{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,29]],"date-time":"2026-09-29T23:17:11Z","timestamp":1790723831158,"version":"4.1.0"},"reference-count":123,"publisher":"Public Library of Science (PLoS)","issue":"1","license":[{"start":{"date-parts":[[2009,1,29]],"date-time":"2009-01-29T00:00:00Z","timestamp":1233187200000},"content-version":"unspecified","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["www.plosone.org"],"crossmark-restriction":false},"short-container-title":["PLoS ONE"],"DOI":"10.1371\/journal.pone.0003675","type":"journal-article","created":{"date-parts":[[2009,1,29]],"date-time":"2009-01-29T00:00:48Z","timestamp":1233187248000},"page":"e3675","update-policy":"https:\/\/doi.org\/10.1371\/journal.pone.corrections_policy","source":"Crossref","is-referenced-by-count":165,"title":["Opposite Effects of Early Maternal Deprivation on Neurogenesis in Male versus Female Rats"],"prefix":"10.1371","volume":"4","author":[{"given":"Charlotte A.","family":"Oomen","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Carlos E. N.","family":"Girardi","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Rudy","family":"Cahyadi","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Eva C.","family":"Verbeek","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Harm","family":"Krugers","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Marian","family":"Jo\u00ebls","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Paul J.","family":"Lucassen","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"340","published-online":{"date-parts":[[2009,1,29]]},"reference":[{"key":"ref1","doi-asserted-by":"crossref","first-page":"516","DOI":"10.1097\/00004714-200110000-00009","article-title":"Rapid reversal of psychotic depression using mifepristone.","volume":"21","author":"JK Belanoff","year":"2001","journal-title":"J Clin Psychopharmacol"},{"key":"ref2","doi-asserted-by":"crossref","first-page":"386","DOI":"10.1016\/S0006-3223(02)01432-4","article-title":"An open label trial of C-1073 (mifepristone) for psychotic major depression.","volume":"52","author":"JK Belanoff","year":"2002","journal-title":"Biol Psychiatry"},{"key":"ref3","doi-asserted-by":"crossref","first-page":"254","DOI":"10.1038\/sj.mp.4001032","article-title":"Organization of the stress system and its dysregulation in melancholic and atypical depression: high vs low CRH\/NE states.","volume":"7","author":"PW Gold","year":"2002","journal-title":"Mol Psychiatry"},{"key":"ref4","doi-asserted-by":"crossref","first-page":"1023","DOI":"10.1016\/S0006-3223(01)01157-X","article-title":"The role of childhood trauma in the neurobiology of mood and anxiety disorders: preclinical and clinical studies.","volume":"49","author":"C Heim","year":"2001","journal-title":"Biol Psychiatry"},{"key":"ref5","doi-asserted-by":"crossref","first-page":"592","DOI":"10.1001\/jama.284.5.592","article-title":"Pituitary-adrenal and autonomic responses to stress in women after sexual and physical abuse in childhood.","volume":"284","author":"C Heim","year":"2000","journal-title":"Jama"},{"key":"ref6","doi-asserted-by":"crossref","first-page":"477","DOI":"10.1016\/S0893-133X(00)00159-7","article-title":"The corticosteroid receptor hypothesis of depression.","volume":"23","author":"F Holsboer","year":"2000","journal-title":"Neuropsychopharmacology"},{"key":"ref7","doi-asserted-by":"crossref","first-page":"1789","DOI":"10.1517\/13543784.10.10.1789","article-title":"Antiglucocorticoid drugs in the treatment of depression.","volume":"10","author":"VI Reus","year":"2001","journal-title":"Expert Opin Investig Drugs"},{"key":"ref8","doi-asserted-by":"crossref","first-page":"4505","DOI":"10.1523\/JNEUROSCI.21-12-04505.2001","article-title":"Impaired recognition of the goal location during spatial navigation in rats with hippocampal lesions.","volume":"21","author":"SA Hollup","year":"2001","journal-title":"J Neurosci"},{"key":"ref9","doi-asserted-by":"crossref","first-page":"47","DOI":"10.1016\/0165-0270(84)90007-4","article-title":"Developments of a water-maze procedure for studying spatial learning in the rat.","volume":"11","author":"R Morris","year":"1984","journal-title":"J Neurosci Methods"},{"key":"ref10","doi-asserted-by":"crossref","first-page":"215","DOI":"10.1016\/j.bbr.2006.05.035","article-title":"Role of the ventral subiculum in stress integration.","volume":"174","author":"JP Herman","year":"2006","journal-title":"Behav Brain Res"},{"key":"ref11","doi-asserted-by":"crossref","first-page":"463","DOI":"10.1038\/nrn1683","article-title":"Stress and the brain: from adaptation to disease.","volume":"6","author":"ER de Kloet","year":"2005","journal-title":"Nat Rev Neurosci"},{"key":"ref12","doi-asserted-by":"crossref","first-page":"1242","DOI":"10.1038\/nn958","article-title":"Smaller hippocampal volume predicts pathologic vulnerability to psychological trauma.","volume":"5","author":"MW Gilbertson","year":"2002","journal-title":"Nat