McCarthy MM: Estradiol and the developing brain. Physiol Rev 2008, 88: 91–124. 10.1152/physrev.00010.2007
Article
CAS
PubMed Central
PubMed
Google Scholar
Amateau SK, Alt JJ, Stamps CL, McCarthy MM: Brain estradiol content in newborn rats: sex differences, regional heterogeneity, and possible de novo synthesis by the female telencephalon. Endocrinology 2004, 145: 2906–2917. 10.1210/en.2003-1363
Article
CAS
PubMed
Google Scholar
Mong JA, McCarthy MM: Steroid-induced developmental plasticity in hypothalamic astrocytes: implications for synaptic patterning. J Neurobiol 1999, 40: 602–619. 10.1002/(SICI)1097-4695(19990915)40:4<602::AID-NEU14>3.0.CO;2-O
Article
CAS
PubMed
Google Scholar
Schwarz JM, McCarthy MM: Cellular mechanisms of estradiol-mediated masculinization of the brain. J Steroid Biochem Mol Biol 2008, 109: 300–306. 10.1016/j.jsbmb.2008.03.012
Article
CAS
PubMed Central
PubMed
Google Scholar
Forger NG, Rosen GJ, Waters EM, Jacob D, Simerly RB, de Vries GJ: Deletion of Bax eliminates sex differences in the mouse forebrain. Proc Natl Acad Sci USA 2004, 101: 13666–13671. 10.1073/pnas.0404644101
Article
CAS
PubMed Central
PubMed
Google Scholar
Sengelaub DR, Forger NG: The spinal nucleus of the bulbocavernosus: firsts in androgen-dependent neural sex differences. Horm Behav 2008, 53: 596–612. 10.1016/j.yhbeh.2007.11.008
Article
CAS
PubMed Central
PubMed
Google Scholar
Phoenix CH, Goy RW, Gerall AA, Young WC: Organizing action of prenatally administered testosterone propionate on the tissues mediating mating behavior in the female guinea pig. Endocrinology 1959, 65: 369–382. 10.1210/endo-65-3-369
Article
CAS
PubMed
Google Scholar
Brake WG, Alves SE, Dunlop JC, Lee SJ, Bulloch K, Allen PB, Greengard P, McEwen BS: Novel target sites for estrogen action in the dorsal hippocampus: an examination of synaptic proteins. Endocrinology 2001, 142: 1284–1289. 10.1210/en.142.3.1284
CAS
PubMed
Google Scholar
Woolley CS: Effects of estrogen in the CNS. Curr Opin Neurobiol 1999, 9: 349–354. 10.1016/S0959-4388(99)80051-8
Article
CAS
PubMed
Google Scholar
Woolley CS: Acute effects of estrogen on neuronal physiology. Annu Rev Pharmacol Toxicol 2007, 47: 657–680. 10.1146/annurev.pharmtox.47.120505.105219
Article
CAS
PubMed
Google Scholar
Cooke BM, Woolley CS: Sexually dimorphic synaptic organization of the medial amygdala. J Neurosci 2005, 25: 10759–10767. 10.1523/JNEUROSCI.2919-05.2005
Article
CAS
PubMed
Google Scholar
Nunez JL, Koss WA, Juraska JM: Hippocampal anatomy and water maze performance are affected by neonatal cryoanesthesia in rats of both sexes. Horm Behav 2000, 37: 169–178. 10.1006/hbeh.2000.1572
Article
CAS
PubMed
Google Scholar
Roof RL: The dentate gyrus is sexually dimorphic in prepubescent rats: testosterone plays a significant role. Brain Res 1993, 610: 148–151. 10.1016/0006-8993(93)91228-K
Article
CAS
PubMed
Google Scholar
Roof RL, Havens MD: Testosterone improves maze performance and induces development of a male hippocampus in females. Brain Res 1992, 572: 310–313. 10.1016/0006-8993(92)90491-Q
Article
CAS
PubMed
Google Scholar
Isgor C, Sengelaub DR: Prenatal gonadal steroids affect adult spatial behavior, CA1 and CA3 pyramidal cell morphology in rats. Horm Behav 1998, 34: 183–198. 10.1006/hbeh.1998.1477
Article
CAS
PubMed
Google Scholar
Mirescu C, Peters JD, Gould E: Early life experience alters response of adult neurogenesis to stress. Nat Neurosci 2004, 7: 841–846. 10.1038/nn1290
Article
CAS
PubMed
Google Scholar
Lemaire V, Koehl M, Le Moal M, Abrous DN: Prenatal stress produces learning deficits associated with an inhibition of neurogenesis in the hippocampus. Proc Natl Acad Sci USA 2000, 97: 11032–11037. 10.1073/pnas.97.20.11032
