Neurochemical Research

, Volume 32, Issue 10, pp 1730–1740 | Cite as

Gender Differences in the Effects of Prenatal Stress on Brain Development and Behaviour

Original Paper

Abstract

An increased incidence of anxiety, depression and attention deficits in children has been linked to psychological stress during pregnancy. Subjection of a pregnant rat to stress at a time when the foetal limbic and hypothalamic pituitary adrenal (HPA) axes develop results in anxiogenic and depressive behaviour and learning and attention deficits in the offspring, which depend on its gender, intensity and timing of the maternal stress and behaviour being tested. Maternal stress increases corticosterone levels in the foetal brain, decreases foetal testosterone and brain aromatase activity in males, and alters brain catecholamine activity to that in females. Learning deficits, reductions in hippocampal neurogenesis, LTP and dendritic spine density in the prefrontal cortex are more readily seen in prenatally-stressed males, while anxiety, depression and increased response of the HPA axis to stress are more prevalent in females. Genders may differ in the sensitivity of developing brain areas to stress hormones.

Keywords

Prenatal stress Male and female rats Anxiety and depression Spatial learning 

References

  1. 1.
    Beversdorf DQ, Manning SE, Hillier A et al (2005) Timing of prenatal stressors and autism. J Autism Dev Disord 35:471–478PubMedGoogle Scholar
  2. 2.
    van Os J, Selten JP (1998) Prenatal exposure to maternal stress and subsequent schizophrenia. The May 1940 invasion of The Netherlands. Br J Psychiatry 172:324–326PubMedGoogle Scholar
  3. 3.
    Weinstock M (2001) Alterations induced by gestational stress in brain morphology and behaviour of the offspring. Prog Neurobiol 65:427–451PubMedGoogle Scholar
  4. 4.
    Woolley CS, Weiland NG, McEwen BS et al (1997) Estradiol increases the sensitivity of hippocampal CA1 pyramidal cells to NMDA receptor-mediated synaptic input: correlation with dendritic spine density. J Neurosci 17:1848–1859PubMedGoogle Scholar
  5. 5.
    Meijer A (1985) Child psychiatric sequelae of maternal war stress. Acta Psychiatr Scand 72:505–511PubMedGoogle Scholar
  6. 6.
    Wust S, Entringer S, Federenko IS et al (2005) Birth weight is associated with salivary cortisol responses to psychosocial stress in adult life. Psychoneuroendocrinology 30:591–598PubMedGoogle Scholar
  7. 7.
    Taylor DC (1969) Differential rates of cerebral maturation between sexes and between hemispheres. Evidence from epilepsy. Lancet 2:140–142PubMedGoogle Scholar
  8. 8.
    Watson JB, Mednick SA, Huttunen M et al (1999) Prenatal teratogens and the development of adult mental illness. Dev Psychopathol 11:457–466PubMedGoogle Scholar
  9. 9.
    Sandman CA, Wadhwa PD, Chicz-DeMet A et al (1999) Maternal corticotropin-releasing hormone and habituation in the human fetus. Dev Psychobiol 34:163–173PubMedGoogle Scholar
  10. 10.
    Inder WJ, Prickett TC, Ellis MJ et al (2001) The utility of plasma CRH as a predictor of preterm delivery. J Clin Endocrinol Metab 86:5706–5710PubMedGoogle Scholar
  11. 11.
    Hadders-Algra M, Huisjes HJ, Touwen BC (1988) Perinatal risk factors and minor neurological dysfunction: significance for behaviour and school achievement at nine years. Dev Med Child Neurol 30:482–491PubMedCrossRefGoogle Scholar
  12. 12.
    Holst K, Andersen E, Philip J et al (1989) Antenatal and perinatal conditions correlated to handicap among 4-year-old children. Am J Perinatol 6:258–267PubMedCrossRefGoogle Scholar
  13. 13.
    Fride E, Dan Y, Feldon J et al (1986) Effects of prenatal stress on vulnerability to stress in prepubertal and adult rats. Physiol Behav 37:681–687PubMedGoogle Scholar
  14. 14.
    Schneider ML (1992) Prenatal stress exposure alters postnatal behavioral expression under conditions of novelty challenge in rhesus monkey infants. Dev Psychobiol 25:529–540PubMedGoogle Scholar
  15. 15.