Neurosci"},{"key":"ref13","doi-asserted-by":"crossref","first-page":"1616","DOI":"10.1038\/sj.npp.1300982","article-title":"Astroglial plasticity in the hippocampus is affected by chronic psychosocial stress and concomitant fluoxetine treatment.","volume":"31","author":"B Czeh","year":"2006","journal-title":"Neuropsychopharmacology"},{"key":"ref14","doi-asserted-by":"crossref","first-page":"742","DOI":"10.1002\/hipo.10212","article-title":"Homeostatic maintenance in excitability of tree shrew hippocampal CA3 pyramidal neurons after chronic stress.","volume":"14","author":"MH Kole","year":"2004","journal-title":"Hippocampus"},{"key":"ref15","doi-asserted-by":"crossref","first-page":"3534","DOI":"10.1523\/JNEUROSCI.16-10-03534.1996","article-title":"Chronic psychosocial stress causes apical dendritic atrophy of hippocampal CA3 pyramidal neurons in subordinate tree shrews.","volume":"16","author":"AM Magarinos","year":"1996","journal-title":"J Neurosci"},{"key":"ref16","doi-asserted-by":"crossref","first-page":"14002","DOI":"10.1073\/pnas.94.25.14002","article-title":"Chronic stress alters synaptic terminal structure in hippocampus.","volume":"94","author":"AM Magarinos","year":"1997","journal-title":"Proc Natl Acad Sci U S A"},{"key":"ref17","article-title":"Brief treatment with the GR antagonist mifepristone normalizes the reduction in neurogenesis after chronic stress. submitted","author":"CA Oomen","year":"2007"},{"key":"ref18","doi-asserted-by":"crossref","first-page":"2492","DOI":"10.1523\/JNEUROSCI.17-07-02492.1997","article-title":"Neurogenesis in the dentate gyrus of the adult tree shrew is regulated by psychosocial stress and NMDA receptor activation.","volume":"17","author":"E Gould","year":"1997","journal-title":"J Neurosci"},{"key":"ref19","doi-asserted-by":"crossref","first-page":"131","DOI":"10.1046\/j.1460-9568.2003.03100.x","article-title":"Suppressed proliferation and apoptotic changes in the rat dentate gyrus after acute and chronic stress are reversible.","volume":"19","author":"VM Heine","year":"2004","journal-title":"Eur J Neurosci"},{"key":"ref20","doi-asserted-by":"crossref","first-page":"879","DOI":"10.1046\/j.1460-9568.2003.02513.x","article-title":"Repeated restraint stress suppresses neurogenesis and induces biphasic PSA-NCAM expression in the adult rat dentate gyrus.","volume":"17","author":"K Pham","year":"2003","journal-title":"Eur J Neurosci"},{"key":"ref21","doi-asserted-by":"crossref","first-page":"523","DOI":"10.1152\/physrev.00055.2003","article-title":"Adult neurogenesis: from precursors to network and physiology.","volume":"85","author":"DN Abrous","year":"2005","journal-title":"Physiol Rev"},{"key":"ref22","doi-asserted-by":"crossref","first-page":"974","DOI":"10.1038\/sj.mp.4001419","article-title":"Differential effects of learning on neurogenesis: learning increases or decreases the number of newly born cells depending on their birth date.","volume":"8","author":"MD Dobrossy","year":"2003","journal-title":"Mol Psychiatry"},{"key":"ref23","doi-asserted-by":"crossref","first-page":"e214","DOI":"10.1371\/journal.pbio.0050214","article-title":"Spatial learning depends on both the addition and removal of new hippocampal neurons.","volume":"5","author":"D Dupret","year":"2007","journal-title":"PLoS Biol"},{"key":"ref24","doi-asserted-by":"crossref","first-page":"355","DOI":"10.1038\/nn1847","article-title":"Preferential incorporation of adult-generated granule cells into spatial memory networks in the dentate gyrus.","volume":"10","author":"N Kee","year":"2007","journal-title":"Nat Neurosci"},{"key":"ref25","doi-asserted-by":"crossref","first-page":"216","DOI":"10.1002\/hipo.20153","article-title":"Is there a link between adult neurogenesis and learning?","volume":"16","author":"B Leuner","year":"2006","journal-title":"Hippocampus"},{"key":"ref26","doi-asserted-by":"crossref","first-page":"1087","DOI":"10.1016\/j.biopsych.2005.11.025","article-title":"Agomelatine, a new antidepressant, induces regional changes in hippocampal neurogenesis.","volume":"59","author":"M Banasr","year":"2006","journal-title":"Biol Psychiatry"},{"key":"ref27","doi-asserted-by":"crossref","first-page":"1136","DOI":"10.1016\/j.biopsych.2006.03.082","article-title":"Hippocampal neurogenesis: regulation by stress and antidepressants.","volume":"59","author":"A Dranovsky","year":"2006","journal-title":"Biol Psychiatry"},{"key":"ref28","doi-asserted-by":"crossref","first-page":"629","DOI":"10.1111\/j.1365-2826.2006.01455.x","article-title":"Brief treatment with the glucocorticoid receptor antagonist mifepristone normalises the corticosterone-induced reduction of adult hippocampal neurogenesis.","volume":"18","author":"JL Mayer","year":"2006","journal-title":"J Neuroendocrinol"},{"key":"ref29","doi-asserted-by":"crossref","first-page":"805","DOI":"10.1126\/science.1083328","article-title":"Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants.","volume":"301","author":"L