Sex-dependent changes induced by prenatal stress in cortical and hippocampal morphology and behaviour in rats: An update

Stress

Volumn 14, Issue 6, 2011, Pages 604-613

  Weinstock, M ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

Anxiety; Corticosterone; Dendritic morphology; Hippocampal formation; Learning deficits; Neurogenesis

Indexed keywords

AROMATASE; CORTICOSTERONE; TESTOSTERONE;

ADRENALECTOMY; ANIMAL BEHAVIOR; ANXIETY; BEHAVIOR CHANGE; BRAIN CORTEX; CELL STRUCTURE; COGNITIVE DEFECT; DENDRITE; ENZYME ACTIVITY; HIPPOCAMPUS; HUMAN; LEARNING DISORDER; LIMBIC SYSTEM; MORPHOLOGY; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PREFRONTAL CORTEX; PRENATAL STRESS; PRIORITY JOURNAL; REVIEW; SEX DIFFERENCE; SEX TRANSFORMATION;

ANIMALS; ANXIETY; AROMATASE; BEHAVIOR, ANIMAL; BRAIN; CHILD; CHILD, PRESCHOOL; COGNITION DISORDERS; CORTICOSTERONE; DENDRITES; FEMALE; HIPPOCAMPUS; HUMANS; MALE; MAZE LEARNING; MEMORY DISORDERS; PREFRONTAL CORTEX; PREGNANCY; PREGNANCY TRIMESTER, SECOND; PRENATAL EXPOSURE DELAYED EFFECTS; RATS; SEX CHARACTERISTICS; STRESS, PSYCHOLOGICAL; TESTOSTERONE;

EID: 80054086064     PISSN: 10253890     EISSN: 16078888     Source Type: Journal    
DOI: 10.3109/10253890.2011.588294     Document Type: Review

References (109)

