Cited by 190Neurogenesis and neuroplasticity mechanismsStress Responses and CortisolMaternal Mental Health During Pregnancy and Postpartum

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Opposite Effects of Early Maternal Deprivation on Neurogenesis in Male versus Female Rats

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Oomen, Charlotte A., Girardi, Carlos E. N., Cahyadi, Rudy, Verbeek, Eva C., Krugers, Harm, Joëls, Marian, Lucassen, Paul J.·2009·PLoS ONE

DOI 10.1371/journal.pone.0003675PMC PMC2629844

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Abstract

BACKGROUND: Major depression is more prevalent in women than in men. The underlying neurobiological mechanisms are not well understood, but recent data shows that hippocampal volume reductions in depressed women occur only when depression is preceded by an early life stressor. This underlines the potential importance of early life stress, at least in women, for the vulnerability to develop depression. Perinatal stress exposure in rodents affects critical periods of brain development that persistently alter structural, emotional and neuroendocrine parameters in adult offspring. Moreover, stress inhibits adult hippocampal neurogenesis, a form of structural plasticity that has been implicated a.o. in antidepressant action and is highly abundant early postnatally. We here tested the hypothesis that early life stress differentially affects hippocampal structural plasticity in female versus male offspring. PRINCIPAL FINDINGS: We show that 24 h of maternal deprivation (MD) at PND3 affects hippocampal structural plasticity at PND21 in a sex-dependent manner. Neurogenesis was significantly increased in male but decreased in female offspring after MD. Since no other structural changes were found in granule cell layer volume, newborn cell survival or proliferation rate, astrocyte number or gliogenesis, this indicates that MD elicits specific changes in subsets of differentiating cells and differentially affects immature neurons. The MD induced sex-specific effects on neurogenesis cannot be explained by differences in maternal care. CONCLUSIONS: Our data shows that early environment has a critical influence on establishing sex differences in neural plasticity and supports the concept that the setpoint for neurogenesis may be determined during perinatal life. It is tempting to speculate that a reduced level of neurogenesis, secondary to early stress exposure, may contribute to maladaptation of the HPA axis and possibly to the increased vulnerability of women to stress-related disorders.

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Developments of a water-maze procedure for studying spatial learning in the rat
Morris, R. (1984) · Journal of Neuroscience Methods · doi:10.1016/0165-0270(84)90007-4 · Cited by 7,180
Stress and the brain: from adaptation to disease
de Kloet, E. R., Joëls, M., & Holsboer, F. (2005) · Nature Reviews Neuroscience · doi:10.1038/nrn1683 · Cited by 4,621
Self-citation
Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants
Santarelli, L., Saxe, M., Gross, C., Surget, A., Battaglia, F., Dulawa, S., Weisstaub, N., Lee, J., Duman, R., Arancio, O., et al. (2003) · Science · doi:10.1126/science.1083328 · Cited by 4,321
Maternal Care, Hippocampal Glucocorticoid Receptors, and Hypothalamic-Pituitary-Adrenal Responses to Stress
Liu, D., Diorio, J., Tannenbaum, B., Caldji, C., Francis, D., Freedman, A., Sharma, S., Pearson, D., Plotsky, P. M., & Meaney, M. J. (1997) · Science · doi:10.1126/science.277.5332.1659 · Cited by 3,170
The role of childhood trauma in the neurobiology of mood and anxiety disorders: preclinical and clinical studies
Heim, C., & Nemeroff, C. B. (2001) · Biological Psychiatry · doi:10.1016/s0006-3223(01)01157-x · Cited by 2,791
Sex and depression in the National Comorbidity Survey, I: lifetime prevalence, chronicity and recurrence
Kessler, R. (1993) · Journal of Affective Disorders · doi:10.1016/0165-0327(93)90026-g · Cited by 2,207
The Corticosteroid Receptor Hypothesis of Depression
Holsboer, F. (2000) · Neuropsychopharmacology · doi:10.1016/s0893-133x(00)00159-7 · Cited by 2,181
Pituitary-adrenal and autonomic responses to stress in women after sexual and physical abuse in childhood
Heim, C. (2000) · JAMA · doi:10.1001/jama.284.5.592 · Cited by 1,968
Early, postnatal experience alters hypothalamic corticotropin-releasing factor (CRF) mRNA, median eminence CRF content and stress-induced release in adult rats
Plotsky, P. M., & Meaney, M. J. (1993) · Molecular Brain Research · doi:10.1016/0169-328x(93)90189-v · Cited by 1,638 · cited 2×
“Also, stress-induced ACTH [59,61] and corticosterone responses were increased in 24 h MD rats [53,60] while similar patterns are found in repeated separation paradigms [56,62–65].”