    Takahashi LK, Haglin C, Kalin NH (1992) Prenatal stress potentiates stress-induced behavior and reduces the propensity to play in juvenile rats. Physiol Behav 51:319–323PubMedGoogle Scholar
  16. 16.
    Alonso SJ, Arevalo R, Afonso D et al (1991) Effects of maternal stress during pregnancy on forced swimming test behavior of the offspring. Physiol Behav 50:511–517PubMedGoogle Scholar
  17. 17.
    Secoli SR, Teixeira NA (1998) Chronic prenatal stress affects development and behavioral depression in rats. Stress 2:273–280PubMedGoogle Scholar
  18. 18.
    Lemaire V, Koehl M, Le Moal M et al (2000) Prenatal stress produces learning deficits associated with an inhibition of neurogenesis in the hippocampus. Proc Natl Acad Sci USA 97:11032–11037PubMedGoogle Scholar
  19. 19.
    Yang J, Han H, Cao J et al (2006) Prenatal stress modifies hippocampal synaptic plasticity and spatial learning in young rat offspring. Hippocampus 16:431–436PubMedGoogle Scholar
  20. 20.
    Burton C, Lovic V, Fleming AS (2006) Early adversity alters attention and locomotion in adult sprague-dawley rats. Behav Neurosci 120:665–675PubMedGoogle Scholar
  21. 21.
    MacLusky NJ, Naftolin F (1981) Sexual differentiation of the central nervous system. Science 211:1294–1302PubMedGoogle Scholar
  22. 22.
    Matsumoto A (1991) Synaptogenic action of sex steroids in developing and adult neuroendocrine brain. Psychoneuroendocrinology 16:25–40PubMedGoogle Scholar
  23. 23.
    McEwen BS, Lieberburg I, Chaptal C et al (1977) Aromatization: important for sexual differentiation of the neonatal rat brain. Horm Behav 9:249–263PubMedGoogle Scholar
  24. 24.
    Selmanoff MK, Brodkin LD, Weiner RI et al (1977) Aromatization and 5alpha-reduction of androgens in discrete hypothalamic and limbic regions of the male and female rat. Endocrinology 101:841–848PubMedGoogle Scholar
  25. 25.
    Palanza P (2001) Animal models of anxiety and depression: how are females different? Neurosci Biobehav Rev 25:219–233PubMedGoogle Scholar
  26. 26.
    Diamond MC, Johnson RE, Young D et al (1983) Age-related morphologic differences in the rat cerebral cortex and hippocampus: male-female; right-left. Exp Neurol 81:1–13PubMedGoogle Scholar
  27. 27.
    Fleming DE, Anderson RH, Rhees RW et al (1986) Effects of prenatal stress on sexually dimorphic asymmetries in the cerebral cortex of the male rat. Brain Res Bull 16:395–398PubMedGoogle Scholar
  28. 28.
    Gorski RA, Gordon JH, Shryne JE et al (1978) Evidence for a morphological sex difference within the medial preoptic area of the rat brain. Brain Res 148:333–346PubMedGoogle Scholar
  29. 29.
    Davis EC, Popper P, Gorski RA (1996) The role of apoptosis in sexual differentiation of the rat sexually dimorphic nucleus of the preoptic area. Brain Res 734:10–18PubMedGoogle Scholar
  30. 30.
    Jones HE, Ruscio MA, Keyser LA et al (1997) Prenatal stress alters the size of the rostral anterior commissure in rats. Brain Res Bull 42:341–346PubMedGoogle Scholar
  31. 31.
    Valenstein ES, Kakolewski JW, Cox VC (1967) Sex differences in taste preference for glucose and saccharin solutions. Science 156:942–943PubMedGoogle Scholar
  32. 32.
    Bowman RE, MacLusky NJ, Sarmiento Y et al (2004) Sexually dimorphic effects of prenatal stress on cognition, hormonal responses, and central neurotransmitters. Endocrinology 145:3778–3787PubMedGoogle Scholar
  33. 33.
    Fride E, Weinstock M (1988) Prenatal stress increases anxiety related behavior and alters cerebral lateralization of dopamine activity. Life Sci 42:1059–1065PubMedGoogle Scholar
  34. 34.
    Johnston AL, File SE (1991) Sex differences in animal tests of anxiety. Physiol Behav 49:245–250PubMedGoogle Scholar
  35. 35.