1. Abrous DN, Koehl M,Le MoalM. 2005. Adult neurogenesis:From precursors to network and physiology. Physiol Rev 85:523-569. (Pubitemid 40404636)
2. Andrade JP, Madeira MD, Paula-Barbosa MM. 2000. Sexual dimorphism in the subiculum of the rat hippocampal formation. Brain Res 875:125-137.
3. Archer JE, Blackman DE. 1971. Prenatal psychological stress and offspring behavior in rats and mice. Dev Psychobiol 4:193-248.
4. Barbazanges A, Piazza PV, Le Moal M, Maccari S. 1996. Maternal glucocorticoid secretion mediates long-term effects of prenatal stress. J Neurosci 16:3943-3949. (Pubitemid 26176058)
5. Barros VG, Rodriguez P, Martijena ID, Perez A, Molina VA, Antonelli MC. 2006. Prenatal stress and early adoption effects on benzodiazepine receptors and anxiogenic behavior in the adult rat brain. Synapse 60:609-618. (Pubitemid 44658267)
6. Bayer SA, Altman J, Russo RJ, Zhang X. 1993. Timetables of neurogenesis in the human brain based on experimentally determined patterns in the rat. Neurotoxicology 14:83-144. (Pubitemid 23195769)
7. Beijers R, Jansen J, Riksen-Walraven M, de Weerth C. 2010. Maternal prenatal anxiety and stress predict infant illnesses and health complaints. Pediatrics 126:e401-e409.
8. Beversdorf DQ, Manning SE, Hillier A, Anderson SL, Nordgren RE, Walters SE, Nagaraja HN, Cooley WC, Gaelic SE, Bauman ML. 2005. Timing of prenatal stressors and autism. J Autism Dev Disord 35:471-478. (Pubitemid 41216433)
9. Biala YN, Bogoch Y, Bejar C, Linial M, Weinstock M. 2010. Prenatal stress diminishes gender differences in behavior and in expression of hippocampal synaptic genes and proteins in rats Hippocampus (available online).
10. Bliss TV, Collingridge GL. 1993. A synaptic model of memory:Long-term potentiation in the hippocampus. Nature 361:31-39. (Pubitemid 23020772)
11. Blokland A, Rutten K, Prickaerts J. 2006. Analysis of spatial orientation strategies of male and female Wistar rats in a Morris water escape task. Behav Brain Res 171:216-224. (Pubitemid 43946493)
12. Bogoch Y, Biala YN, Linial M, Weinstock M. 2007. Anxiety induced by prenatal stress is associated with suppression of hippocampal genes involved in synaptic function. J Neurochem 101:1018-1030. (Pubitemid 46683862)
13. Bosch OJ, Musch W, Bredewold R, Slattery DA, Neumann ID. 2007. Prenatal stress increases HPA axis activity and impairs maternal care in lactating female offspring:Implications for postpartum mood disorder. Psychoneuroendocrinology 32:267-278. (Pubitemid 46400279)
14. Bourne JN, Harris KM. 2008. Balancing structure and function at hippocampal dendritic spines. Annu Rev Neurosci 31:47-67.
15. Bowman RE, MacLusky NJ, Sarmiento Y, Frankfurt M,Gordon M, Luine VN. 2004. Sexually dimorphic effects of prenatal stress on cognition, hormonal responses, and central neurotransmitters. Endocrinology 145:3778-3787. (Pubitemid 39037565)
16. Brunton PJ, Russell JA. 2010. Prenatal social stress in the rat programmes neuroendocrine and behavioural responses to stress in the adult offspring:Sex-specific effects. J Neuroendocrinol 22:258-271.
17. Buss C, Davis EP, Muftuler LT, Head K, Sandman CA. 2010. High pregnancy anxiety during mid-gestation is associated with decreased gray matter density in 6-9-year-old children. Psychoneuroendocrinology 35:141-153.
18. Charil A, Laplante DP, Vaillancourt C, King S. 2010. Prenatal stress and brain development. Brain Res Rev 65:56-79.
19. Coe CL, Kramer M, Czeh B, Gould E, Reeves AJ, Kirschbaum C, Fuchs E. 2003. Prenatal stress diminishes neurogenesis in the dentate gyrus of juvenile rhesus monkeys. Biol Psychiatry 54:1025-1034. (Pubitemid 37415037)
20. Davis EP, Sandman CA. 2010. The timing of prenatal exposure to maternal cortisol and psychosocial stress is associated with human infant cognitive development. Child Dev 81:131-148.
21. de Bruijn AT, van Bakel HJ, van Baar AL. 2009. Sex differences in the relation between prenatal maternal emotional complaints and child outcome. Early Hum Dev 85:319-324.
22. de Bruin JP, Moita MP, de Brabander HM, Joosten RN. 2001. Place and response learning of rats in a Morris water maze:Differential effects of fimbria fornix and medial prefrontal cortex lesions. Neurobiol Learn Mem 75:164-178. (Pubitemid 34127517)