Santarelli","year":"2003","journal-title":"Science"},{"key":"ref30","first-page":"183","article-title":"Even neural stem cells get the blues: evidence for a molecular link between modulation of adult neurogenesis and depression.","volume":"14","author":"RM Thomas","year":"2008","journal-title":"Gene Expr"},{"key":"ref31","doi-asserted-by":"crossref","first-page":"83","DOI":"10.1016\/j.neuroscience.2005.08.073","article-title":"Raised circulating corticosterone inhibits neuronal differentiation of progenitor cells in the adult hippocampus.","volume":"137","author":"EY Wong","year":"2006","journal-title":"Neuroscience"},{"key":"ref32","doi-asserted-by":"crossref","first-page":"233","DOI":"10.1002\/hipo.20155","article-title":"Stress and adult neurogenesis.","volume":"16","author":"C Mirescu","year":"2006","journal-title":"Hippocampus"},{"key":"ref33","first-page":"363","article-title":"Regulation of hippocampal neurogenesis by systemic factors including stress, glucocorticoids, sleep, and inflammation.;","author":"PJ Lucassen","year":"2008"},{"key":"ref34","doi-asserted-by":"crossref","first-page":"367","DOI":"10.1177\/070674379704200403","article-title":"Epidemiology of affective disorders: a review.","volume":"42","author":"RC Bland","year":"1997","journal-title":"Can J Psychiatry"},{"key":"ref35","doi-asserted-by":"crossref","first-page":"85","DOI":"10.1016\/0165-0327(93)90026-G","article-title":"Sex and depression in the National Comorbidity Survey. I: Lifetime prevalence, chronicity and recurrence.","volume":"29","author":"RC Kessler","year":"1993","journal-title":"J Affect Disord"},{"key":"ref36","first-page":"54","article-title":"Cross-national epidemiology of depression and gender.","volume":"3","author":"TB Ustun","year":"2000","journal-title":"J Gend Specif Med"},{"key":"ref37","doi-asserted-by":"crossref","first-page":"816","DOI":"10.1176\/ajp.156.6.816","article-title":"Childhood sexual abuse as a risk factor for depression in women: psychosocial and neurobiological correlates.","volume":"156","author":"EL Weiss","year":"1999","journal-title":"Am J Psychiatry"},{"key":"ref38","first-page":"21","article-title":"Sex differences and the HPA axis: implications for psychiatric disease.","volume":"1","author":"EA Young","year":"1998","journal-title":"J Gend Specif Med"},{"key":"ref39","doi-asserted-by":"crossref","first-page":"2072","DOI":"10.1176\/appi.ajp.159.12.2072","article-title":"Childhood trauma associated with smaller hippocampal volume in women with major depression.","volume":"159","author":"M Vythilingam","year":"2002","journal-title":"Am J Psychiatry"},{"key":"ref40","doi-asserted-by":"crossref","first-page":"370","DOI":"10.1016\/j.yhbeh.2006.04.008","article-title":"High post-partum levels of corticosterone given to dams influence postnatal hippocampal cell proliferation and behavior of offspring: A model of post-partum stress and possible depression.","volume":"50","author":"S Brummelte","year":"2006","journal-title":"Horm Behav"},{"key":"ref41","doi-asserted-by":"crossref","first-page":"1025","DOI":"10.1016\/S0006-3223(03)00698-X","article-title":"Prenatal stress diminishes neurogenesis in the dentate gyrus of juvenile rhesus monkeys.","volume":"54","author":"CL Coe","year":"2003","journal-title":"Biol Psychiatry"},{"key":"ref42","doi-asserted-by":"crossref","first-page":"571","DOI":"10.1016\/j.brainresrev.2007.11.004","article-title":"Epigenetic programming of the stress response in male and female rats by prenatal restraint stress.","volume":"57","author":"M Darnaudery","year":"2008","journal-title":"Brain Res Rev"},{"key":"ref43","doi-asserted-by":"crossref","first-page":"65","DOI":"10.1007\/BF03033231","article-title":"Long term neurodevelopmental and behavioral effects of perinatal life events in rats.","volume":"3","author":"M Koehl","year":"2001","journal-title":"Neurotox Res"},{"key":"ref44","doi-asserted-by":"crossref","first-page":"457","DOI":"10.1016\/S0149-7634(02)00015-5","article-title":"The role of prenatal stress in the etiology of developmental behavioural disorders.","volume":"26","author":"O Kofman","year":"2002","journal-title":"Neurosci Biobehav Rev"},{"key":"ref45","doi-asserted-by":"crossref","first-page":"11032","DOI":"10.1073\/pnas.97.20.11032","article-title":"Prenatal stress produces learning deficits associated with an inhibition of neurogenesis in the hippocampus.","volume":"97","author":"V Lemaire","year":"2000","journal-title":"Proc Natl Acad Sci U S A"},{"key":"ref46","doi-asserted-by":"crossref","first-page":"786","DOI":"10.1016\/j.biopsych.2005.11.009","article-title":"Postnatal stimulation of the pups counteracts prenatal stress-induced deficits in hippocampal neurogenesis.","volume":"59","author":"V Lemaire","year":"2006","journal-title":"Biol Psychiatry"},{"key":"ref47","doi-asserted-by":"crossref","first-page":"575","DOI":"10.1002\/dneu.20600","article-title":"Stress experienced in utero reduces sexual dichotomies in neurogenesis, microenvironment, and