conference Statement, August17-18, 2000. Obstet. Gynecol., 98, 144-50.
96. Norman, L. J., Lye, S.J., Wlodek, M. E. and Challis, J.R.G. (1985). Changes in pituitary responses to synthetic ovine corti- cotrophin releasing factor in fetal sheep. Can. J. Physiol. Pharmacol., 63, 1398-403.
97. O’Connor, T. G., Heron, J., Golding, J. and Glover, V (2003). Maternal antenatal anxiety and behavioural/emotional problems in children: a test of a programming hypothesis. J. Child Psychol. and Psychiatry., 44, 1025-36.
98. Owen, D. and Matthews, S. G. (2003). Glucocorticoids and sex-dependent development of brain glucocorticoid and mineralocorticoid receptors. Endocrinology, 144, 2775-84.
99. Page, R. B. (1988). The anatomy of the hypothalamo- hypophyseal complex. In The Physiology of Reproduction (ed. E. Knobil and J. D. Neill). New York, NY: Raven Press pp. 1161-233.
100. Pasamanick, B. and Lilienfeld, A. M. (1955).Associationof mater- nal and fetal factors with development of mental deficiency. 1. Abnormalities in the prenatal and paranatal periods. J Am Med Assoc, 159, 155-60.
101. Perry, R.A., Robinson, P M. and Ryan, G. B. (1982). Ultrastructure of the pars intermedia of the developing sheep hypophysis. Cell Tissue Res., 224, 369-81.
102. Perry, R.A., Mulvogue, H. M., McMillen, I. C. and Robinson, P M. (1985). Immunohistochemical localization of ACTH in the adult and fetal sheep pituitary. J. Dev. Physiol., 7, 397-404.
103. Phillips, D. I. (2001). Fetal growth and programming of the hypothalamic-pituitary-adrenal axis. Clin. Exp. Pharmacol. Physiol., 28, 967-70.
104. Quinlivan, J. A., Dunlop, S. A., Newnham, J., Evans, S. F and Beazley, L. D. (1999). Repeated, but not single, maternal administration of corticosteroids delays myelination in the brain of fetal sheep. Prenat. NeonatalMed., 4, 47-55.
105. Reperant, E. N. and Durand, P (1997). The development of the ovine fetal adrenal gland and its regulation. Reprod. Nutr. Dev. 37, 81-95.
106. Reul, J. M. H. M. and De Kloet, E. R. (1985). Two receptor systems for corticosterone in rat brain: microdistribution and differential occupation. Endocrinology, 117, 2505-11.
107. Reynolds, R. M., Walker, B. R., Syddall, H. E. et al. (2001a).Altered control of cortisol secretion in adult men with low birth weight and cardiovascular risk factors. J. Clin. Endocrinol. Metab., 86, 245-50.
108. Reynolds, R. M., Walker, B. R., Syddall, H. E. et al. (2001b). Elevated plasma cortisol in glucose-intolerant men: differences in responses to glucose and habituation to venepuncture. J. Clin. Endocrinol. Metab., 86, 1149-53.
109. Richards, M., Hardy, R., Kuh, D. and Wadsworth, M. E. J. (2001). Birth weight and cognitive function in the British 1946 birth cohort: longitudinal population based study. BMJ, 322, 199-203.
110. Roussel, S., Hemsworth, P. H., Boissy, A. and Duvaux-Ponter, C. (2004). Effects of repeated stress during pregnancy in ewes on the behavioural and physiological responses to stressful events and birth weight of their offspring. Appl. Anim. Behav. Sci., 85, 259-76.
111. Rubin, R. T., Mandell, A. J. and Crandall, P. H. (1966). Corticosteroid responses to limbic stimulation in man: localization of stimulus site. Science, 153, 767-8.
112. Sebaai, N., Lesage, J., Breton, C., Vieau, D. and Deloof, S. (2004). Perinatal food deprivation induces marked alterations of the hypothalamo-pituitary-adrenal axis in 8-month-old male rats both under basal conditions and after a dehydration period. Neuroendocrinology, 79, 163-73.
113. Setiawan, E., Owen, D., McCabe, L., Kostaki, A., Andrews, M. H. and Matthews, S. G. (2004). Glucocorticoids do not alter developmental expression of hippocampal or pituitary steroid receptor coactivator-1 and -2 in the late gestation fetal guinea pig. Endocrinology, 145, 3796-803.
114. Sloboda, D. M., Newnham, J. and Challis, J. R. G. (2000). Effects of repeated maternal betamethasone administration on growth and hypothalamic-pituitary-adrenal function of the ovine fetus at term. J. Endocrinol., 165, 79-91.
115. Sloboda, D. M., Moss, T. J., Gurrin, L. C., Newnham, J. and Challis, J. R. G. (2002). The effect of prenatal betamethasone administration on postnatal ovine hypothalamic- pituitary-adrenalfunction. J. Endocrinol., 172, 71-81.