23. Diaz R, Brown RW, Seckl JR. 1998. Distinct ontogeny of glucocorticoid and mineralocorticoid receptor and 11beta-hydroxysteroid dehydrogenase types I and II mRNAs in the fetal rat brain suggest a complex control of glucocorticoid actions. J Neurosci 18:2570-2580.
24. DiPietro JA, Novak MF, Costigan KA, Atella LD, Reusing SP. 2006. Maternal psychological distress during pregnancy in relation to child development at age two. Child Dev 77:573-587. (Pubitemid 43736535)
25. Fride E, Weinstock M. 1988. Prenatal stress increases anxiety related behavior and alters cerebral lateralization of dopamine activity. Life Sci 42:1059-1065. (Pubitemid 18056843)
26. Fujioka A, Fujioka T, Ishida Y, Maekawa T, Nakamura S. 2006. Differential effects of prenatal stress on the morphological maturation of hippocampal neurons. Neuroscience 141:907-915. (Pubitemid 44066657)
27. Garcia-Falgueras A, Pinos H, Collado P, Pasaro E, Fernandez R, Segovia S, Guillamon A. 2005. The expression of brain sexual dimorphism in artificial selection of rat strains. Brain Res 1052:130-138. (Pubitemid 41116770)
28. Gerardin DC, Pereira OC, Kempinas WG, Florio JC, Moreira EG, Bernardi MM. 2005. Sexual behavior, neuroendocrine, and neurochemical aspects in male rats exposed prenatally to stress. Physiol Behav 84:97-104. (Pubitemid 40092070)
29. Gould E, Westlind-Danielsson A, Frankfurt M, McEwen BS. 1990. Sex differences and thyroid hormone sensitivity of hippocampal pyramidal cells. J Neurosci 10:996-1003. (Pubitemid 20104795)
30. Gregory E. 1975. Comparison of postnatal CNS development between male and female rats. Brain Res 99:152-156.
31. Grizenko N, Shayan YR, Polotskaia A, Ter-Stepanian M, Joober R. 2008. Relation of maternal stress during pregnancy to symptom severity and response to treatment in children with ADHD. J Psychiatry Neurosci 33:10-16. (Pubitemid 351252491)
32. Hosseini-Sharifabad M, Hadinedoushan H. 2007. Prenatal stress induces learning deficits and is associated with a decrease in granules and CA3 cell dendritic tree size in rat hippocampus. Anat Sci Int 82:211-217. (Pubitemid 350090515)
33. Jia N, Yang K, Sun Q, Cai Q, Li H, Cheng D, Fan X, Zhu Z. 2010. Prenatal stress causes dendritic atrophy of pyramidal neurons in hippocampal CA3 region by glutamate in offspring rats. Dev Neurobiol 70:114-125.
34. Johnston AL, File SE. 1991. Sex differences in animal tests of anxiety. Physiol Behav 49:245-250.
35. Juraska JM, Fitch JM, Henderson C, Rivers N. 1985. Sex differences in the dendritic branching of dentate granule cells following differential experience. Brain Res 333:73-80. (Pubitemid 15124350)
36. Kanit L, Taskiran D, Yilmaz OA, Balkan B, Demirgoren S, Furedy JJ, Pogun S. 2000. Sexually dimorphic cognitive style in rats emerges after puberty. Brain Res Bull 52:243-248. (Pubitemid 30365026)
37. Khashan AS, Abel KM, McNamee R, Pedersen MG, Webb RT, Baker PN, Kenny LC, Mortensen PB. 2008. Higher risk of offspring schizophrenia following antenatal maternal exposure to severe adverse life events. Arch Gen Psychiatry 65:146-152. (Pubitemid 351214313)
38. Kim HW, Cho SC, Kim BN, Kim JW, Shin MS, Kim Y. 2009. Perinatal and familial risk factors are associated with full syndrome and subthreshold attention-deficit hyperactivity disorder in a korean community sample. Psychiatry Investig 6:278-285.
39. King S, Laplante DP. 2005. The effects of prenatal maternal stress on children's cognitive development:Project Ice Storm. Stress 8:35-45. (Pubitemid 40776471)
40. Kinney DK, Miller AM, Crowley DJ, Huang E, Gerber E. 2008. Autism prevalence following prenatal exposure to hurricanes and tropical storms in Louisiana. J Autism Dev Disord 38:481-488. (Pubitemid 351322368)
41. Kofman O. 2002. The role of prenatal stress in the etiology of developmental behavioural disorders. Neurosci Biobehav Rev 26:457-470. (Pubitemid 36163348)
42. Konkle AT, McCarthy MM. 2010. Developmental time course of estradiol, testosterone, and dihydrotestosterone levels in discrete regions of male and female rat brain. Endocrinology 152(1):223-235.
43. Laplante DP, Brunet A, Schmitz N, Ciampi A, King S. 2008. Project Ice Storm:Prenatal maternal stress affects cognitive and linguistic functioning in 5 1/2-year-old children. J Am Acad Child Adolesc Psychiatry 47:1063-1072.