Background
Smaller hippocampal volume predicts pathologic vulnerability to psychological trauma
Gilbertson, M. W., Shenton, M. E., Ciszewski, A., Kasai, K., Lasko, N. B., Orr, S. P., & Pitman, R. K. (2002) · Nature Neuroscience · doi:10.1038/nn958 · Cited by 1,635
Neurogenesis in the Dentate Gyrus of the Adult Tree Shrew Is Regulated by Psychosocial Stress and NMDA Receptor Activation
Gould, E., McEwen, B. S., Tanapat, P., Galea, L. A. M., & Fuchs, E. (1997) · The Journal of Neuroscience · doi:10.1523/jneurosci.17-07-02492.1997 · Cited by 1,496
Enhanced synaptic plasticity in newly generated granule cells of the adult hippocampus
Schmidt-Hieber, C., Jonas, P., & Bischofberger, J. (2004) · Nature · doi:10.1038/nature02553 · Cited by 1,292
Organization of the stress system and its dysregulation in melancholic and atypical depression: high vs low CRH/NE states
Gold, P. W., & Chrousos, G. P. (2002) · Molecular Psychiatry · doi:10.1038/sj.mp.4001032 · Cited by 1,274
Prenatal stress produces learning deficits associated with an inhibition of neurogenesis in the hippocampus
Lemaire, V., Koehl, M., Le Moal, M., & Abrous, D. N. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.20.11032 · Cited by 1,044 · cited 2×
“As the dentate gyrus of the hippocampus is largely formed postnatally [76,77], effects on neurogenesis and structural plasticity are potentially more pronounced and longer lasting when stress is applied early in life [45,78].”
Background
Variations in maternal care in the rat as a mediating influence for the effects of environment on development
Champagne, F. A., Francis, D. D., Mar, A., & Meaney, M. J. (2003) · Physiology & Behavior · doi:10.1016/s0031-9384(03)00149-5 · Cited by 1,021
Estrogen Stimulates a Transient Increase in the Number of New Neurons in the Dentate Gyrus of the Adult Female Rat
Tanapat, P., Hastings, N. B., Reeves, A. J., & Gould, E. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-14-05792.1999 · Cited by 994
Adult neurogenesis: from precursors to network and physiology
Abrous, D. N., Koehl, M., & Le Moal, M. (2005) · Physiological Reviews · doi:10.1152/physrev.00055.2003 · Cited by 971
Prenatal stress, glucocorticoids and the programming of the brain
Welberg, L. A. M., & Seckl, J. R. (2001) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2001.00601.x · Cited by 928
Preferential incorporation of adult-generated granule cells into spatial memory networks in the dentate gyrus
Kee, N., Teixeira, C. M., Wang, A. H., & Frankland, P. W. (2007) · Nature Neuroscience · doi:10.1038/nn1847 · Cited by 875
Chronic Psychosocial Stress Causes Apical Dendritic Atrophy of Hippocampal CA3 Pyramidal Neurons in Subordinate Tree Shrews
Magariños, A. M., McEwen, B. S., Flügge, G., & Fuchs, E. (1996) · The Journal of Neuroscience · doi:10.1523/jneurosci.16-10-03534.1996 · Cited by 864
Migration and distribution of two populations of hippocampal granule cell precursors during the perinatal and postnatal periods
Altman, J., & Bayer, S. A. (1990) · Journal of Comparative Neurology · doi:10.1002/cne.903010304 · Cited by 819
Cell Proliferation in Adult Hippocampus is Decreased by Inescapable Stress: Reversal by Fluoxetine Treatment
Malberg, J. E., & Duman, R. S. (2003) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300234 · Cited by 815
Childhood trauma associated with smaller hippocampal volume in women with major depression
Vythilingam, M., Heim, C., Newport, J., Miller, A. H., Anderson, E., Bronen, R., Brummer, M., Staib, L., Vermetten, E., Charney, D. S., et al. (2002) · American Journal of Psychiatry · doi:10.1176/appi.ajp.159.12.2072 · Cited by 812
Prenatal Stress Induces High Anxiety and Postnatal Handling Induces Low Anxiety in Adult Offspring: Correlation with Stress-Induced Corticosterone Secretion
Vallée, M., Mayo, W., Dellu-Hagedorn, F., Moal, M. L., Simon, H., & Maccari, S. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-07-02626.1997 · Cited by 787
An autoradiographic study of the time of origin and the pattern of granule cell migration in the dentate gyrus of the rat
Schlessinger, A. R., Cowan, W. M., & Gottlieb, D. I. (1975) · The Journal of Comparative Neurology · doi:10.1002/cne.901590202 · Cited by 731
Stress and adult neurogenesis
Mirescu, C., & Gould, E. (2006) · Hippocampus · doi:10.1002/hipo.20155 · Cited by 701