cell death in the adult rat hippocampus.","volume":"68","author":"CD Mandyam","year":"2008","journal-title":"Dev Neurobiol"},{"key":"ref48","doi-asserted-by":"crossref","first-page":"1730","DOI":"10.1007\/s11064-007-9339-4","article-title":"Gender differences in the effects of prenatal stress on brain development and behaviour.","volume":"32","author":"M Weinstock","year":"2007","journal-title":"Neurochem Res"},{"key":"ref49","doi-asserted-by":"crossref","first-page":"113","DOI":"10.1111\/j.1365-2826.2001.00601.x","article-title":"Prenatal stress, glucocorticoids and the programming of the brain.","volume":"13","author":"LA Welberg","year":"2001","journal-title":"J Neuroendocrinol"},{"key":"ref50","doi-asserted-by":"crossref","first-page":"341","DOI":"10.1111\/j.1365-2826.1994.tb00591.x","article-title":"Prenatal stress increases the hypothalamo-pituitary-adrenal axis response in young and adult rats.","volume":"6","author":"C Henry","year":"1994","journal-title":"J Neuroendocrinol"},{"key":"ref51","doi-asserted-by":"crossref","first-page":"2626","DOI":"10.1523\/JNEUROSCI.17-07-02626.1997","article-title":"Prenatal stress induces high anxiety and postnatal handling induces low anxiety in adult offspring: correlation with stress-induced corticosterone secretion.","volume":"17","author":"M Vallee","year":"1997","journal-title":"J Neurosci"},{"key":"ref52","doi-asserted-by":"crossref","first-page":"810","DOI":"10.1038\/sj.mp.4001118","article-title":"Depression: reduced number of granule cells in the hippocampus of female, but not male, rats due to prenatal restraint stress.","volume":"7","author":"C Schmitz","year":"2002","journal-title":"Mol Psychiatry"},{"key":"ref53","doi-asserted-by":"crossref","first-page":"141","DOI":"10.1016\/S0091-3057(02)00788-8","article-title":"Effect of a single maternal separation at different pup ages on the corticosterone stress response in adult and aged rats.","volume":"73","author":"J Lehmann","year":"2002","journal-title":"Pharmacol Biochem Behav"},{"key":"ref54","doi-asserted-by":"crossref","first-page":"475","DOI":"10.1111\/j.1467-6494.1956.tb01283.x","article-title":"The effects of early shock and handling on later avoidance learning.","volume":"24","author":"S Levine","year":"1956","journal-title":"J Pers"},{"key":"ref55","doi-asserted-by":"crossref","first-page":"57","DOI":"10.1016\/S0149-7634(03)00009-5","article-title":"Long-term neurobehavioural impact of the postnatal environment in rats: manipulations, effects and mediating mechanisms.","volume":"27","author":"CR Pryce","year":"2003","journal-title":"Neurosci Biobehav Rev"},{"key":"ref56","doi-asserted-by":"crossref","first-page":"195","DOI":"10.1016\/0169-328X(93)90189-V","article-title":"Early, postnatal experience alters hypothalamic corticotropin-releasing factor (CRF) mRNA, median eminence CRF content and stress-induced release in adult rats.","volume":"18","author":"PM Plotsky","year":"1993","journal-title":"Brain Res Mol Brain Res"},{"key":"ref57","doi-asserted-by":"crossref","first-page":"275","DOI":"10.1111\/j.1749-6632.1994.tb39245.x","article-title":"The ontogeny of the hypothalamic-pituitary-adrenal axis. The influence of maternal factors.","volume":"746","author":"S Levine","year":"1994","journal-title":"Ann N Y Acad Sci"},{"key":"ref58","doi-asserted-by":"crossref","first-page":"1445","DOI":"10.1210\/endo-118-4-1445","article-title":"Ontogeny of the stress response in the rat: role of the pituitary and the hypothalamus.","volume":"118","author":"CD Walker","year":"1986","journal-title":"Endocrinology"},{"key":"ref59","doi-asserted-by":"crossref","first-page":"569","DOI":"10.1046\/j.1365-2826.2001.00668.x","article-title":"Differential and age-dependent effects of maternal deprivation on the hypothalamic-pituitary-adrenal axis of brown norway rats from youth to senescence.","volume":"13","author":"JO Workel","year":"2001","journal-title":"J Neuroendocrinol"},{"key":"ref60","doi-asserted-by":"crossref","first-page":"747","DOI":"10.1046\/j.0953-816x.2001.01691.x","article-title":"Postnatal maternal deprivation produces long-lasting modifications of the stress response, feeding and stress-related behaviour in the rat.","volume":"14","author":"Z Penke","year":"2001","journal-title":"Eur J Neurosci"},{"key":"ref61","doi-asserted-by":"crossref","first-page":"199","DOI":"10.1016\/S0165-3806(97)81796-8","article-title":"The Brown Norway rat displays enhanced stress-induced ACTH reactivity at day 18 after 24-h maternal deprivation at day 3.","volume":"103","author":"JO Workel","year":"1997","journal-title":"Brain Res Dev Brain Res"},{"key":"ref62","doi-asserted-by":"crossref","first-page":"1212","DOI":"10.1210\/endo.137.4.8625891","article-title":"Persistent changes in corticotropin-releasing factor neuronal systems induced by maternal deprivation.","volume":"137","author":"CO Ladd","year":"1996","journal-title":"Endocrinology"},{"key":"ref63","doi-asserted-by":"crossref","first-page":"5","DOI":"10.1046\/j.1365-2826.2000.00422.x","article-title":"Influence