44. Lazinski MJ, Shea AK, Steiner M. 2008. Effects of maternal prenatal stress on offspring development:A commentary. Arch Womens Ment Health 11:363-375.
45. Lemaire V, Lamarque S, Le Moal M, Piazza PV, Abrous DN. 2006. Postnatal stimulation of the pups counteracts prenatal stress-induced deficits in hippocampal neurogenesis. Biol Psychiatry 59:786-792.
46. Li J, Olsen J, Vestergaard M, Obel C. 2010. Attention-deficit/ hyperactivity disorder in the offspring following prenatal maternal bereavement:A nationwide follow-up study in Denmark. Eur Child Adolesc Psychiatry 19:747-753.
47. Maccari S, Piazza PV, Kabbaj M, Barbazanges A, Simon H, Le Moal M. 1995. Adoption reverses the long-term impairment in glucocorticoid feedback induced by prenatal stress. J Neurosci 15:110-116.
48. Maccari S, Darnaudery M, Morley-Fletcher S, Zuena AR, Cinque C, Van Reeth O. 2003. Prenatal stress and long-term consequences:Implications of glucocorticoid hormones. Neurosci Biobehav Rev 27:119-127. (Pubitemid 36535394)
49. Madeira MD, Lieberman AR. 1995. Sexual dimorphism in the mammalian limbic system. Prog Neurobiol 45:275-333.
50. Mandyam CD, Crawford EF, Eisch AJ, Rivier CL, Richardson HN. 2008. Stress experienced in utero reduces sexual dichotomies in neurogenesis, microenvironment, and cell death in the adult rat hippocampus. Dev Neurobiol 68:575-589. (Pubitemid 351466289)
51. Markham JA, Koenig JI. 2011. Prenatal stress:Role in psychotic and depressive diseases. Psychopharmacology (Berl) 214(1):89-106.
52. Martinez-Tellez RI, Hernandez-Torres E, Gamboa C, Flores G. 2009. Prenatal stress alters spine density and dendritic length of nucleus accumbens and hippocampus neurons in rat offspring. Synapse 63:794-804.
53. Martini J, Knappe S, Beesdo-Baum K, Lieb R, Wittchen HU. 2010. Anxiety disorders before birth and self-perceived distress during pregnancy:Associations with maternal depression and obstetric, neonatal and early childhood outcomes. Early Hum Dev 86:305-310.
54. McCormick CM, Smythe JW, Sharma S, Meaney MJ. 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.
55. McGivern RF, Poland RE, Taylor AN, Branch BJ, Raum WJ. 1986. Prenatal stress feminizes adult male saccharin preference and maze learning:Antagonism by propranolol. Monogr Neural Sci 12:172-178.
56. Mennes M, Stiers P, Lagae L, Van den Bergh B. 2006. Long-term cognitive sequelae of antenatal maternal anxiety:Involvement of the orbitofrontal cortex. Neurosci Biobehav Rev 30:1078-1086. (Pubitemid 44855150)
57. Meunier J, Gue M, Recasens M, Maurice T. 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. (Pubitemid 38969664)
58. Meyer G, Ferres-Torres R, MasM.1978. The effects ofpubertyand castration on hippocampal dendritic spines of mice. A Golgi study. Brain Res 155:108-112. (Pubitemid 8404616)
59. Michelsen KA, van den Hove DL, Schmitz C, Segers O, Prickaerts J, Steinbusch HW. 2007. Prenatal stress and subsequent exposure to chronic mild stress influence dendritic spine density and morphology in the rat medial prefrontal cortex. BMC Neurosci 8:107.
60. Munoz-Cueto JA, Garcia-Segura LM, Ruiz-Marcos A. 1990. Developmental sex differences and effect of ovariectomy on the number of cortical pyramidal cell dendritic spines. Brain Res 515:64-68. (Pubitemid 20176096)
61. Murmu MS, Salomon S, Biala Y, Weinstock M, Braun K, Bock J. 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. (Pubitemid 44401670)
62. Nagano M, Ozawa H, Suzuki H. 2008. Prenatal dexamethasone exposure affects anxiety-like behaviour and neuroendocrine systems in an age-dependent manner. Neurosci Res 60:364-371.
63. Newhouse P, Newhouse C, Astur RS. 2007. Sex differences in visual-spatial learning using a virtual water maze in pre-pubertal children. Behav Brain Res 183:1-7. (Pubitemid 47259521)
64. Odagiri K, Abe H, Kawagoe C, Takeda R, Ikeda T, Matsuo H, Nonaka H, Ebihara K, Nishimori T, Ishizuka Y, Hashiguchi H, Ishida Y. 2008. Psychological prenatal stress reduced the number of BrdU immunopositive cells in the dorsal hippocampus without affecting the open field behavior of male and female rats at one month of age. Neurosci Lett 446:25-29.