Article
CAS
PubMed Central
PubMed
Google Scholar
Goel N, Bale TL: Organizational and activational effects of testosterone on masculinization of female physiological and behavioral stress responses. Endocrinology 2008, 149: 6399–6405. 10.1210/en.2008-0433
Article
CAS
PubMed Central
PubMed
Google Scholar
Perrot-Sinal TS, Kavaliers M, Ossenkopp KP: Spatial learning and hippocampal volume in male deer mice: relations to age, testosterone and adrenal gland weight. Neuroscience 1998, 86: 1089–1099. 10.1016/S0306-4522(98)00131-6
Article
CAS
PubMed
Google Scholar
Bangasser DA, Shors TJ: The bed nucleus of the stria terminalis modulates learning after stress in masculinized but not cycling females. J Neurosci 2008, 28: 6383–6387. 10.1523/JNEUROSCI.0831-08.2008
Article
CAS
PubMed Central
PubMed
Google Scholar
Nunez JL, McCarthy MM: Resting intracellular calcium concentration, depolarizing Gamma-Aminobutyric Acid and possible role of local estradiol synthesis in the developing male and female hippocampus. Neuroscience 2009, 158: 623–634. 10.1016/j.neuroscience.2008.09.061
Article
CAS
PubMed Central
PubMed
Google Scholar
Nunez JL, Bambrick LL, Krueger BK, McCarthy MM: Prolongation and enhancement of gamma-aminobutyric acid receptor mediated excitation by chronic treatment with estradiol in developing rat hippocampal neurons. Eur J Neurosci 2005, 21: 3251–3261. 10.1111/j.1460-9568.2005.04175.x
Article
PubMed
Google Scholar
Nunez JL, McCarthy MM: Androgens predispose males to GABAA-mediated excitotoxicity in the developing hippocampus. Exp Neurol 2008, 210: 699–708. 10.1016/j.expneurol.2008.01.001
Article
CAS
PubMed Central
PubMed
Google Scholar
Nunez JL, Aberdeen GW, Albrecht ED, McCarthy MM: Impact of estradiol on gamma-aminobutyric acid- and glutamate-mediated calcium responses of fetal baboon (Papio anubis) hippocampal and cortical neurons. Endocrinology 2008, 149: 6433–6443. 10.1210/en.2007-1720
Article
CAS
PubMed Central
PubMed
Google Scholar
Zhang JM, Konkle AT, Zup SL, McCarthy MM: Impact of sex and hormones on new cells in the developing rat hippocampus: a novel source of sex dimorphism? Eur J Neurosci 2008, 27: 791–800. 10.1111/j.1460-9568.2008.06073.x
Article
PubMed Central
PubMed
Google Scholar
Altman J, Das GD: Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J Comp Neurol 1965, 124: 319–335. 10.1002/cne.901240303
Article
CAS
PubMed
Google Scholar
Hine RJ, Das GD: Neuroembryogenesis in the hippocampal formation of the rat. An autoradiographic study. Z Anat Entwicklungsgesch 1974, 144: 173–186. 10.1007/BF00519773
Article
CAS
PubMed
Google Scholar
Schlessinger AR, Cowan WM, Gottlieb DI: An autoradiographic study of the time of origin and the pattern of granule cell migration in the dentate gyrus of the rat. J Comp Neurol 1975, 159: 149–175. 10.1002/cne.901590202
Article
CAS
PubMed
Google Scholar
Bayer SA: Development of the hippocampal region in the rat. I. Neurogenesis examined with 3H-thymidine autoradiography. J Comp Neurol 1980, 190: 87–114. 10.1002/cne.901900107
Article
CAS
PubMed
Google Scholar
Muramatsu R, Ikegaya Y, Matsuki N, Koyama R: Neonatally born granule cells numerically dominate adult mice dentate gyrus. Neuroscience 2007, 148: 593–598. 10.1016/j.neuroscience.2007.06.040
Article
CAS
PubMed
Google Scholar
Forger NG: Cell death and sexual differentiation of the nervous system. Neuroscience 2006, 138: 929–938. 10.1016/j.neuroscience.2005.07.006
Article
CAS
PubMed
Google Scholar
Mong JA, Glaser E, McCarthy MM: Gonadal steroids promote glial differentiation and alter neuronal morphology in the developing hypothalamus in a regionally specific manner. J Neurosci 1999, 19: 1464–1472.