of neonatal rearing conditions on stress-induced adrenocorticotropin responses and norepinepherine release in the hypothalamic paraventricular nucleus.","volume":"12","author":"D Liu","year":"2000","journal-title":"J Neuroendocrinol"},{"key":"ref64","doi-asserted-by":"crossref","first-page":"1017","DOI":"10.1111\/j.1460-9568.2004.03541.x","article-title":"Dissociation in the effects of neonatal maternal separations on maternal care and the offspring&apos;s HPA and fear responses in rats.","volume":"20","author":"S Macri","year":"2004","journal-title":"Eur J Neurosci"},{"key":"ref65","doi-asserted-by":"crossref","first-page":"2192","DOI":"10.1038\/sj.npp.1300769","article-title":"Long-term consequences of neonatal rearing on central corticotropin-releasing factor systems in adult male rat offspring.","volume":"30","author":"PM Plotsky","year":"2005","journal-title":"Neuropsychopharmacology"},{"key":"ref66","doi-asserted-by":"crossref","first-page":"259","DOI":"10.1016\/j.ijdevneu.2008.02.004","article-title":"Sexually dimorphic effects of maternal separation stress on corticotrophin-releasing factor and vasopressin systems in the adult rat brain.","volume":"26","author":"L Desbonnet","year":"2008","journal-title":"Int J Dev Neurosci"},{"key":"ref67","doi-asserted-by":"crossref","first-page":"131","DOI":"10.1016\/S0091-3057(02)00781-5","article-title":"Long-lasting changes in stress-induced corticosterone response and anxiety-like behaviors as a consequence of neonatal maternal separation in Long-Evans rats.","volume":"73","author":"M Kalinichev","year":"2002","journal-title":"Pharmacol Biochem Behav"},{"key":"ref68","doi-asserted-by":"crossref","first-page":"123","DOI":"10.1016\/j.brainres.2006.04.066","article-title":"Long-lasting changes in behavioural and neuroendocrine indices in the rat following neonatal maternal separation: gender-dependent effects.","volume":"1097","author":"HA Slotten","year":"2006","journal-title":"Brain Res"},{"key":"ref69","doi-asserted-by":"crossref","first-page":"293","DOI":"10.1016\/S0031-9384(98)00300-X","article-title":"Periodic maternal deprivation induces gender-dependent alterations in behavioral and neuroendocrine responses to emotional stress in adult rats.","volume":"66","author":"A Wigger","year":"1999","journal-title":"Physiol Behav"},{"key":"ref70","doi-asserted-by":"crossref","first-page":"9328","DOI":"10.1523\/JNEUROSCI.2281-05.2005","article-title":"Mechanisms of late-onset cognitive decline after early-life stress.","volume":"25","author":"KL Brunson","year":"2005","journal-title":"J Neurosci"},{"key":"ref71","doi-asserted-by":"crossref","first-page":"403","DOI":"10.1007\/s00429-007-0169-6","article-title":"The impact of maternal separation on adult mouse behaviour and on the total neuron number in the mouse hippocampus.","volume":"212","author":"K Fabricius","year":"2008","journal-title":"Brain Struct Funct"},{"key":"ref72","doi-asserted-by":"crossref","first-page":"52","DOI":"10.1016\/S0006-8993(02)02985-2","article-title":"Neonatal maternal separation reduces hippocampal mossy fiber density in adult Long Evans rats.","volume":"950","author":"RL Huot","year":"2002","journal-title":"Brain Res"},{"key":"ref73","doi-asserted-by":"crossref","first-page":"841","DOI":"10.1038\/nn1290","article-title":"Early life experience alters response of adult neurogenesis to stress.","volume":"7","author":"C Mirescu","year":"2004","journal-title":"Nat Neurosci"},{"key":"ref74","doi-asserted-by":"crossref","first-page":"2903","DOI":"10.1111\/j.1460-9568.2003.02965.x","article-title":"Maternal care influences neuronal survival in the hippocampus of the rat.","volume":"18","author":"TW Bredy","year":"2003","journal-title":"Eur J Neurosci"},{"key":"ref75","doi-asserted-by":"crossref","first-page":"772","DOI":"10.1002\/jnr.20418","article-title":"Increased adult hippocampal brain-derived neurotrophic factor and normal levels of neurogenesis in maternal separation rats.","volume":"79","author":"MH Greisen","year":"2005","journal-title":"J Neurosci Res"},{"key":"ref76","doi-asserted-by":"crossref","first-page":"365","DOI":"10.1002\/cne.903010304","article-title":"Migration and distribution of two populations of hippocampal granule cell precursors during the perinatal and postnatal periods.","volume":"301","author":"J Altman","year":"1990","journal-title":"J Comp Neurol"},{"key":"ref77","doi-asserted-by":"crossref","first-page":"325","DOI":"10.1002\/cne.903010302","article-title":"Mosaic organization of the hippocampal neuroepithelium and the multiple germinal sources of dentate granule cells.","volume":"301","author":"J Altman","year":"1990","journal-title":"J Comp Neurol"},{"key":"ref78","doi-asserted-by":"crossref","first-page":"180","DOI":"10.1016\/j.yfrne.2006.02.001","article-title":"Hippocampal neuroplasticity induced by early-life stress: functional and molecular aspects.","volume":"27","author":"KA