Efficacy of doublecortin as a marker to analyse the absolute number anddendritic growth of newly generated neurons in the adult dentate gyrus
Rao, M. S. R., & Shetty, A. K. (2004) · European Journal of Neuroscience · doi:10.1111/j.0953-816x.2003.03123.x · Cited by 665
Hippocampal Neurogenesis: Regulation by Stress and Antidepressants
Dranovsky, A., & Hen, R. (2006) · Biological Psychiatry · doi:10.1016/j.biopsych.2006.03.082 · Cited by 663
Maternal care and hippocampal plasticity: evidence for experience-dependent structural plasticity, altered synaptic functioning, and differential responsiveness to glucocorticoids and stress
Champagne, D. L., Bagot, R. C., van Hasselt, F., Ramakers, G., Meaney, M. J., de Kloet, E. R., Joels, M., & Krugers, H. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.0526-08.2008 · Cited by 661
Self-citation
Repeated restraint stress suppresses neurogenesis and induces biphasic PSA‐NCAM expression in the adult rat dentate gyrus
Pham, K., Nacher, J., Hof, P. R., & McEwen, B. S. (2003) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2003.02513.x · Cited by 657
Maternal Glucocorticoid Secretion Mediates Long-Term Effects of Prenatal Stress
Barbazanges, A., Piazza, P., le Moal, M., & Maccari, S. (1996) · Journal of Neuroscience · doi:10.1523/jneurosci.16-12-03943.1996 · Cited by 655
Early life experience alters response of adult neurogenesis to stress
Mirescu, C., Peters, J. D., & Gould, E. (2004) · Nature Neuroscience · doi:10.1038/nn1290 · Cited by 625
Drug Transporters in the Central Nervous System: Brain Barriers and Brain Parenchyma Considerations
Lee, G. S., Dallas, S., Hong, M., & Bendayan, R. (2001) · Pharmacological Reviews · doi:10.1016/s0031-6997(24)01513-8 · Cited by 547
Is there a link between adult neurogenesis and learning?
Leuner, B., Gould, E., & Shors, T. J. (2006) · Hippocampus · doi:10.1002/hipo.20153 · Cited by 543
Chronic stress alters synaptic terminal structure in hippocampus
Magariños, A. M., Verdugo, J. M. G., & McEwen, B. S. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.25.14002 · Cited by 543
Persistent changes in corticotropin-releasing factor neuronal systems induced by maternal deprivation.
Ladd, C. O., Owens, M. J., & Nemeroff, C. (1996) · Endocrinology · doi:10.1210/endo.137.4.8625891 · Cited by 536
Neurotrophic and Neuroprotective Actions of Estrogens and Their Therapeutic Implications
Lee, S. H., & McEwen, B. S. (2001) · The Annual Review of Pharmacology and Toxicology · doi:10.1146/annurev.pharmtox.41.1.569 · Cited by 533
Prenatal Stress Increases the Hypothalamo‐Pituitary‐Adrenal Axis Response in Young and Adult Rats
Henry, C., Kabbaj, M., Simon, H., Moal, M. L., & Maccari, S. (1994) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.1994.tb00591.x · Cited by 528
Long term consequences of neonatal rearing on central corticotropin-releasing factor systems in adult male rat offspring
Plotsky, P. M., Thrivikraman, K. V., Nemeroff, C. B., Caldji, C., Sharma, S., & Meaney, M. J. (2005) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300769 · Cited by 522
Childhood sexual abuse as a risk factor for depression in women: Psychosocial and neurobiological correlates
Weiss, E. L., Longhurst, J. G., & Mazure, C. M. (1999) · American Journal of Psychiatry · doi:10.1176/ajp.156.6.816 · Cited by 517
Transient calretinin expression defines early postmitotic step of neuronal differentiation in adult hippocampal neurogenesis of mice
Brandt, M., Jessberger, S., Steiner, B., Kronenberg, G., Reuter, K., Bick‐Sander, A., von der Behrens, W., & Kempermann, G. (2003) · Molecular and Cellular Neuroscience · doi:10.1016/s1044-7431(03)00207-0 · Cited by 510
Sex Differences and Opposite Effects of Stress on Dendritic Spine Density in the Male Versus Female Hippocampus
Shors, T. J., Chua, C., & Falduto, J. (2001) · The Journal of Neuroscience · doi:10.1523/jneurosci.21-16-06292.2001 · Cited by 496
Long-lasting changes in stress-induced corticosterone response and anxiety-like behaviors as a consequence of neonatal maternal separation in Long–Evans rats
Kalinichev, M., Easterling, K. W., Plotsky, P. M., & Holtzman, S. G. (2002) · Pharmacology Biochemistry and Behavior · doi:10.1016/s0091-3057(02)00781-5 · Cited by 484
Mechanisms of late-onset cognitive decline after early-life stress