CAS
PubMed
Google Scholar
Poulet FM, Roessler ML, Vancutsem PM: Initial uterine alterations caused by developmental exposure to tamoxifen. Reprod Toxicol 1997, 11: 815–822. 10.1016/S0890-6238(97)00065-8
Article
CAS
PubMed
Google Scholar
Yuan H, Bowlby DA, Brown TJ, Hochberg RB, MacLusky NJ: Distribution of occupied and unoccupied estrogen receptors in the rat brain: effects of physiological gonadal steroid exposure. Endocrinology 1995, 136: 96–105. 10.1210/en.136.1.96
CAS
PubMed
Google Scholar
Shughrue PJ, Lane MV, Merchenthaler I: Regulation of progesterone receptor messenger ribonucleic acid in the rat medial preoptic nucleus by estrogenic and antiestrogenic compounds: an in situ hybridization study. Endocrinology 1997, 138: 5476–5484. 10.1210/en.138.12.5476
Article
CAS
PubMed
Google Scholar
Galea LA: Gonadal hormone modulation of neurogenesis in the dentate gyrus of adult male and female rodents. Brain Res Rev 2008, 57: 332–341. 10.1016/j.brainresrev.2007.05.008
Article
CAS
PubMed
Google Scholar
Taupin P: BrdU immunohistochemistry for studying adult neurogenesis: paradigms, pitfalls, limitations, and validation. Brain Res Rev 2007, 53: 198–214. 10.1016/j.brainresrev.2006.08.002
Article
CAS
PubMed
Google Scholar
Norbury C, Nurse P: Animal cell cycles and their control. Annu Rev Biochem 1992, 61: 441–470. 10.1146/annurev.bi.61.070192.002301
Article
CAS
PubMed
Google Scholar
Lopez F, Belloc F, Lacombe F, Dumain P, Reiffers J, Bernard P, Boisseau MR: Modalities of synthesis of Ki67 antigen during the stimulation of lymphocytes. Cytometry 1991, 12: 42–49. 10.1002/cyto.990120107
Article
CAS
PubMed
Google Scholar
Endl E, Gerdes J: The Ki-67 protein: fascinating forms and an unknown function. Exp Cell Res 2000, 257: 231–237. 10.1006/excr.2000.4888
Article
CAS
PubMed
Google Scholar
Zacchetti A, van Garderen E, Teske E, Nederbragt H, Dierendonck JH, Rutteman GR: Validation of the use of proliferation markers in canine neoplastic and non-neoplastic tissues: comparison of KI-67 and proliferating cell nuclear antigen (PCNA) expression versus in vivo bromodeoxyuridine labelling by immunohistochemistry. APMIS 2003, 111: 430–438. 10.1034/j.1600-0463.2003.t01-1-1110208.x
Article
CAS
PubMed
Google Scholar
Scholzen T, Gerdes J: The Ki-67 protein: from the known and the unknown. J Cell Physiol 2000, 182: 311–322. 10.1002/(SICI)1097-4652(200003)182:3<311::AID-JCP1>3.0.CO;2-9
Article
CAS
PubMed
Google Scholar
Barha CK, Lieblich SE, Galea LA: Different forms of oestrogen rapidly upregulate cell proliferation in the dentate gyrus of adult female rats. J Neuroendocrinol 2009, 21: 155–166. 10.1111/j.1365-2826.2008.01809.x
Article
CAS
PubMed
Google Scholar
Galea LA, Spritzer MD, Barker JM, Pawluski JL: Gonadal hormone modulation of hippocampal neurogenesis in the adult. Hippocampus 2006, 16: 225–232. 10.1002/hipo.20154
Article
CAS
PubMed
Google Scholar
Woolley CS: Estrogen-mediated structural and functional synaptic plasticity in the female rat hippocampus. Horm Behav 1998, 34: 140–148. 10.1006/hbeh.1998.1466
Article
CAS
PubMed
Google Scholar
Lee SJ, Romeo RD, Svenningsson P, Campomanes CR, Allen PB, Greengard P, McEwen BS: Estradiol affects spinophilin protein differently in gonadectomized males and females. Neuroscience 2004, 127: 983–988. 10.1016/j.neuroscience.2004.05.049
Article
CAS
PubMed
Google Scholar
Woolley CS, Weiland NG, McEwen BS, Schwartzkroin PA: Estradiol increases the sensitivity of hippocampal CA1 pyramidal cells to NMDA receptor-mediated synaptic input: correlation with dendritic spine density. J Neurosci 1997, 17: 1848–1859.