    Nishio H, Kasuga S, Ushijima M et al (2001) Prenatal stress and postnatal development of neonatal rats—sex-dependent effects on emotional behavior and learning ability of neonatal rats. Int J Dev Neurosci 19:37–45PubMedGoogle Scholar
  36. 36.
    Frye CA, Wawrzycki J (2003) Effect of prenatal stress and gonadal hormone condition on depressive behaviors of female and male rats. Horm Behav 44:319–326PubMedGoogle Scholar
  37. 37.
    Marcondes FK, Miguel KJ, Melo LL et al (2001) Estrous cycle influences the response of female rats in the elevated plus-maze test. Physiol Behav 74:435–440PubMedGoogle Scholar
  38. 38.
    Farabollini F, Fluck E, Albonetti ME et al (1996) Sex differences in benzodiazepine binding in the frontal cortex and amygdala of the rat 24 h after restraint stress. Neurosci Lett 218:177–180PubMedGoogle Scholar
  39. 39.
    Fride E, Dan Y, Gavish M et al (1985) Prenatal stress impairs maternal behavior in a conflict situation and reduces hippocampal benzodiazepine receptors. Life Sci 36:2103–2109PubMedGoogle Scholar
  40. 40.
    Ward IL, Weisz J (1984) Differential effects of maternal stress on circulating levels of corticosterone, progesterone, and testosterone in male and female rat fetuses and their mothers. Endocrinology 114:1635–1644PubMedCrossRefGoogle Scholar
  41. 41.
    Ward IL (1972) Prenatal stress feminizes and demasculinizes the behavior of males. Science 175:82–84PubMedGoogle Scholar
  42. 42.
    Weisz J, Brown BL, Ward IL (1982) Maternal stress decreases steroid aromatase activity in brains of male and female rat fetuses. Neuroendocrinology 35:374–379PubMedGoogle Scholar
  43. 43.
    Reznikov AG, Nosenko ND, Tarasenko LV (1999) Prenatal stress and glucocorticoid effects on the developing gender-related brain. J Steroid Biochem Mol Biol 69:109–115PubMedGoogle Scholar
  44. 44.
    Rhees RW, Al-Saleh HN, Kinghorn EW et al (1999) Relationship between sexual behavior and sexually dimorphic structures in the anterior hypothalamus in control and prenatally stressed male rats. Brain Res Bull 50:193–199PubMedGoogle Scholar
  45. 45.
    Reznikov AG, Nosenko ND (1995) Catecholamines in steroid-dependent brain development. J Steroid Biochem Mol Biol 53:349–353PubMedGoogle Scholar
  46. 46.
    Ward IL, Stehm KE (1991) Prenatal stress feminizes juvenile play patterns in male rats. Physiol Behav 50:601–605PubMedGoogle Scholar
  47. 47.
    Masterpasqua F, Chapman RH, Lore RK (1976) The effects of prenatal psychological stress on the sexual behavior and reactivity of male rats. Dev Psychobiol 9:403–411PubMedGoogle Scholar
  48. 48.
    McGivern RF, Poland RE, Taylor AN et al (1986) Prenatal stress feminizes adult male saccharin preference and maze learning: antagonism by propranolol. Monogr Neural Sci 12:172–178PubMedGoogle Scholar
  49. 49.
    Jimbo M, Okubo K, Toma Y et al (1998) Inhibitory effects of catecholamines and maternal stress on aromatase activity in the fetal rat brain. J Obstet Gynaecol Res 24:291–297PubMedCrossRefGoogle Scholar
  50. 50.
    Raum WJ, Marcano M, Swerdloff RS (1984) Nuclear accumulation of estradiol derived from the aromatization of testosterone is inhibited by hypothalamic beta-receptor stimulation in the neonatal female rat. Biol Reprod 30:388–396PubMedGoogle Scholar
  51. 51.
    Rojo M, Marin B, Menendez-Patterson A (1985) Effects of low stress during pregnancy on certain parameters of the offspring. Physiol Behav 34:895–899PubMedGoogle Scholar
  52. 52.
    Holson RR, Gough B, Sullivan P et al (1995) Prenatal dexamethasone or stress but not ACTH or corticosterone alter sexual behavior in male rats. Neurotoxicol Teratol 17:393–401PubMedGoogle Scholar
  53. 53.
    Keshet GI, Weinstock M (1995) Maternal naltrexone prevents morphological and behavioral alterations induced in rats by prenatal stress. Pharmacol Biochem Behav 50:413–419PubMedGoogle Scholar
  54. 54.