Brunson, K. L., Kramár, E., Lin, B., Chen, Y., Colgin, L. L., Yanagihara, T. K., Lynch, G., & Baram, T. Z. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.2281-05.2005 · Cited by 479
Prenatal stress diminishes neurogenesis in the dentate gyrus of juvenile rhesus monkeys
Coe, C. L., Kramer, M., Czéh, B., Gould, E., Reeves, A. J., Kirschbaum, C., & Fuchs, E. (2003) · Biological Psychiatry · doi:10.1016/s0006-3223(03)00698-x · Cited by 477
Long-term neurobehavioural impact of the postnatal environment in rats: manipulations, effects and mediating mechanisms
Pryce, C. R., & Feldon, J. (2003) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(03)00009-5 · Cited by 467
Influence of Neonatal Rearing Conditions on Stress‐Induced Adrenocorticotropin Responses and Norepinepherine Release in the Hypothalamic Paraventricular Nucleus
Liu, Caldji, Sharma, Plotsky, & Meaney (2000) · Journal of Neuroendocrinology · doi:10.1046/j.1365-2826.2000.00422.x · Cited by 456
Periodic Maternal Deprivation Induces Gender-Dependent Alterations in Behavioral and Neuroendocrine Responses to Emotional Stress in Adult Rats
Wigger, A., & Neumann, I. D. (1999) · Physiology & Behavior · doi:10.1016/s0031-9384(98)00300-x · Cited by 443
Astroglial Plasticity in the Hippocampus is Affected by Chronic Psychosocial Stress and Concomitant Fluoxetine Treatment
Czéh, B., Simon, M., Schmelting, B., Hiemke, C., & Fuchs, E. (2006) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300982 · Cited by 434
Epigenetic programming of the stress response in male and female rats by prenatal restraint stress
Darnaudéry, M., & Maccari, S. (2008) · Brain Research Reviews · doi:10.1016/j.brainresrev.2007.11.004 · Cited by 412
Spatial Learning Depends on Both the Addition and Removal of New Hippocampal Neurons
Dupret, D., Fabre, A., Döbrössy, M. D., Panatier, A., Rodriguez, J. J., Lamarque, S., Lemaire, V., Oliet, S. H. R., Piazza, P., & Abrous, D. N. (2007) · PLoS Biology · doi:10.1371/journal.pbio.0050214 · Cited by 410
Mosaic organization of the hippocampal neuroepithelium and the multiple germinal sources of dentate granule cells
Altman, J., & Bayer, S. A. (1990) · The Journal of Comparative Neurology · doi:10.1002/cne.903010302 · Cited by 401
Neonatal maternal separation reduces hippocampal mossy fiber density in adult Long Evans rats
Huot, R. L., Plotsky, P. M., Lenox, R. H., & McNamara, R. K. (2002) · Brain Research · doi:10.1016/s0006-8993(02)02985-2 · Cited by 392
Chronic stress: Implications for neuronal morphology, function and neurogenesis
Joëls, M., Karst, H., Krugers, H. J., & Lucassen, P. J. (2007) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2007.04.001 · Cited by 381
Self-citation
Mother rats interact differently with male amd female offspring.
Moore, C. L., & Morelli, G. A. (1979) · Journal of Comparative and Physiological Psychology · doi:10.1037/h0077599 · Cited by 353
Gender Differences in the Effects of Prenatal Stress on Brain Development and Behaviour
Weinstock, M. (2007) · Neurochemical Research · doi:10.1007/s11064-007-9339-4 · Cited by 349
The Ontogeny of the Hypothalamic‐Pituitary‐Adrenal Axis. The Influence of Maternal Factorsa
Levine, S. D. (1994) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1994.tb39245.x · Cited by 343
Differential regulation of gliogenesis in the context of adult hippocampal neurogenesis in mice
Steiner, B., Kronenberg, G., Jessberger, S., Brandt, M., Reuter, K., & Kempermann, G. (2004) · Glia · doi:10.1002/glia.10337 · Cited by 337
The role of prenatal stress in the etiology of developmental behavioural disorders
Kofman, O. (2002) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(02)00015-5 · Cited by 337
An open label trial of C-1073 (mifepristone) for psychotic major depression*
Belanoff, J. K., Rothschild, A. J., Cassidy, F., DeBattista, C., Baulieu, E.-E., Schold, C., & Schatzberg, A. F. (2002) · Biological Psychiatry · doi:10.1016/s0006-3223(02)01432-4 · Cited by 320
Age and gender effects on microglia and astrocyte numbers in brains of mice
Mouton, P. R., Long, J. M., Lei, D.-L., Howard, V., Jucker, M., Calhoun, M. E., & Ingram, D. K. (2002) · Brain Research · doi:10.1016/s0006-8993(02)03475-3 · Cited by 320
Agomelatine, a new antidepressant, induces regional changes in hippocampal neurogenesis