CAS
PubMed
Google Scholar
Woolley CS, McEwen BS: Estradiol regulates hippocampal dendritic spine density via an N-methyl-D-aspartate receptor-dependent mechanism. J Neurosci 1994, 14: 7680–7687.
CAS
PubMed
Google Scholar
Leranth C, Petnehazy O, MacLusky NJ: Gonadal hormones affect spine synaptic density in the CA1 hippocampal subfield of male rats. J Neurosci 2003, 23: 1588–1592.
CAS
PubMed
Google Scholar
Barker JM, Galea LA: Repeated estradiol administration alters different aspects of neurogenesis and cell death in the hippocampus of female, but not male, rats. Neuroscience 2008, 152: 888–902. 10.1016/j.neuroscience.2007.10.071
Article
CAS
PubMed
Google Scholar
Levin ER: Cell localization, physiology, and nongenomic actions of estrogen receptors. J Appl Physiol 2001, 91: 1860–1867.
CAS
PubMed
Google Scholar
Dahlman-Wright K, Cavailles V, Fuqua SA, Jordan VC, Katzenellenbogen JA, Korach KS, Maggi A, Muramatsu M, Parker MG, Gustafsson JA: International Union of Pharmacology. LXIV. Estrogen receptors. Pharmacol Rev 2006, 58: 773–781. 10.1124/pr.58.4.8
Article
CAS
PubMed
Google Scholar
Isgor C, Watson SJ: Estrogen receptor alpha and beta mRNA expressions by proliferating and differentiating cells in the adult rat dentate gyrus and subventricular zone. Neuroscience 2005, 134: 847–856. 10.1016/j.neuroscience.2005.05.008
Article
CAS
PubMed
Google Scholar
Mazzucco CA, Lieblich SE, Bingham BI, Williamson MA, Viau V, Galea LA: Both estrogen receptor alpha and estrogen receptor beta agonists enhance cell proliferation in the dentate gyrus of adult female rats. Neuroscience 2006, 141: 1793–1800. 10.1016/j.neuroscience.2006.05.032
Article
CAS
PubMed
Google Scholar
Mitra SW, Hoskin E, Yudkovitz J, Pear L, Wilkinson HA, Hayashi S, Pfaff DW, Ogawa S, Rohrer SP, Schaeffer JM, McEwen BS, Alves SE: Immunolocalization of estrogen receptor beta in the mouse brain: comparison with estrogen receptor alpha. Endocrinology 2003, 144: 2055–2067. 10.1210/en.2002-221069
Article
CAS
PubMed
Google Scholar
Ivanova T, Beyer C: Ontogenetic expression and sex differences of aromatase and estrogen receptor-alpha/beta mRNA in the mouse hippocampus. Cell Tissue Res 2000, 300: 231–237. 10.1007/s004410000199
Article
CAS
PubMed
Google Scholar
Shughrue PJ, Lane MV, Merchenthaler I: Comparative distribution of estrogen receptor-alpha and -beta mRNA in the rat central nervous system. J Comp Neurol 1997, 388: 507–525. 10.1002/(SICI)1096-9861(19971201)388:4<507::AID-CNE1>3.0.CO;2-6
Article
CAS
PubMed
Google Scholar
Prewitt AK, Wilson ME: Changes in estrogen receptor-alpha mRNA in the mouse cortex during development. Brain Res 2007, 1134: 62–69. 10.1016/j.brainres.2006.11.069
Article
CAS
PubMed Central
PubMed
Google Scholar
Miranda RC, Toran-Allerand CD: Developmental expression of estrogen receptor mRNA in the rat cerebral cortex: a nonisotopic in situ hybridization histochemistry study. Cereb Cortex 1992, 2: 1–15. 10.1093/cercor/2.1.1
Article
CAS
PubMed
Google Scholar