65. Oomen CA, Girardi CE, Cahyadi R, Verbeek EC, Krugers H, Joels M, Lucassen PJ. 2009. Opposite effects of early maternal deprivation on neurogenesis in male versus female rats. PLoS One 4:e3675.
66. Perfilieva E, Risedal A, Nyberg J, Johansson BB, Eriksson PS. 2001. Gender and strain influence on neurogenesis in dentate gyrus of young rats. J Cereb Blood Flow Metab 21:211-217. (Pubitemid 32207420)
67. Pfister HP, Muir JL. 1989. Psychological stress and administered oxytocin during pregnancy:Effect corticosterone and prolactin response in lactating rats. Int J Neurosci 45:91-99.
68. Poltyrev T, Gorodetsky E, Bejar C, Schorer-Apelbaum D, Weinstock M. 2005. Effect of chronic treatment with ladostigil (TV-3326) on anxiogenic and depressive-like behaviour and on activity of the hypothalamic-pituitary-adrenal axis in male and female prenatally stressed rats. Psychopharmacology (Berl) 181:118-125. (Pubitemid 41440922)
69. Rice D, Barone S, Jr. 2000. Critical periods of vulnerability for the developing nervous system:Evidence from humans and animal models. Environ Health Perspect 108(Suppl 3):511-533. (Pubitemid 30466179)
70. Richardson HN, Zorrilla EP, Mandyam CD, Rivier CL. 2006. Exposure to repetitive versus varied stress during prenatal development generates two distinct anxiogenic and neuroendo-crine profiles in adulthood. Endocrinology 147:2506-2517.
71. Rodriguez A, Bohlin G. 2005. Are maternal smoking and stress during pregnancy related to ADHD symptoms in children? J Child Psychol Psychiatry 46:246-254. (Pubitemid 40439430)
72. Rodriguez N, Mayer N, Gauna HF. 2007. Effects of prenatal stress on male offspring sexual maturity. Biocell 31:67-74. (Pubitemid 46797821)
73. Sakuma Y. 2009. Gonadal steroid action and brain sex differentiation in the rat. J Neuroendocrinol 21:410-414.
74. Salehi B, Cordero MI, Sandi C. 2010. Learning under stress:The inverted-U-shape function revisited. Learn Mem 17:522-530.
75. Salomon S, Bejar C, Schorer-Apelbaum D, Weinstock M. 2011. Corticosterone mediates some but not other behavioural changes induced by prenatal stress in rats. J Neuroendocrinol 23:118-128.
76. Sandstrom NJ, Kaufman J, Huettel SA. 1998. Males and females use different distal cues in a virtual environment navigation task. Brain Res Cogn Brain Res 6:351-360. (Pubitemid 28247562)
77. Seckl JR. 2008. Glucocorticoids, developmental "programming" and the risk of affective dysfunction. Prog Brain Res 167:17-34. (Pubitemid 350123222)
78. Segal M. 2005. Dendritic spines and long-term plasticity. Nat Rev Neurosci 6:277-284. (Pubitemid 40469982)
79. Segal M. 2010. Dendritic spines, synaptic plasticity and neuronal survival:Activity shapes dendritic spines to enhance neuronal viability. Eur J Neurosci 31:2178-2184.
80. Son GH, Geum D, Chung S, Kim EJ, Jo JH, Kim CM, Lee KH, Kim H, Choi S, Kim HT, Lee CJ, Kim K. 2006. Maternal stress produces learning deficits associated with impairment of NMDA receptor-mediated synaptic plasticity. J Neurosci 26:3309-3318.
81. Stewart PM, Murry BA, Mason JI. 1994. Type 2 11 beta-hydroxysteroid dehydrogenase in human fetal tissues. J Clin Endocrinol Metab 78:1529-1532.
82. Szuran TF, Pliska V, Pokorny J, Welzl H. 2000. Prenatal stress in rats:Effects on plasma corticosterone, hippocampal glucocorti-coid receptors, and maze performance. Physiol Behav 71:353-362. (Pubitemid 32058841)
83. Takahashi LK, Turner JG, Kalin NH. 1998. Prolonged stress-induced elevation in plasma corticosterone during pregnancy in the rat:Implications for prenatal stress studies. Psychoneur-oendocrinology 23:571-581. (Pubitemid 28459555)
84. Talge NM, Neal C, Glover V. 2007. Antenatal maternal stress and long-term effects on child neurodevelopment:How and why? J Child Psychol Psychiatry 48:245-261. (Pubitemid 46372120)
85. Thorup A, Petersen L, Jeppesen P, Ohlenschlaeger J, Christensen T, Krarup G, Jorgensen P, Nordentoft M. 2007. Gender differences in young adults with first-episode schizophrenia spectrum disorders at baseline in the Danish OPUS study. J Nerv Ment Dis 195:396-405. (Pubitemid 46763241)