Fenoglio","year":"2006","journal-title":"Front Neuroendocrinol"},{"key":"ref79","article-title":"Adult neurogenesis, Stem Cells and Neuronal Development in the Adult Brain","author":"G Kempermann","year":"2006"},{"key":"ref80","doi-asserted-by":"crossref","first-page":"865","DOI":"10.1111\/j.1365-2826.2006.01482.x","article-title":"Metabolic signals modulate hypothalamic-pituitary-adrenal axis activation during maternal separation of the neonatal mouse.","volume":"18","author":"MV Schmidt","year":"2006","journal-title":"J Neuroendocrinol"},{"key":"ref81","doi-asserted-by":"crossref","first-page":"503","DOI":"10.1002\/dev.420270804","article-title":"Potentiation of isolation-induced vocalization by brief exposure of rat pups to maternal cues.","volume":"27","author":"MA Hofer","year":"1994","journal-title":"Dev Psychobiol"},{"key":"ref82","doi-asserted-by":"crossref","first-page":"677","DOI":"10.1037\/h0077599","article-title":"Mother rats interact differently with male and female offspring.","volume":"93","author":"CL Moore","year":"1979","journal-title":"J Comp Physiol Psychol"},{"key":"ref83","doi-asserted-by":"crossref","first-page":"1659","DOI":"10.1126\/science.277.5332.1659","article-title":"Maternal care, hippocampal glucocorticoid receptors, and hypothalamic-pituitary-adrenal responses to stress.","volume":"277","author":"D Liu","year":"1997","journal-title":"Science"},{"key":"ref84","doi-asserted-by":"crossref","first-page":"239","DOI":"10.1002\/dev.1018","article-title":"Comparison of the effects of early handling and early deprivation on maternal care in the rat.","volume":"38","author":"CR Pryce","year":"2001","journal-title":"Dev Psychobiol"},{"key":"ref85","doi-asserted-by":"crossref","first-page":"359","DOI":"10.1016\/S0031-9384(03)00149-5","article-title":"Variations in maternal care in the rat as a mediating influence for the effects of environment on development.","volume":"79","author":"FA Champagne","year":"2003","journal-title":"Physiol Behav"},{"key":"ref86","doi-asserted-by":"crossref","first-page":"361","DOI":"10.1016\/S0197-4580(03)00090-3","article-title":"Prominent decline of newborn cell proliferation, differentiation, and apoptosis in the aging dentate gyrus, in absence of an age-related hypothalamus-pituitary-adrenal axis activation.","volume":"25","author":"VM Heine","year":"2004","journal-title":"Neurobiol Aging"},{"key":"ref87","doi-asserted-by":"crossref","first-page":"149","DOI":"10.1002\/cne.901590202","article-title":"An autoradiographic study of the time of origin and the pattern of granule cell migration in the dentate gyrus of the rat.","volume":"159","author":"AR Schlessinger","year":"1975","journal-title":"J Comp Neurol"},{"key":"ref88","article-title":"Prenatal stress reduces postnatal neurogenesis in rats selectively bred for heigh, but not low anxiety: possible key role of induction of placental 11B-hydroxysteroid dehydrogenase type 2.","author":"PJ Lucassen","year":"2008","journal-title":"Eur J Neurosci"},{"key":"ref89","doi-asserted-by":"crossref","first-page":"497","DOI":"10.1111\/j.1750-3639.2008.00149.x","article-title":"No long-term effect two years after intrauterine exposure to dexamethasone on dentate gyrus volume, neuronal proliferation and differentiation in common marmoset monkeys.","volume":"18","author":"SC Tauber","year":"2008","journal-title":"Brain Pathol"},{"key":"ref90","doi-asserted-by":"crossref","first-page":"3943","DOI":"10.1523\/JNEUROSCI.16-12-03943.1996","article-title":"Maternal glucocorticoid secretion mediates long-term effects of prenatal stress.","volume":"16","author":"A Barbazanges","year":"1996","journal-title":"J Neurosci"},{"key":"ref91","doi-asserted-by":"crossref","first-page":"353","DOI":"10.1016\/S0031-9384(00)00351-6","article-title":"Prenatal stress in rats: effects on plasma corticosterone, hippocampal glucocorticoid receptors, and maze performance.","volume":"71","author":"TF Szuran","year":"2000","journal-title":"Physiol Behav"},{"key":"ref92","doi-asserted-by":"crossref","first-page":"22","DOI":"10.1016\/S0006-8993(03)02542-3","article-title":"Sex differences in cell proliferation, cell death and defensive behavior following acute predator odor stress in adult rats.","volume":"975","author":"EM Falconer","year":"2003","journal-title":"Brain Res"},{"key":"ref93","doi-asserted-by":"crossref","first-page":"1845","DOI":"10.1111\/j.1460-9568.2006.05061.x","article-title":"Endocannabinoids modulate stress-induced suppression of hippocampal cell proliferation and activation of defensive behaviours.","volume":"24","author":"MN Hill","year":"2006","journal-title":"Eur J Neurosci"},{"key":"ref94","doi-asserted-by":"crossref","first-page":"1562","DOI":"10.1038\/sj.npp.1300234","article-title":"Cell proliferation in adult hippocampus is decreased by inescapable stress: reversal by fluoxetine treatment.","volume":"28","author":"JE