    Ward OB, Monaghan EP, Ward IL (1986) Naltrexone blocks the effects of prenatal stress on sexual behavior differentiation in male rats. Pharmacol Biochem Behav 25:573–576PubMedGoogle Scholar
  55. 55.
    Takahashi LK, Turner JG, Kalin NH (1998) Prolonged stress-induced elevation in plasma corticosterone during pregnancy in the rat: implications for prenatal stress studies. Psychoneuroendocrinology 23:571–581PubMedGoogle Scholar
  56. 56.
    Weinstock M, Fride E, Hertzberg R (1988) Prenatal stress effects on functional development of the offspring. Prog Brain Res 73:319–331PubMedCrossRefGoogle Scholar
  57. 57.
    Rohde W, Ohkawa T, Dobashi K et al (1983) Acute effects of maternal stress on fetal blood catecholamines and hypothalamic LH-RH content. Exp Clin Endocrinol 82:268–274PubMedGoogle Scholar
  58. 58.
    Cintra A, Solfrini V, Bunnemann B et al (1993) Prenatal development of glucocorticoid receptor gene expression and immunoreactivity in the rat brain and pituitary gland: a combined in situ hybridization and immunocytochemical analysis. Neuroendocrinology 57:1133–1147PubMedGoogle Scholar
  59. 59.
    Fujioka T, Sakata Y, Yamaguchi K et al (1999) The effects of prenatal stress on the development of hypothalamic paraventricular neurons in fetal rats. Neuroscience 92:1079–1088PubMedGoogle Scholar
  60. 60.
    Fujioka T, Fujioka A, Endoh H et al (2003) Materno-fetal coordination of stress-induced Fos expression in the hypothalamic paraventricular nucleus during pregnancy. Neuroscience 118:409–415PubMedGoogle Scholar
  61. 61.
    Ohkawa T, Rohde W, Takeshita S et al (1991) Effect of an acute maternal stress on the fetal hypothalamo-pituitary-adrenal system in late gestational life of the rat. Exp Clin Endocrinol 98:123–129PubMedCrossRefGoogle Scholar
  62. 62.
    Ohkawa T, Takeshita S, Murase T et al (1991) The effect of an acute stress in late pregnancy on hypothalamic catecholamines of the rat fetus. Nippon Sanka Fujinka Gakkai Zasshi 43:783–787PubMedGoogle Scholar
  63. 63.
    Maccari S, Darnaudery M, Morley-Fletcher S et al (2003) Prenatal stress and long-term consequences: implications of glucocorticoid hormones. Neurosci Biobehav Rev 27:119–127PubMedGoogle Scholar
  64. 64.
    Weinstock M (2005) The potential influence of maternal stress hormones on development and mental health of the offspring. Brain Behav Immun 19:296–308PubMedGoogle Scholar
  65. 65.
    Szuran TF, Pliska V, Pokorny J et al (2000) Prenatal stress in rats: effects on plasma corticosterone, hippocampal glucocorticoid receptors, and maze performance. Physiol Behav 71:353–362PubMedGoogle Scholar
  66. 66.
    Weinstock M, Matlina E, Maor GI et al (1992) Prenatal stress selectively alters the reactivity of the hypothalamic-pituitary adrenal system in the female rat. Brain Res 595:195–200PubMedGoogle Scholar
  67. 67.
    Koehl M, Darnaudery M, Dulluc J et al (1999) Prenatal stress alters circadian activity of hypothalamo-pituitary-adrenal axis and hippocampal corticosteroid receptors in adult rats of both gender. J Neurobiol 40:302–315PubMedGoogle Scholar
  68. 68.
    Henry C, Kabbaj M, Simon H et al (1994) Prenatal stress increases the hypothalamo-pituitary-adrenal axis response in young and adult rats. J Neuroendocrinol 6:341–345PubMedGoogle Scholar
  69. 69.
    Richardson HN, Zorrilla EP, Mandyam CD et al (2006) Exposure to repetitive versus varied stress during prenatal development generates two distinct anxiogenic and neuroendocrine profiles in adulthood. Endocrinology 147:2506–2517PubMedGoogle Scholar
  70. 70.
    Smith JW, Seckl JR, Evans AT et al (2004) Gestational stress induces post-partum depression-like behaviour and alters maternal care in rats. Psychoneuroendocrinology 29:227–244PubMedGoogle Scholar
  71. 71.
