Gender Differences in the Effects of Prenatal Stress on Brain Development and Behaviour
Tóm tắt
Từ khóa
Tài liệu tham khảo
Beversdorf DQ, Manning SE, Hillier A et al (2005) Timing of prenatal stressors and autism. J Autism Dev Disord 35:471–478
van Os J, Selten JP (1998) Prenatal exposure to maternal stress and subsequent schizophrenia. The May 1940 invasion of The Netherlands. Br J Psychiatry 172:324–326
Weinstock M (2001) Alterations induced by gestational stress in brain morphology and behaviour of the offspring. Prog Neurobiol 65:427–451
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 17:1848–1859
Wust S, Entringer S, Federenko IS et al (2005) Birth weight is associated with salivary cortisol responses to psychosocial stress in adult life. Psychoneuroendocrinology 30:591–598
Taylor DC (1969) Differential rates of cerebral maturation between sexes and between hemispheres. Evidence from epilepsy. Lancet 2:140–142
Watson JB, Mednick SA, Huttunen M et al (1999) Prenatal teratogens and the development of adult mental illness. Dev Psychopathol 11:457–466
Sandman CA, Wadhwa PD, Chicz-DeMet A et al (1999) Maternal corticotropin-releasing hormone and habituation in the human fetus. Dev Psychobiol 34:163–173
Inder WJ, Prickett TC, Ellis MJ et al (2001) The utility of plasma CRH as a predictor of preterm delivery. J Clin Endocrinol Metab 86:5706–5710
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 30:482–491
Holst K, Andersen E, Philip J et al (1989) Antenatal and perinatal conditions correlated to handicap among 4-year-old children. Am J Perinatol 6:258–267
Fride E, Dan Y, Feldon J et al (1986) Effects of prenatal stress on vulnerability to stress in prepubertal and adult rats. Physiol Behav 37:681–687
Schneider ML (1992) Prenatal stress exposure alters postnatal behavioral expression under conditions of novelty challenge in rhesus monkey infants. Dev Psychobiol 25:529–540
Takahashi LK, Haglin C, Kalin NH (1992) Prenatal stress potentiates stress-induced behavior and reduces the propensity to play in juvenile rats. Physiol Behav 51:319–323
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 50:511–517
Secoli SR, Teixeira NA (1998) Chronic prenatal stress affects development and behavioral depression in rats. Stress 2:273–280
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 97:11032–11037
Yang J, Han H, Cao J et al (2006) Prenatal stress modifies hippocampal synaptic plasticity and spatial learning in young rat offspring. Hippocampus 16:431–436
Burton C, Lovic V, Fleming AS (2006) Early adversity alters attention and locomotion in adult sprague-dawley rats. Behav Neurosci 120:665–675
MacLusky NJ, Naftolin F (1981) Sexual differentiation of the central nervous system. Science 211:1294–1302
Matsumoto A (1991) Synaptogenic action of sex steroids in developing and adult neuroendocrine brain. Psychoneuroendocrinology 16:25–40
McEwen BS, Lieberburg I, Chaptal C et al (1977) Aromatization: important for sexual differentiation of the neonatal rat brain. Horm Behav 9:249–263
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 101:841–848
Palanza P (2001) Animal models of anxiety and depression: how are females different? Neurosci Biobehav Rev 25:219–233
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 81:1–13
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 16:395–398
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 148:333–346
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 734:10–18
Jones HE, Ruscio MA, Keyser LA et al (1997) Prenatal stress alters the size of the rostral anterior commissure in rats. Brain Res Bull 42:341–346
Valenstein ES, Kakolewski JW, Cox VC (1967) Sex differences in taste preference for glucose and saccharin solutions. Science 156:942–943
Bowman RE, MacLusky NJ, Sarmiento Y et al (2004) Sexually dimorphic effects of prenatal stress on cognition, hormonal responses, and central neurotransmitters. Endocrinology 145:3778–3787
Fride E, Weinstock M (1988) Prenatal stress increases anxiety related behavior and alters cerebral lateralization of dopamine activity. Life Sci 42:1059–1065
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 19:37–45
Frye CA, Wawrzycki J (2003) Effect of prenatal stress and gonadal hormone condition on depressive behaviors of female and male rats. Horm Behav 44:319–326
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 74:435–440
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 218:177–180
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 36:2103–2109
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 114:1635–1644
Ward IL (1972) Prenatal stress feminizes and demasculinizes the behavior of males. Science 175:82–84
Weisz J, Brown BL, Ward IL (1982) Maternal stress decreases steroid aromatase activity in brains of male and female rat fetuses. Neuroendocrinology 35:374–379
Reznikov AG, Nosenko ND, Tarasenko LV (1999) Prenatal stress and glucocorticoid effects on the developing gender-related brain. J Steroid Biochem Mol Biol 69:109–115
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 50:193–199
Reznikov AG, Nosenko ND (1995) Catecholamines in steroid-dependent brain development. J Steroid Biochem Mol Biol 53:349–353
Ward IL, Stehm KE (1991) Prenatal stress feminizes juvenile play patterns in male rats. Physiol Behav 50:601–605
Masterpasqua F, Chapman RH, Lore RK (1976) The effects of prenatal psychological stress on the sexual behavior and reactivity of male rats. Dev Psychobiol 9:403–411
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 12:172–178
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 24:291–297
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 30:388–396
Rojo M, Marin B, Menendez-Patterson A (1985) Effects of low stress during pregnancy on certain parameters of the offspring. Physiol Behav 34:895–899
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 17:393–401
Keshet GI, Weinstock M (1995) Maternal naltrexone prevents morphological and behavioral alterations induced in rats by prenatal stress. Pharmacol Biochem Behav 50:413–419
Ward OB, Monaghan EP, Ward IL (1986) Naltrexone blocks the effects of prenatal stress on sexual behavior differentiation in male rats. Pharmacol Biochem Behav 25:573–576
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 23:571–581
Weinstock M, Fride E, Hertzberg R (1988) Prenatal stress effects on functional development of the offspring. Prog Brain Res 73:319–331
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 82:268–274
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 57:1133–1147