86. Van den Bergh BR, Marcoen A. 2004. High antenatal maternal anxiety is related to ADHD symptoms, externalizing problems, and anxiety in 8-and 9-year-olds. Child Dev 75:1085-1097. (Pubitemid 39137756)
87. Van den Bergh BR, Mennes M, Oosterlaan J, Stevens V, Stiers P, Lagae MA. 2005. High antenatal maternal anxiety is related to impulsivity during performance on cognitive tasks in 14-and 15-year-olds. Neurosci Biobehav Revs 29:259-269. (Pubitemid 40461743)
88. Van den Bergh BR, Van Calster B, Smits T, Van Huffel S, Lagae L. 2008. Antenatal maternal anxiety is related to HPA-axis dysregulation and self-reported depressive symptoms in adolescence:A prospective study on the fetal origins of depressed mood. Neuropsychopharmacology 33:536-545.
89. Van Lieshout RJ, Boylan K. 2010. Increased depressive symptoms in female but not male adolescents born at low birth weight in the offspring of a national cohort. Can J Psychiatry 55:422-430.
90. Wakshlak A, Weinstock M. 1990. Neonatal handling reverses behavioral abnormalities induced in rats by prenatal stress. Physiol Behav 48:289-292. (Pubitemid 20270242)
91. Ward IL. 1972. Prenatal stress feminizes and demasculinizes the behavior of males. Science 175:82-84.
92. 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. (Pubitemid 14140314)
93. Warren SG, Humphreys AG, Juraska JM, Greenough WT. 1995. LTP varies across the estrous cycle:Enhanced synaptic plasticity in proestrus rats. Brain Res 703:26-30.
94. Weinstock M. 1997. Does prenatal stress impair coping and regulation of hypothalamic-pituitary-adrenal axis? Neurosci Biobehav Rev 21:1-10. (Pubitemid 27044546)
95. Weinstock M. 2001. Alterations induced by gestational stress in brain morphology and behaviour of the offspring. Prog Neurobiol 65:427-451. (Pubitemid 33016408)
96. Weinstock M. 2007. Gender differences in the effects of prenatal stress on brain development and behaviour. Neurochem Res 32:1730-1740. (Pubitemid 47428852)
97. Weinstock M. 2008. The long-term behavioural consequences of prenatal stress. Neurosci Biobehav Rev 32:1073-1086.
98. Weinstock M, Matlina E, Maor GI, Rosen H, McEwen BS. 1992. Prenatal stress selectively alters the reactivity of the hypothala-mic-pituitary adrenal system in the female rat. Brain Res 595:195-200.
99. 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. (Pubitemid 12033897)
100. Westenbroek C, Den Boer JA, Veenhuis M, Ter Horst GJ. 2004. Chronic stress and social housing differentially affect neurogen-esis in male and female rats. Brain Res Bull 64:303-308. (Pubitemid 39550765)
101. Wimer CC, Wimer RE. 1989. On the sources of strain and sex differences in granule cell number in the dentate area of house mice. Brain Res Dev Brain Res 48:167-176. (Pubitemid 19195788)
102. Woolley CS, McEwen BS. 1992. Estradiol mediates fluctuation in hippocampal synapse density during the estrous cycle in the adult rat. J Neurosci 12:2549-2554.
103. Woolley CS, Weiland NG, McEwen BS, Schwartzkroin PA. 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. (Pubitemid 27089829)
104. Wu J, Song TB, Li YJ, He KS, Ge L, Wang LR. 2007. Prenatal restraint stress impairs learning and memory and hippocampal PKCbeta1 expression and translocation in offspring rats. Brain Res 1141:205-213. (Pubitemid 46365651)
105. Yaka R, Salomon S, Matzner H, Weinstock M. 2007. Effect ofvaried gestational stress on acquisition of spatial memory, hippocampal LTP and synaptic proteins in juvenile male rats. Behav Brain Res 179: 126-132. (Pubitemid 46441493)
106. Yang J, Han H, Cao J, Li L, Xu L. 2006. Prenatal stress modifies hippocampal synaptic plasticity and spatial learning in young rat offspring. Hippocampus 16:431-436. (Pubitemid 44712066)
107. 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. (Pubitemid 44781115)
108. Zohar I, Weinstock M. 2011. Differential effect of prenatal stress on the expression of cortiocotropin releasing hormone and its receptors in the hypothalamus and amygdala in male and female rats. J Neuroendocrinol 23:320-328.
109. Zuena AR, Mairesse J, Casolini P, Cinque C, Alema GS, Morley-Fletcher S, Chiodi V, Spagnoli LG, Gradini R, Catalani A, Nicoletti F, Maccari S. 2008. Prenatal restraint stress generates two distinct behavioral and neurochemical profiles in male and female rats. PLoS One 3:e2170.