116. Sloboda, D. M., Moss, T., Nitsos, I., Doherty, D. A., Challis, J. R. G. and Newnham, J. P. (2003). Antenatal glucocorticoid treatment in sheep results in adrenal suppression in adulthood. J. Soc. Gynecol. Investig., 10, 233A.
117. Stathis, S. L., O’Callaghan, M., Harvey, J. and Rogers, Y. (1999). Head circumference in ELBW babies is associated with learning difficulties and cognition but not ADHD in the school-aged child. Dev. Med. Child Neurol., 41, 375-80.
118. Stewart, PM., Rogerson, FM. and Mason, J. I. (1995).Type211p hydroxysteroid dehydrogenase messenger ribonucleic acid and activity in human placenta and fetal membranes: its relationship to birthweight and putative role in fetal adrenal steroidogenesis. J. Clin. Endocrinol. Metab., 80, 885-90.
119. Swanson, L. W and Sawchenko, P E. (1983). Hypothalamic integration: organization of the paraventricular and supraoptic nuclei. Ann. Rev. Neurosci., 6, 269-324.
120. Swanson, L. W and Simmons, D. M. (1989).Differential steroid hormone and neural influences on peptide mRNA levels in CRH cells of the paraventricular nucleus: a hybridization histochemical study in the rat. J. Comp. Neurol., 285, 413-35.
121. Takahashi, L. K. (1998). Prenatal stress: consequences of glucocorticoids on hippocampal development and function. Internat. J. Neurosci., 16, 199-207.
122. Takahashi, L. K. and Kalin, N. H. (1991). Early developmental and temporal characteristics of stress-induced secretion of pituitary adrenal hormones in prenatally stressed rat pups. Brain Res., 558, 75-8.
123. Tonolo, G., Fraser, G., Connell, J. M. and Kenyon, C. J. (1988). Chronic low dose infusions of dexamethasone in rats: effects on blood pressure, body weight and plasma atrial natriuretic peptide. J. Hypertens., 6, 25-31.
124. Toth, M. (2003). 5-HT1A receptor knockout mouse as a genetic model of anxiety. Eur. J. Pharmacol., 463, 177-84.
125. Uno, H., Lohmiller, L., Thieme, C. et al. (1990). Brain damage induced by prenatal exposure to dexamethasone in fetal rhesus macaques. I. Hippocampus. Dev. Brain Res., 53, 157-67.
126. Uno, H., Eisele, S., Sakai, A. et al. (1994). Neurotoxicityof gluco- corticoids in the primate brain. Horm. Behav., 28, 336-48.
127. Vallee, M., Mayo, W., Maccari, S., Le Moal, M. and Simon, H. (1996). Long-term effects of prenatal stress and handling on metabolic parameters: relationship to corticosterone secretion response. Brain Res., 712, 287-92.
128. Van den Bergh, B. R. and Marcoen, A. (2004). High antenatal maternal anxiety is related to ADHD symptoms, externalizing problems, and anxiety in 8- and 9-year-olds Child Dev., 75, 1085-97.
129. Vazquez, D. M., Van Oers, H., Levine, S. and Akil, H. (1996). Regulation of glucocorticoid and mineralocorticoid receptor mRNAs in the hippocampus of the maternallydeprived infant rat. BrainRes., 761, 79-90.
130. Wang, J. J., Valego, N. K., Su, Y., Smith, J. and Rose, J. C. (2004). Developmental aspects of ovine adrenal adrenocorticotropic hormone receptorexpression. J. Soc. Gynecol. Investig., 11, 27-35.
131. Weaver, I. C., Cervoni, N., Champagne, F. A. et al. (2004). Epi- genetic programming by maternal behavior. Nat. Neurosci., 7, 847-54.
132. Webb, P D. (1980). Development of the adrenal cortex in the fetal sheep: an ultrastructural study. J. Dev. Physiol., 2, 161-81.
133. Weinstock, M. (1996). Does prenatal stress impair coping and regulation of hypothalamic-pituitary-adrenal axis? Neurosci. Biobehav. Rev., 21, 1-10.
134. Weinstock, M., Matlina, E., Maor, G. I., Rosen, H. and McEwen, B. S. (1992). Prenatal stress selectivelyaltersthe reactivityof the hypothalamic-pituitary-adrenal system in the female rat. Brain Res., 595, 195-200.
135. Welberg, L. A. M. and Seckl, J. R. (2001). Prenatal stress, glucocorticoids and the programming of the brain. J. Neuroen- docrinol., 13, 113-28.
136. Welberg, L.A. M., Seckl, J. R. and Holmes, M. C. (2000).Inhibition of 11β-hydroxysteroid dehydrogenase, the fetal-placental barrier to maternal glucocorticoids, permanenetly programs amygdala GRmRNA expression and anxiety-like behaviour in the offspring. Eur. J. Neurosci., 12, 1047-54.
137. Wintour, E. M., Brown, E. H., Denton, D. A. et al. (1975). The ontogeny and regulation of corticosteroid secretion by the ovine foetal adrenal. ActaEndocrinol., 79, 301-16.