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 92:1079–1088
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 118:409–415
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 98:123–129
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 43:783–787
Maccari S, Darnaudery M, Morley-Fletcher S et al (2003) Prenatal stress and long-term consequences: implications of glucocorticoid hormones. Neurosci Biobehav Rev 27:119–127
Weinstock M (2005) The potential influence of maternal stress hormones on development and mental health of the offspring. Brain Behav Immun 19:296–308
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 71:353–362
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 595:195–200
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 40:302–315
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 6:341–345
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 147:2506–2517
Smith JW, Seckl JR, Evans AT et al (2004) Gestational stress induces post-partum depression-like behaviour and alters maternal care in rats. Psychoneuroendocrinology 29:227–244
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 11:2906–2916
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 84:55–61
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 82:56–63
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:E729–739
Barbazanges A, Piazza PV, Le Moal M et al (1996) Maternal glucocorticoid secretion mediates long-term effects of prenatal stress. J Neurosci 16:3943–3949
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 47:430–438
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 2:281–287
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 97:325–330
Burke HM, Davis MC, Otte C et al (2005) Depression and cortisol responses to psychological stress: a meta-analysis. Psychoneuroendocrinology 30:846–856
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 38:163–171
Porsolt RD, Anton G, Blavet N et al (1978) Behavioural despair in rats: a new model sensitive to antidepressant treatments. Eur J Pharmacol 47:379–391
Borsini F, Meli A (1988) Is the forced swimming test a suitable model for revealing antidepressant activity? Psychopharmacology (Berl) 94:147–160
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 18:3367–3374
Poltyrev T, Weinstock M (2004) Gender difference in the prevention of hyperanxiety in adult prenatally stressed rats by chronic treatment with amitriptyline. Psychopharmacology (Berl) 171:270–276
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) 93:358–364
Papp M, Willner P, Muscat R (1993) Behavioural sensitization to a dopamine agonist is associated with reversal of stress-induced anhedonia. Psychopharmacology (Berl) 110:159–164
Nestler EJ, Carlezon WA Jr. (2006) The mesolimbic dopamine reward circuit in depression. Biol Psychiatry 59:1151–1159
Alonso SJ, Navarro E, Rodriguez M (1994) Permanent dopaminergic alterations in the n. accumbens after prenatal stress. Pharmacol Biochem Behav 49:353–358
Corbett BA, Mendoza S, Abdullah M et al (2006) Cortisol circadian rhythms and response to stress in children with autism. Psychoneuroendocrinology 31:59–68
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 140:75–80
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 17:2626–2636
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 24:525–529
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
Zagron G, Weinstock M (2006) Maternal adrenal hormone secretion mediates behavioural alterations induced by prenatal stress in male and female rats. Behav Brain Res 175:323–328
Estanislau C, Morato S (2006) Behavior ontogeny in the elevated plus-maze: prenatal stress effects. Int J Dev Neurosci 24:255–262
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 14:83–144
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 148:159–167
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 877:760–763
Kraszpulski M, Dickerson PA, Salm AK (2006) Prenatal stress affects the developmental trajectory of the rat amygdala. Stress 9:85–95
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 675:297–302
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 70:359–366
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 142:689–700
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 169:128–136
Fujioka T, Fujioka A, Tan N et al (2001) Mild prenatal stress enhances learning performance in the non-adopted rat offspring. Neuroscience 103:301–307
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 30:1617–1623
Andrade JP, Madeira MD, Paula-Barbosa MM (2000) Sexual dimorphism in the subiculum of the rat hippocampal formation. Brain Res 875:125–137
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 83:775–786
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 78:837–844
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 7:810–813
Herrenkohl LR (1979) Prenatal stress reduces fertility and fecundity in female offspring. Science 206:1097–1099
McEwen BS, Alves SE, Bulloch K et al (1997) Ovarian steroids and the brain: implications for cognition and aging. Neurology 48:S8–15
Galea LA, Spritzer MD, Barker JM et al (2006) Gonadal hormone modulation of hippocampal neurogenesis in the adult. Hippocampus 16:225–232
Dalley JW, Cardinal RN, Robbins TW (2004) Prefrontal executive and cognitive functions in rodents: neural and neurochemical substrates. Neurosci Biobehav Rev 28:771–784
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 24:1477–1487
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 1090:29–34
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 76:488–496
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 27:1525–1533
Wakshlak A, Weinstock M (1990) Neonatal handling reverses behavioral abnormalities induced in rats by prenatal stress. Physiol Behav 48:289–292
Moore CL, Power KL (1986) Prenatal stress affects mother-infant interaction in Norway rats. Dev Psychobiol 19:235–245
Power KL, Moore CL (1986) Prenatal stress eliminates differential maternal attention to male offspring in Norway rats. Physiol Behav 38:667–671
Melniczek JR, Ward IL (1994) Patterns of ano-genital licking mother rats exhibit toward prenatally stressed neonates. Physiol Behav 56:457–461
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 3:85–95
Meek LR, Dittel PL, Sheehan MC et al (2001) Effects of stress during pregnancy on maternal behavior in mice. Physiol Behav 72:473–479
Maccari S, Piazza PV, Kabbaj M et al (1995) Adoption reverses the long-term impairment in glucocorticoid feedback induced by prenatal stress. J Neurosci 15:110–116