Banasr, M., Soumier, A., Hery, M., Mocaër, E., & Daszuta, A. (2006) · Biological Psychiatry · doi:10.1016/j.biopsych.2005.11.025 · Cited by 318
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
Heine, V. M., Maslam, S., Joëls, M., & Lucassen, P. J. (2004) · Neurobiology of Aging · doi:10.1016/s0197-4580(03)00090-3 · Cited by 318
Self-citation
Suppressed proliferation and apoptotic changes in the rat dentate gyrus after acute and chronic stress are reversible
Heine, V. M., Maslam, S., Zareno, J., Joëls, M., & Lucassen, P. J. (2004) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2003.03100.x · Cited by 317
Self-citation
Ontogeny of the Stress Response in the Rat: Role of the Pituitary and the Hypothalamus*
Walker, C., Perrin, M. H., Vale, W., & RIVIER, C. L. (1986) · Endocrinology · doi:10.1210/endo-118-4-1445 · Cited by 309
Rapid Reversal of Psychotic Depression Using Mifepristone
Belanoff, J. K., Flores, B. H., Kalezhan, M., Sund, B., & Schatzberg, A. F. (2001) · Journal of Clinical Psychopharmacology · doi:10.1097/00004714-200110000-00009 · Cited by 282
Sex and seasonal changes in the rate of cell proliferation in the dentate gyrus of adult wild meadow voles
Galea, L. A. M., & McEwen, B. S. (1999) · Neuroscience · doi:10.1016/s0306-4522(98)00345-5 · Cited by 281
Comparison of the effects of early handling and early deprivation on maternal care in the rat
Pryce, C. R., Rüedi‐Bettschen, D., & Feldon, J. (2001) · Developmental Psychobiology · doi:10.1002/dev.1018 · Cited by 280
Testosterone and dihydrotestosterone, but not estradiol, enhance survival of new hippocampal neurons in adult male rats
Spritzer, M. D., & Galea, L. A. M. (2007) · Developmental Neurobiology · doi:10.1002/dneu.20457 · Cited by 277
Differential effects of learning on neurogenesis: learning increases or decreases the number of newly born cells depending on their birth date
Döbrössy, M. D., Drapeau, E., Aurousseau, C., Moal, M. L., Piazza, P. V., & Abrous, D. N. (2003) · Molecular Psychiatry · doi:10.1038/sj.mp.4001419 · Cited by 266
Gonadal hormone modulation of neurogenesis in the dentate gyrus of adult male and female rodents
Galea, L. A. M. (2007) · Brain Research Reviews · doi:10.1016/j.brainresrev.2007.05.008 · Cited by 260
Prenatal stress in rats: effects on plasma corticosterone, hippocampal glucocorticoid receptors, and maze performance
Szuran, T. F., Pliška, V., Pokorny, J., & Welzl, H. (2000) · Physiology & Behavior · doi:10.1016/s0031-9384(00)00351-6 · Cited by 253
Chronic stress and social housing differentially affect neurogenesis in male and female rats
Westenbroek, C., den Boer, J. A., Veenhuis, M., & Horst, G. J. T. (2004) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2004.08.006 · Cited by 249
Acute Psychosocial Stress Reduces Cell Survival in Adult Hippocampal Neurogenesis without Altering Proliferation
Thomas, R. M., Hotsenpiller, G., & Peterson, D. A. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.3849-06.2007 · Cited by 245
Dissociation in the effects of neonatal maternal separations on maternal care and the offspring's HPA and fear responses in rats
Macrı̀, S., Mason, G. J., & Würbel, H. (2004) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2004.03541.x · Cited by 245
Influence of gender on working and spatial memory in the novel object recognition task in the rat
Sutcliffe, J., Marshall, K. M., & Neill, J. C. (2006) · Behavioural Brain Research · doi:10.1016/j.bbr.2006.10.029 · Cited by 239
Gonadal hormone modulation of hippocampal neurogenesis in the adult
Galea, L. A. M., Spritzer, M. D., Barker, J. M., & Pawluski, J. L. (2006) · Hippocampus · doi:10.1002/hipo.20154 · Cited by 238
Brief treatment with the glucocorticoid receptor antagonist mifepristone normalizes the reduction in neurogenesis after chronic stress
Oomen, C. A., Mayer, J. L., de Kloet, E. R., Joëls, M., & Lucassen, P. J. (2007) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2007.05972.x · Cited by 237
Self-citation
Role of the ventral subiculum in stress integration
Herman, J. P., & Mueller, N. K. (2006) · Behavioural Brain Research · doi:10.1016/j.bbr.2006.05.035 · Cited by 235
Hippocampal neuroplasticity induced by early-life stress: Functional and molecular aspects
Fenoglio, K. A., Brunson, K. L., & Baram, T. (2006) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2006.02.001 · Cited by 224