    Vallee M, MacCari S, Dellu F et al (1999) Long-term effects of prenatal stress and postnatal handling on age-related glucocorticoid secretion and cognitive performance: a longitudinal study in the rat. Eur J Neurosci 11:2906–2916PubMedGoogle Scholar
  72. 72.
    McCormick CM, Smythe JW, Sharma S et al (1995) 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 84:55–61PubMedGoogle Scholar
  73. 73.
    Bakker JM, van den Dobbelsteen GP, Kroes H et al (1998) Long-term gender-specific effects of manipulation during pregnancy on immune and endocrine responsiveness in rat offspring. J Neuroimmunol 82:56–63PubMedGoogle Scholar
  74. 74.
    Liu L, Li A, Matthews SG (2001) Maternal glucocorticoid treatment programs HPA regulation in adult offspring: sex-specific effects. Am J Physiol Endocrinol Metab 280:E729–739PubMedGoogle Scholar
  75. 75.
    Barbazanges A, Piazza PV, Le Moal M et al (1996) Maternal glucocorticoid secretion mediates long-term effects of prenatal stress. J Neurosci 16:3943–3949PubMedGoogle Scholar
  76. 76.
    Bhatnagar S, Lee TM, Vining C (2005) Prenatal stress differentially affects habituation of corticosterone responses to repeated stress in adult male and female rats. Horm Behav 47:430–438PubMedGoogle Scholar
  77. 77.
    Deuschle M, Weber B, Colla M et al (1998) Effects of major depression, aging and gender upon calculated diurnal free plasma cortisol concentrations: a re-evaluation study. Stress 2:281–287PubMedGoogle Scholar
  78. 78.
    Wong ML, Kling MA, Munson PJ et al (2000) Pronounced and sustained central hypernoradrenergic function in major depression with melancholic features: relation to hypercortisolism and corticotropin-releasing hormone. Proc Natl Acad Sci USA 97:325–330PubMedGoogle Scholar
  79. 79.
    Burke HM, Davis MC, Otte C et al (2005) Depression and cortisol responses to psychological stress: a meta-analysis. Psychoneuroendocrinology 30:846–856PubMedGoogle Scholar
  80. 80.
    Holsboer-Trachsler E, Stohler R, Hatzinger M (1991) Repeated administration of the combined dexamethasone-human corticotropin releasing hormone stimulation test during treatment of depression. Psychiatry Res 38:163–171PubMedGoogle Scholar
  81. 81.
    Porsolt RD, Anton G, Blavet N et al (1978) Behavioural despair in rats: a new model sensitive to antidepressant treatments. Eur J Pharmacol 47:379–391PubMedGoogle Scholar
  82. 82.
    Borsini F, Meli A (1988) Is the forced swimming test a suitable model for revealing antidepressant activity? Psychopharmacology (Berl) 94:147–160Google Scholar
  83. 83.
    Morley-Fletcher S, Rea M, Maccari S et al (2003) Environmental enrichment during adolescence reverses the effects of prenatal stress on play behaviour and HPA axis reactivity in rats. Eur J Neurosci 18:3367–3374PubMedGoogle Scholar
  84. 84.
    Poltyrev T, Weinstock M (2004) Gender difference in the prevention of hyperanxiety in adult prenatally stressed rats by chronic treatment with amitriptyline. Psychopharmacology (Berl) 171:270–276Google Scholar
  85. 85.
    Willner P, Towell A, Sampson D et al (1987) Reduction of sucrose preference by chronic unpredictable mild stress, and its restoration by a tricyclic antidepressant. Psychopharmacology (Berl) 93:358–364Google Scholar
  86. 86.
    Papp M, Willner P, Muscat R (1993) Behavioural sensitization to a dopamine agonist is associated with reversal of stress-induced anhedonia. Psychopharmacology (Berl) 110:159–164Google Scholar
  87. 87.
    Wise RA, Rompre PP (1989) Brain dopamine and reward. Annu Rev Psychol 40:191–225PubMedGoogle Scholar
  88. 88.
    Nestler EJ, Carlezon WA Jr. (2006) The mesolimbic dopamine reward circuit in depression. Biol Psychiatry 59:1151–1159PubMedGoogle Scholar
  89. 89.
    Alonso SJ, Navarro E, Rodriguez M (1994) Permanent dopaminergic alterations in the n. accumbens after prenatal stress. Pharmacol Biochem Behav 49:353–358PubMedGoogle Scholar
  90. 90.