Solum DT, Handa RJ: Localization of estrogen receptor alpha (ER alpha) in pyramidal neurons of the developing rat hippocampus. Brain Res Dev Brain Res 2001, 128: 165–175. 10.1016/S0165-3806(01)00171-7
Article
CAS
PubMed
Google Scholar
Martinez-Cerdeno V, Noctor SC, Kriegstein AR: Estradiol stimulates progenitor cell division in the ventricular and subventricular zones of the embryonic neocortex. Eur J Neurosci 2006, 24: 3475–3488. 10.1111/j.1460-9568.2006.05239.x
Article
PubMed
Google Scholar
Konkle AT, McCarthy MM: Developmental Time Course of Estradiol, Testosterone, and Dihydrotestosterone Levels in Discrete Regions of Male and Female Rat Brain. Endocrinology 2010.
Google Scholar
Lam TT, Leranth C: Role of the medial septum diagonal band of Broca cholinergic neurons in oestrogen-induced spine synapse formation on hippocampal CA1 pyramidal cells of female rats. Eur J Neurosci 2003, 17: 1997–2005. 10.1046/j.1460-9568.2003.02637.x
Article
PubMed
Google Scholar
Campbell NR, Fernandes CC, Halff AW, Berg DK: Endogenous signaling through alpha7-containing nicotinic receptors promotes maturation and integration of adult-born neurons in the hippocampus. J Neurosci 2010, 30: 8734–8744. 10.1523/JNEUROSCI.0931-10.2010
Article
CAS
PubMed Central
PubMed
Google Scholar
Mitsushima D, Takase K, Takahashi T, Kimura F: Activational and organisational effects of gonadal steroids on sex-specific acetylcholine release in the dorsal hippocampus. J Neuroendocrinol 2009, 21: 400–405. 10.1111/j.1365-2826.2009.01848.x
Article
CAS
PubMed
Google Scholar
Mitsushima D, Takase K, Funabashi T, Kimura F: Gonadal steroids maintain 24 h acetylcholine release in the hippocampus: organizational and activational effects in behaving rats. J Neurosci 2009, 29: 3808–3815. 10.1523/JNEUROSCI.5301-08.2009
Article
CAS
PubMed
Google Scholar
Schaevitz LR, Berger-Sweeney J: Neurogenesis of the cholinergic medial septum in female and male C57BL/6J mice. J Neurobiol 2005, 65: 294–303. 10.1002/neu.20188
Article
PubMed
Google Scholar
Crews JK, Murphy JG, Khalil RA: Gender differences in Ca(2+) entry mechanisms of vasoconstriction in Wistar-Kyoto and spontaneously hypertensive rats. Hypertension 1999, 34: 931–936.
Article
CAS
PubMed
Google Scholar
Murphy JG, Khalil RA: Gender-specific reduction in contractility and [Ca(2+)](i) in vascular smooth muscle cells of female rat. Am J Physiol Cell Physiol 2000, 278: C834–844.
CAS
PubMed
Google Scholar
Li Z, Krause DN, Doolen S, Duckles SP: Ovariectomy eliminates sex differences in rat tail artery response to adrenergic nerve stimulation. Am J Physiol 1997, 272: H1819–1825.
CAS
PubMed
Google Scholar
Geary GG, Krause DN, Duckles SP: Estrogen reduces mouse cerebral artery tone through endothelial NOS- and cyclooxygenase-dependent mechanisms. Am J Physiol Heart Circ Physiol 2000, 279: H511–519.
CAS
PubMed
Google Scholar
Haynes MP, Sinha D, Russell KS, Collinge M, Fulton D, Morales-Ruiz M, Sessa WC, Bender JR: Membrane estrogen receptor engagement activates endothelial nitric oxide synthase via the PI3-kinase-Akt pathway in human endothelial cells. Circ Res 2000, 87: 677–682.