Age‐dependent expression of glucocorticoid‐ and mineralocorticoid receptors on neural precursor cell populations in the adult murine hippocampus
Garcia, A. D. R., Steiner, B., Kronenberg, G., Bick‐Sander, A., & Kempermann, G. (2004) · Aging Cell · doi:10.1111/j.1474-9728.2004.00130.x · Cited by 213
Postnatal stimulation of the pups counteracts prenatal stress-induced deficits in hippocampal neurogenesis
Lemaire, V., Lamarque, S., Le Moal, M., Piazza, P.-V., & Abrous, D. N. (2006) · Biological Psychiatry · doi:10.1016/j.biopsych.2005.11.009 · Cited by 211
Maternal care influences neuronal survival in the hippocampus of the rat
Bredy, T. W., Grant, R. J., Champagne, D. L., & Meaney, M. J. (2003) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2003.02965.x · Cited by 209
The Effects of Early Shock and Handling on Later Avoidance Learning1
Levine, S., Chevalier, J. A., & Korchin, S. J. (1956) · Journal of Personality · doi:10.1111/j.1467-6494.1956.tb01283.x · Cited by 206
Raised circulating corticosterone inhibits neuronal differentiation of progenitor cells in the adult hippocampus
Wong, E. Y. H., & Herbert, J. (2005) · Neuroscience · doi:10.1016/j.neuroscience.2005.08.073 · Cited by 205
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
Brummelte, S., Pawluski, J. L., & Galea, L. A. M. (2006) · Hormones and Behavior · doi:10.1016/j.yhbeh.2006.04.008 · Cited by 199
Sex differences in cell proliferation, cell death and defensive behavior following acute predator odor stress in adult rats
Falconer, E. M., & Galea, L. A. M. (2003) · Brain Research · doi:10.1016/s0006-8993(03)02542-3 · Cited by 197
Brief Treatment With the Glucocorticoid Receptor Antagonist Mifepristone Normalises the Corticosterone‐Induced Reduction of Adult Hippocampal Neurogenesis
Mayer, J. L., Klumpers, L. E., Maslam, S., de Kloet, E. R., Joëls, M., & Lucassen, P. J. (2006) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2006.01455.x · Cited by 186
Self-citation
Long-lasting changes in behavioural and neuroendocrine indices in the rat following neonatal maternal separation: Gender-dependent effects
Slotten, H. A., Kalinichev, M., Hagan, J. J., Marsden, C. A., & Fone, K. C. F. (2006) · Brain Research · doi:10.1016/j.brainres.2006.04.066 · Cited by 179
Adult Neurogenesis: Stem Cells and Neuronal Development in the Adult Brain
Kempermann, G. (2005) · Cited by 176
The impact of maternal separation on adult mouse behaviour and on the total neuron number in the mouse hippocampus
Fabricius, K., Wörtwein, G., & Pakkenberg, B. (2008) · Brain Structure and Function · doi:10.1007/s00429-007-0169-6 · Cited by 171
Epidemiology of Affective Disorders: A Review
Bland, R. C. (1997) · The Canadian Journal of Psychiatry · doi:10.1177/070674379704200403 · Cited by 153
Prenatal stress reduces postnatal neurogenesis in rats selectively bred for high, but not low, anxiety: possible key role of placental 11β‐hydroxysteroid dehydrogenase type 2
Lucassen, P. J., Bosch, O. J., Jousma, E., Krömer, S. A., Andrew, R., Seckl, J. R., & Neumann, I. D. (2008) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2008.06543.x · Cited by 140
Self-citation
Depression: reduced number of granule cells in the hippocampus of female, but not male, rats due to prenatal restraint stress
Schmitz, C., Rhodes, M. E., Bludau, M., Kaplan, S., Ong, P., Ueffing, I., Vehoff, J., Korr, H., & Frye, C. A. (2002) · Molecular Psychiatry · doi:10.1038/sj.mp.4001118 · Cited by 140
Granule Cells in Aging Rats Are Sexually Dimorphic in Their Response to Estradiol
Miranda, P. J., Williams, C. L., & Einstein, G. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-09-03316.1999 · Cited by 134
A spoonful of sugar: feedback signals of energy stores and corticosterone regulate responses to chronic stress
Dallman, M. F., Akana, S. F., Laugero, K. D., Gómez-Oliver, F., Manalo, S. L., Bell, M. E., & Bhatnagar, S. (2003) · Physiology & Behavior · doi:10.1016/s0031-9384(03)00100-8 · Cited by 129
Long-term effects of neonatal maternal deprivation and ACTH on hippocampal mineralocorticoid and glucocorticoid receptors
Sutanto, W., Rosenfeld, P., de Kloet, E. R., & Levine, S. D. (1996) · Developmental Brain Research · doi:10.1016/0165-3806(95)00213-8 · Cited by 128
Sex differences and the HPA axis: implications for psychiatric disease.