    Corbett BA, Mendoza S, Abdullah M et al (2006) Cortisol circadian rhythms and response to stress in children with autism. Psychoneuroendocrinology 31:59–68PubMedGoogle Scholar
  91. 91.
    Rimondini R, Agren G, Borjesson S et al (2003) Persistent behavioral and autonomic supersensitivity to stress following prenatal stress exposure in rats. Behav Brain Res 140:75–80PubMedGoogle Scholar
  92. 92.
    Vallee M, Mayo W, Dellu F et al (1997) Prenatal stress induces high anxiety and postnatal handling induces low anxiety in adult offspring: correlation with stress-induced corticosterone secretion. J Neurosci 17:2626–2636PubMedGoogle Scholar
  93. 93.
    Pellow S, File SE (1986) Anxiolytic and anxiogenic drug effects on exploratory activity in an elevated plus-maze: a novel test of anxiety in the rat. Pharmacol Biochem Behav 24:525–529PubMedGoogle Scholar
  94. 94.
    Bogoch Y, Biala YN, Linial M et al (2007) Anxiety induced by prenatal stress is associated with suppression of hippocampal genes involved in synaptic function. J Neurochem, available online Google Scholar
  95. 95.
    Zagron G, Weinstock M (2006) Maternal adrenal hormone secretion mediates behavioural alterations induced by prenatal stress in male and female rats. Behav Brain Res 175:323–328PubMedGoogle Scholar
  96. 96.
    Estanislau C, Morato S (2006) Behavior ontogeny in the elevated plus-maze: prenatal stress effects. Int J Dev Neurosci 24:255–262PubMedGoogle Scholar
  97. 97.
    Bayer SA, Altman J, Russo RJ et al (1993) Timetables of neurogenesis in the human brain based on experimentally determined patterns in the rat. Neurotoxicology 14:83–144PubMedGoogle Scholar
  98. 98.
    Salm AK, Pavelko M, Krouse EM et al (2004) Lateral amygdaloid nucleus expansion in adult rats is associated with exposure to prenatal stress. Brain Res Dev Brain Res 148:159–167PubMedGoogle Scholar
  99. 99.
    Miller SD, Mueller E, Gifford GW et al (1999) Prenatal stress-induced modifications of neuronal nitric oxide synthase in amygdala and medial preoptic area. Ann N Y Acad Sci 877:760–763PubMedGoogle Scholar
  100. 100.
    Kraszpulski M, Dickerson PA, Salm AK (2006) Prenatal stress affects the developmental trajectory of the rat amygdala. Stress 9:85–95PubMedCrossRefGoogle Scholar
  101. 101.
    Cratty MS, Ward HE, Johnson EA et al (1995) Prenatal stress increases corticotropin-releasing factor (CRF) content and release in rat amygdala minces. Brain Res 675:297–302PubMedGoogle Scholar
  102. 102.
    Ward HE, Johnson EA, Salm AK et al (2000) Effects of prenatal stress on defensive withdrawal behavior and corticotropin releasing factor systems in rat brain. Physiol Behav 70:359–366PubMedGoogle Scholar
  103. 103.
    Meunier J, Gue M, Recasens M et al (2004) Attenuation by a sigma1 (sigma1) receptor agonist of the learning and memory deficits induced by a prenatal restraint stress in juvenile rats. Br J Pharmacol 142:689–700PubMedGoogle Scholar
  104. 104.
    Cannizzaro C, Plescia F, Martire M et al (2006) Single, intense prenatal stress decreases emotionality and enhances learning performance in the adolescent rat offspring: interaction with a brief, daily maternal separation. Behav Brain Res 169:128–136PubMedGoogle Scholar
  105. 105.
    Fujioka T, Fujioka A, Tan N et al (2001) Mild prenatal stress enhances learning performance in the non-adopted rat offspring. Neuroscience 103:301–307PubMedGoogle Scholar
  106. 106.
    Kreider ML, Levin ED, Seidler FJ et al (2005) Gestational dexamethasone treatment elicits sex-dependent alterations in locomotor activity, reward-based memory and hippocampal cholinergic function in adolescent and adult rats. Neuropsychopharmacology 30:1617–1623PubMedGoogle Scholar
  107. 107.
    Andrade JP, Madeira MD, Paula-Barbosa MM (2000) Sexual dimorphism in the subiculum of the rat hippocampal formation. Brain Res 875:125–137PubMedGoogle Scholar
  108. 108.