Malberg","year":"2003","journal-title":"Neuropsychopharmacology"},{"key":"ref95","doi-asserted-by":"crossref","first-page":"40","DOI":"10.1016\/j.neulet.2004.07.062","article-title":"Chronic non-invasive glucocorticoid administration decreases polysialylated neural cell adhesion molecule expression in the adult rat dentate gyrus.","volume":"370","author":"J Nacher","year":"2004","journal-title":"Neurosci Lett"},{"key":"ref96","doi-asserted-by":"crossref","first-page":"2734","DOI":"10.1523\/JNEUROSCI.3849-06.2007","article-title":"Acute psychosocial stress reduces cell survival in adult hippocampal neurogenesis without altering proliferation.","volume":"27","author":"RM Thomas","year":"2007","journal-title":"J Neurosci"},{"key":"ref97","doi-asserted-by":"crossref","first-page":"308","DOI":"10.1016\/j.expneurol.2006.04.010","article-title":"Acute exposure to predator odor elicits a robust increase in corticosterone and a decrease in activity without altering proliferation in the adult rat hippocampus.","volume":"201","author":"RM Thomas","year":"2006","journal-title":"Exp Neurol"},{"key":"ref98","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1016\/S0031-9384(03)00100-8","article-title":"A spoonful of sugar: feedback signals of energy stores and corticosterone regulate responses to chronic stress.","volume":"79","author":"MF Dallman","year":"2003","journal-title":"Physiol Behav"},{"key":"ref99","doi-asserted-by":"crossref","first-page":"530","DOI":"10.1016\/j.neuropharm.2007.11.009","article-title":"The number of granule cells in rat hippocampus is reduced after chronic mild stress and re-established after chronic escitalopram treatment.","volume":"54","author":"MN Jayatissa","year":"2008","journal-title":"Neuropharmacology"},{"key":"ref100","doi-asserted-by":"crossref","first-page":"955","DOI":"10.1016\/S0306-4522(98)00345-5","article-title":"Sex and seasonal differences in the rate of cell proliferation in the dentate gyrus of adult wild meadow voles.","volume":"89","author":"LA Galea","year":"1999","journal-title":"Neuroscience"},{"key":"ref101","doi-asserted-by":"crossref","first-page":"225","DOI":"10.1002\/hipo.20154","article-title":"Gonadal hormone modulation of hippocampal neurogenesis in the adult.","volume":"16","author":"LA Galea","year":"2006","journal-title":"Hippocampus"},{"key":"ref102","doi-asserted-by":"crossref","first-page":"3316","DOI":"10.1523\/JNEUROSCI.19-09-03316.1999","article-title":"Granule cells in aging rats are sexually dimorphic in their response to estradiol.","volume":"19","author":"P Miranda","year":"1999","journal-title":"J Neurosci"},{"key":"ref103","doi-asserted-by":"crossref","first-page":"6292","DOI":"10.1523\/JNEUROSCI.21-16-06292.2001","article-title":"Sex differences and opposite effects of stress on dendritic spine density in the male versus female hippocampus.","volume":"21","author":"TJ Shors","year":"2001","journal-title":"J Neurosci"},{"key":"ref104","doi-asserted-by":"crossref","first-page":"117","DOI":"10.1016\/j.bbr.2006.10.029","article-title":"Influence of gender on working and spatial memory in the novel object recognition task in the rat.","volume":"177","author":"JS Sutcliffe","year":"2007","journal-title":"Behav Brain Res"},{"key":"ref105","doi-asserted-by":"crossref","first-page":"5792","DOI":"10.1523\/JNEUROSCI.19-14-05792.1999","article-title":"Estrogen stimulates a transient increase in the number of new neurons in the dentate gyrus of the adult female rat.","volume":"19","author":"P Tanapat","year":"1999","journal-title":"J Neurosci"},{"key":"ref106","doi-asserted-by":"crossref","first-page":"303","DOI":"10.1016\/j.brainresbull.2004.08.006","article-title":"Chronic stress and social housing differentially affect neurogenesis in male and female rats.","volume":"64","author":"C Westenbroek","year":"2004","journal-title":"Brain Res Bull"},{"key":"ref107","doi-asserted-by":"crossref","first-page":"332","DOI":"10.1016\/j.brainresrev.2007.05.008","article-title":"Gonadal hormone modulation of neurogenesis in the dentate gyrus of adult male and female rodents.","volume":"57","author":"LA Galea","year":"2008","journal-title":"Brain Res Rev"},{"key":"ref108","doi-asserted-by":"crossref","first-page":"569","DOI":"10.1146\/annurev.pharmtox.41.1.569","article-title":"Neurotrophic and neuroprotective actions of estrogens and their therapeutic implications.","volume":"41","author":"SJ Lee","year":"2001","journal-title":"Annu Rev Pharmacol Toxicol"},{"key":"ref109","doi-asserted-by":"crossref","first-page":"185","DOI":"10.3109\/10253890009001122","article-title":"Androgens are neuroprotective in the dentate gyrus of adrenalectomized female rats.","volume":"3","author":"CA Frye","year":"2000","journal-title":"Stress"},{"key":"ref110","doi-asserted-by":"crossref","first-page":"357","DOI":"10.1016\/0006-8993(88)90239-9","article-title":"The distribution of glial fibrillary acidic protein in the adult rat brain is influenced by the neonatal levels of sex steroids.","volume":"456","author":"LM