Young, E. A. (1998) · PubMed · Cited by 126
Increased adult hippocampal brain‐derived neurotrophic factor and normal levels of neurogenesis in maternal separation rats
Greisen, M. H., Altar, C. A., Bolwig, T. G., Whitehead, R. E., & Wörtwein, G. (2005) · Journal of Neuroscience Research · doi:10.1002/jnr.20418 · Cited by 123
Effect of a single maternal separation at different pup ages on the corticosterone stress response in adult and aged rats
Lehmann, J., Russig, H. D., Feldon, J., & Pryce, C. R. (2002) · Pharmacology Biochemistry and Behavior · doi:10.1016/s0091-3057(02)00788-8 · Cited by 111
Acute exposure to predator odor elicits a robust increase in corticosterone and a decrease in activity without altering proliferation in the adult rat hippocampus
THOMAS, R., URBAN, J., & Peterson, D. A. (2006) · Experimental Neurology · doi:10.1016/j.expneurol.2006.04.010 · Cited by 105
Adult Neurogenesis: Stem cells and neuronal development in the adult brain
Jellinger, K. A. (2007) · European Journal of Neurology · doi:10.1111/j.1468-1331.2007.01730.x · Cited by 104
The distribution of glial fibrillary acidic protein in the adult rat brain is influenced by the neonatal levels of sex steroids
García‐Segura, L. M., Suarez, I., Segovia, S., Tranque, P., Calés, J. M., Aguilera, P., Olmos, G., & Guillamón, A. (1988) · Brain Research · doi:10.1016/0006-8993(88)90239-9 · Cited by 102
Differential and Age‐Dependent Effects of Maternal Deprivation on the Hypothalamic‐Pituitary‐Adrenal Axis of Brown Norway Rats from Youth to Senescence
Workel, J. O., Oitzl, M. S., Fluttert, M., Lesscher, H. M. B., Karssen, A. M., & de Kloet, E. R. (2001) · Journal of Neuroendocrinology · doi:10.1046/j.1365-2826.2001.00668.x · Cited by 102
Endocannabinoids modulate stress‐induced suppression of hippocampal cell proliferation and activation of defensive behaviours
Hill, M. N., Kambo, J. S., Sun, J. C., Gorzalka, B. B., & Galea, L. A. M. (2006) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2006.05061.x · Cited by 101
Sexually dimorphic effects of maternal separation stress on corticotrophin‐releasing factor and vasopressin systems in the adult rat brain
Desbonnet, L., Garrett, L., Daly, E., McDermott, K. W. G., & Dinan, T. G. (2008) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2008.02.004 · Cited by 98
Stress experienced in utero reduces sexual dichotomies in neurogenesis, microenvironment, and cell death in the adult rat hippocampus
Mandyam, C. D., Crawford, E. F., Eisch, A. J., RIVIER, C. L., & Richardson, H. N. (2008) · Developmental Neurobiology · doi:10.1002/dneu.20600 · Cited by 93
The number of granule cells in rat hippocampus is reduced after chronic mild stress and re-established after chronic escitalopram treatment
Jayatissa, M. N., Bisgaard, C. F., West, M. J., & Wiborg, O. (2007) · Neuropharmacology · doi:10.1016/j.neuropharm.2007.11.009 · Cited by 93
Metabolic Signals Modulate Hypothalamic‐Pituitary‐Adrenal Axis Activation During Maternal Separation of the Neonatal Mouse
Schmidt, M. V., Levine, S. D., Alam, S., Harbich, D., Sterlemann, V., Ganea, K., de Kloet, E. R., Holsboer, F., & Müller, M. B. (2006) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2006.01482.x · Cited by 93
Impaired Recognition of the Goal Location during Spatial Navigation in Rats with Hippocampal Lesions
Hollup, S., Kjelstrup, K. B., Hoff, J., Moser, M., & Moser, E. I. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-12-04505.2001 · Cited by 91
Potentiation of isolation‐induced vocalization by brief exposure of rat pups to maternal cues
Hofer, M. A., Brunelli, S. A., & Shair, H. N. (1994) · Developmental Psychobiology · doi:10.1002/dev.420270804 · Cited by 89
Postnatal maternal deprivation produces long‐lasting modifications of the stress response, feeding and stress‐related behaviour in the rat
Penke, Z., Felszeghy, K., Fernette, B., Ciocca, D., Nyakas, C. J., & Burlet, A. J. (2001) · European Journal of Neuroscience · doi:10.1046/j.0953-816x.2001.01691.x · Cited by 88
Gender‐dependent cellular and biochemical effects of maternal deprivation on the hippocampus of neonatal rats: A possible role for the endocannabinoid system
Llorente, R., Llorente‐Berzal, A., Petrosino, S., Marco, E. M., Guaza, C., Prada, C., López‐Gallardo, M., Marzo, V. D., & Viveros, M. (2008) · Developmental Neurobiology · doi:10.1002/dneu.20666 · Cited by 85
Antiglucocorticoid drugs in the treatment of depression
Reus, V. I., & Wolkowitz, O. M. (2001) · Expert Opinion on Investigational Drugs · doi:10.1517/13543784.10.10.1789 · Cited by 82
Extranuclear estrogen receptor beta immunoreactivity is on doublecortin-containing cells in the adult and neonatal rat dentate gyrus
Herrick, S. P., Waters, E. M., Drake, C. T., McEwen, B. S., & Milner, T. A. (2006) · Brain Research · doi:10.1016/j.brainres.2006.08.084 · Cited by 77
Long term neurodevelopmental and behavioral effects of perinatal life events in rats
Koehl, M., Lemaire, V., Vallée, M., Abrous, D. N., Piazza, P. V., Mayo, W., Maccari, S., & Moal, M. L. (2001) · Neurotoxicity Research · doi:10.1007/bf03033231 · Cited by 55
Homeostatic maintenance in excitability of tree shrew hippocampal CA3 pyramidal neurons after chronic stress
Kole, M. H. P., Czéh, B., & Fuchs, E. (2004) · Hippocampus · doi:10.1002/hipo.10212 · Cited by 51
Cross-national epidemiology of depression and gender.