    Liu HH, Payne HR, Wang B et al (2006) Gender differences in response of hippocampus to chronic glucocorticoid stress: role of glutamate receptors. J Neurosci Res 83:775–786PubMedGoogle Scholar
  109. 109.
    Zhu Z, Li X, Chen W et al (2004) Prenatal stress causes gender-dependent neuronal loss and oxidative stress in rat hippocampus. J Neurosci Res 78:837–844PubMedGoogle Scholar
  110. 110.
    Schmitz C, Rhodes ME, Bludau M et al (2002) Depression: reduced number of granule cells in the hippocampus of female, but not male, rats due to prenatal restraint stress. Mol Psychiatry 7:810–813PubMedGoogle Scholar
  111. 111.
    Herrenkohl LR (1979) Prenatal stress reduces fertility and fecundity in female offspring. Science 206:1097–1099PubMedGoogle Scholar
  112. 112.
    McEwen BS, Alves SE, Bulloch K et al (1997) Ovarian steroids and the brain: implications for cognition and aging. Neurology 48:S8–15PubMedGoogle Scholar
  113. 113.
    Galea LA, Spritzer MD, Barker JM et al (2006) Gonadal hormone modulation of hippocampal neurogenesis in the adult. Hippocampus 16:225–232PubMedGoogle Scholar
  114. 114.
    Dalley JW, Cardinal RN, Robbins TW (2004) Prefrontal executive and cognitive functions in rodents: neural and neurochemical substrates. Neurosci Biobehav Rev 28:771–784PubMedGoogle Scholar
  115. 115.
    Murmu MS, Salomon S, Biala Y et al (2006) Changes of spine density and dendritic complexity in the prefrontal cortex in offspring of mothers exposed to stress during pregnancy. Eur J Neurosci 24:1477–1487PubMedGoogle Scholar
  116. 116.
    Van den Hove DL, Lauder JM, Scheepens A et al (2006) Prenatal stress in the rat alters 5-HT1A receptor binding in the ventral hippocampus. Brain Res 1090:29–34PubMedGoogle Scholar
  117. 117.
    Barros VG, Berger MA, Martijena ID et al (2004) Early adoption modifies the effects of prenatal stress on dopamine and glutamate receptors in adult rat brain. J Neurosci Res 76:488–496PubMedGoogle Scholar
  118. 118.
    Berger MA, Barros VG, Sarchi MI et al (2002) Long-term effects of prenatal stress on dopamine and glutamate receptors in adult rat brain. Neurochem Res 27:1525–1533PubMedGoogle Scholar
  119. 119.
    Wakshlak A, Weinstock M (1990) Neonatal handling reverses behavioral abnormalities induced in rats by prenatal stress. Physiol Behav 48:289–292PubMedGoogle Scholar
  120. 120.
    Moore CL, Power KL (1986) Prenatal stress affects mother-infant interaction in Norway rats. Dev Psychobiol 19:235–245PubMedGoogle Scholar
  121. 121.
    Power KL, Moore CL (1986) Prenatal stress eliminates differential maternal attention to male offspring in Norway rats. Physiol Behav 38:667–671PubMedGoogle Scholar
  122. 122.
    Melniczek JR, Ward IL (1994) Patterns of ano-genital licking mother rats exhibit toward prenatally stressed neonates. Physiol Behav 56:457–461PubMedGoogle Scholar
  123. 123.
    Poltyrev T, Weinstock M (1999) Effect of gestational stress on maternal behavior in response to cage transfer and handling of pups in two strains of rat. Stress 3:85–95PubMedGoogle Scholar
  124. 124.
    Meek LR, Dittel PL, Sheehan MC et al (2001) Effects of stress during pregnancy on maternal behavior in mice. Physiol Behav 72:473–479PubMedGoogle Scholar
  125. 125.
    Maccari S, Piazza PV, Kabbaj M et al (1995) Adoption reverses the long-term impairment in glucocorticoid feedback induced by prenatal stress. J Neurosci 15:110–116PubMedGoogle Scholar
  126. 126.
    Pfister HP, Muir JL (1989) Psychological stress and administered oxytocin during pregnancy: effect corticosterone and prolactin response in lactating rats. Int J Neurosci 45:91–99PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2007

Authors and Affiliations

  1. 1.Department of PharmacologyHebrew University Medical CentreEin Kerem, JerusalemIsrael

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