Article
CAS
PubMed
Google Scholar
Stirone C, Boroujerdi A, Duckles SP, Krause DN: Estrogen receptor activation of phosphoinositide-3 kinase, akt, and nitric oxide signaling in cerebral blood vessels: rapid and long-term effects. Mol Pharmacol 2005, 67: 105–113. 10.1124/mol.104.004465
Article
CAS
PubMed
Google Scholar
Chambliss KL, Yuhanna IS, Mineo C, Liu P, German Z, Sherman TS, Mendelsohn ME, Anderson RG, Shaul PW: Estrogen receptor alpha and endothelial nitric oxide synthase are organized into a functional signaling module in caveolae. Circ Res 2000, 87: E44–52.
Article
CAS
PubMed
Google Scholar
Pare G, Krust A, Karas RH, Dupont S, Aronovitz M, Chambon P, Mendelsohn ME: Estrogen receptor-alpha mediates the protective effects of estrogen against vascular injury. Circ Res 2002, 90: 1087–1092. 10.1161/01.RES.0000021114.92282.FA
Article
CAS
PubMed
Google Scholar
Mendelsohn ME: Genomic and nongenomic effects of estrogen in the vasculature. Am J Cardiol 2002, 90: 3F-6F. 10.1016/S0002-9149(02)02418-9
Article
CAS
PubMed
Google Scholar
Trejo JL, Carro E, Torres-Aleman I: Circulating insulin-like growth factor I mediates exercise-induced increases in the number of new neurons in the adult hippocampus. J Neurosci 2001, 21: 1628–1634.
CAS
PubMed
Google Scholar
van Praag H, Kempermann G, Gage FH: Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nat Neurosci 1999, 2: 266–270. 10.1038/6368
Article
CAS
PubMed
Google Scholar
Altman J, Das GD: Postnatal neurogenesis in the guinea-pig. Nature 1967, 214: 1098–1101. 10.1038/2141098a0
Article
CAS
PubMed
Google Scholar
Gould E, Tanapat P, McEwen BS, Flugge G, Fuchs E: Proliferation of granule cell precursors in the dentate gyrus of adult monkeys is diminished by stress. Proc Natl Acad Sci USA 1998, 95: 3168–3171. 10.1073/pnas.95.6.3168
Article
CAS
PubMed Central
PubMed
Google Scholar
Moore CL: The role of maternal stimulation in the development of sexual behavior and its neural basis. Ann N Y Acad Sci 1992, 662: 160–177. 10.1111/j.1749-6632.1992.tb22859.x
Article
CAS
PubMed
Google Scholar
Knable MB, Barci BM, Webster MJ, Meador-Woodruff J, Torrey EF: Molecular abnormalities of the hippocampus in severe psychiatric illness: postmortem findings from the Stanley Neuropathology Consortium. Mol Psychiatry 2004, 9: 609–620. 544 10.1038/sj.mp.4001471
Article
CAS
PubMed
Google Scholar
McEwen BS: Possible mechanisms for atrophy of the human hippocampus. Mol Psychiatry 1997, 2: 255–262. 10.1038/sj.mp.4000254
Article
CAS
PubMed
Google Scholar
Nestor PG, Kubicki M, Kuroki N, Gurrera RJ, Niznikiewicz M, Shenton ME, McCarley RW: Episodic memory and neuroimaging of hippocampus and fornix in chronic schizophrenia. Psychiatry Res 2007, 155: 21–28. 10.1016/j.pscychresns.2006.12.020
Article
PubMed
Google Scholar
Tanskanen P, Veijola JM, Piippo UK, Haapea M, Miettunen JA, Pyhtinen J, Bullmore ET, Jones PB, Isohanni MK: Hippocampus and amygdala volumes in schizophrenia and other psychoses in the Northern Finland 1966 birth cohort. Schizophr Res 2005, 75: 283–294. 10.1016/j.schres.2004.09.022
Article
PubMed
Google Scholar
Schmidt-Kastner R, Freund TF: Selective vulnerability of the hippocampus in brain ischemia. Neuroscience 1991, 40: 599–636. 10.1016/0306-4522(91)90001-5
Article
CAS
PubMed
Google Scholar