Garcia-Segura","year":"1988","journal-title":"Brain Res"},{"key":"ref111","doi-asserted-by":"crossref","first-page":"1334","DOI":"10.1002\/dneu.20666","article-title":"Gender-dependent cellular and biochemical effects of maternal deprivation on the hippocampus of neonatal rats: A possible role for the endocannabinoid system.","volume":"68","author":"R Llorente","year":"2008","journal-title":"Dev Neurobiol"},{"key":"ref112","doi-asserted-by":"crossref","first-page":"30","DOI":"10.1016\/S0006-8993(02)03475-3","article-title":"Age and gender effects on microglia and astrocyte numbers in brains of mice.","volume":"956","author":"PR Mouton","year":"2002","journal-title":"Brain Res"},{"key":"ref113","doi-asserted-by":"crossref","first-page":"488","DOI":"10.1002\/jnr.20372","article-title":"Influence of gonadal steroids on the glial fibrillary acidic protein-immunoreactive astrocyte population in young rat hippocampus.","volume":"79","author":"NM Conejo","year":"2005","journal-title":"J Neurosci Res"},{"key":"ref114","doi-asserted-by":"crossref","first-page":"41","DOI":"10.1002\/glia.10337","article-title":"Differential regulation of gliogenesis in the context of adult hippocampal neurogenesis in mice.","volume":"46","author":"B Steiner","year":"2004","journal-title":"Glia"},{"key":"ref115","doi-asserted-by":"crossref","first-page":"234","DOI":"10.1111\/j.0953-816X.2003.03123.x","article-title":"Efficacy of doublecortin as a marker to analyse the absolute number and dendritic growth of newly generated neurons in the adult dentate gyrus.","volume":"19","author":"MS Rao","year":"2004","journal-title":"Eur J Neurosci"},{"key":"ref116","doi-asserted-by":"crossref","first-page":"603","DOI":"10.1016\/S1044-7431(03)00207-0","article-title":"Transient calretinin expression defines early postmitotic step of neuronal differentiation in adult hippocampal neurogenesis of mice.","volume":"24","author":"MD Brandt","year":"2003","journal-title":"Mol Cell Neurosci"},{"key":"ref117","doi-asserted-by":"crossref","first-page":"6037","DOI":"10.1523\/JNEUROSCI.0526-08.2008","article-title":"Maternal care and hippocampal plasticity: evidence for experience-dependent structural plasticity, altered synaptic functioning, and differential responsiveness to glucocorticoids and stress.","volume":"28","author":"DL Champagne","year":"2008","journal-title":"J Neurosci"},{"key":"ref118","doi-asserted-by":"crossref","first-page":"46","DOI":"10.1016\/j.brainres.2006.08.084","article-title":"Extranuclear estrogen receptor beta immunoreactivity is on doublecortin-containing cells in the adult and neonatal rat dentate gyrus.","volume":"1121","author":"SP Herrick","year":"2006","journal-title":"Brain Res"},{"key":"ref119","doi-asserted-by":"crossref","first-page":"1321","DOI":"10.1002\/dneu.20457","article-title":"Testosterone and dihydrotestosterone, but not estradiol, enhance survival of new hippocampal neurons in adult male rats.","volume":"67","author":"MD Spritzer","year":"2007","journal-title":"Dev Neurobiol"},{"key":"ref120","doi-asserted-by":"crossref","first-page":"156","DOI":"10.1016\/0165-3806(95)00213-8","article-title":"Long-term effects of neonatal maternal deprivation and ACTH on hippocampal mineralocorticoid and glucocorticoid receptors.","volume":"92","author":"W Sutanto","year":"1996","journal-title":"Brain Res Dev Brain Res"},{"key":"ref121","doi-asserted-by":"crossref","first-page":"363","DOI":"10.1111\/j.1474-9728.2004.00130.x","article-title":"Age-dependent expression of glucocorticoid- and mineralocorticoid receptors on neural precursor cell populations in the adult murine hippocampus.","volume":"3","author":"A Garcia","year":"2004","journal-title":"Aging Cell"},{"key":"ref122","doi-asserted-by":"crossref","first-page":"184","DOI":"10.1038\/nature02553","article-title":"Enhanced synaptic plasticity in newly generated granule cells of the adult hippocampus.","volume":"429","author":"C Schmidt-Hieber","year":"2004","journal-title":"Nature"},{"key":"ref123","article-title":"Chronic stress; implications for neuron morphology, function and neurogenesis.","author":"M Joels","year":"2007","journal-title":"Frontiers in Neuroendocrinology"}],"container-title":["PLoS ONE"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/dx.plos.org\/10.1371\/journal.pone.0003675","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,3,9]],"date-time":"2024-03-09T17:35:17Z","timestamp":1710005717000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pone.0003675"}},"subtitle":[],"editor":[{"given":"Bernhard","family":"Baune","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"editor"}]}],"short-title":[],"issued":{"date-parts":[[2009,1,29]]},"references-count":123,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2009,1,29]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pone.0003675","relation":{},"ISSN":["1932-6203"],"issn-type":[{"value":"1932-6203","type":"electronic"}],"subject":[],"published":{"date-parts":[[2009,1,29]]}}}