Üstün, T. (2001) · PubMed · Cited by 51
Influence of gonadal steroids on the glial fibrillary acidic protein‐immunoreactive astrocyte population in young rat hippocampus
Conejo, N. M., González‐Pardo, H., Cimadevilla, J. M., Argüelles, J., Díaz, F., Vallejo, G., & Árias, J. (2004) · Journal of Neuroscience Research · doi:10.1002/jnr.20372 · Cited by 49
Androgens Are Neuroprotective in the Dentate Gyrus of Adrenalectomized Female Rats
Frye, C. A., & McCormick, C. M. (2000) · Stress · doi:10.3109/10253890009001122 · Cited by 44
The Brown Norway rat displays enhanced stress-induced ACTH reactivity at day 18 after 24-h maternal deprivation at day 3
Workel, J. O., Oitzl, M. S., Ledeboer, A., & de Kloet, E. R. (1997) · Developmental Brain Research · doi:10.1016/s0165-3806(97)81796-8 · Cited by 41
Chronic non-invasive glucocorticoid administration decreases polysialylated neural cell adhesion molecule expression in the adult rat dentate gyrus
Nácher, J., Gómez‐Climent, M. Á., & McEwen, B. S. (2004) · Neuroscience Letters · doi:10.1016/j.neulet.2004.07.062 · Cited by 37
Even neural stem cells get the blues: evidence for a molecular link between modulation of adult neurogenesis and depression.
Thomas, R. M., & Peterson, D. A. (2008) · Europe PMC (PubMed Central) · Cited by 34
No Long‐Term Effect Two Years after Intrauterine Exposure to Dexamethasone on Dentate Gyrus Volume, Neuronal Proliferation and Differentiation in Common Marmoset Monkeys
Tauber, S. C., Bunkowski, S., Schlumbohm, C., Rühlmann, M., Fuchs, E., Nau, R., & Gerber, J. (2008) · Brain Pathology · doi:10.1111/j.1750-3639.2008.00149.x · Cited by 19
18 Regulation of Hippocampal Neurogenesis by Systemic Factors Including Stress, Glucocorticoids, Sleep, and Inflammation
Lucassen, P. J., Oomen, C. A., Dam, A. M., & Czéh, B. (2008) · UvA-DARE (University of Amsterdam) · doi:10.1101/087969784.52.363 · Cited by 7
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Modulation of the Hypothalamic-Pituitary-Adrenal Axis by Early Life Stress Exposure
van Bodegom, M., Homberg, J. R., & Henckens, M. J. A. G. (2017) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2017.00087 · Cited by 606
Regulation of adult neurogenesis by stress, sleep disruption, exercise and inflammation: Implications for depression and antidepressant action☆
Lucassen, P. J., Meerlo, P., Naylor, A. S., van Dam, A. M., Dayer, A. G., Fuchs, E., Oomen, C. A., & Czéh, B. (2010) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2009.08.003 · Cited by 449
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Unraveling the Time Domains of Corticosteroid Hormone Influences on Brain Activity: Rapid, Slow, and Chronic Modes
Joëls, M., Sarabdjitsingh, R. A., & Karst, H. (2012) · Pharmacological Reviews · doi:10.1124/pr.112.005892 · Cited by 445
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Chronic early life stress induced by limited bedding and nesting (LBN) material in rodents: critical considerations of methodology, outcomes and translational potential
Walker, C., Bath, K. G., Joëls, M., Kőrösi, A., Larauche, M. H., Lucassen, P. J., Morris, M. J., Raineki, C., Roth, T. L., Sullivan, R. M., et al. (2017) · Stress · doi:10.1080/10253890.2017.1343296 · Cited by 432
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Severe Early Life Stress Hampers Spatial Learning and Neurogenesis, but Improves Hippocampal Synaptic Plasticity and Emotional Learning under High-Stress Conditions in Adulthood
Oomen, C. A., Soeters, H., Audureau, N., Vermunt, L., van Hasselt, F. N., Manders, E. M. M., Joëls, M., Lucassen, P. J., & Krugers, H. J. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.0247-10.2010 · Cited by 367
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Authors: Oomen, C. A., Girardi, C. E. N., Cahyadi, R., Verbeek, E. C., Krugers, H., Joëls, M., & Lucassen, P. J.
Affiliations: University of Amsterdam (NL)
Corresponding author: Lucassen, Paul J.
ORCID: Girardi, Carlos E. N.
Verbeek, Eva C.
Krugers, Harm
Joëls, Marian
Lucassen, Paul J.
Venue: PLoS ONE
Publisher: Public Library of Science (PLoS)
Published: 2009-01-29
Volume: 4
Issue: 1
Pages: e3675
ISSN: 1932-6203 (ISSN-L)
DOI: 10.1371/journal.pone.0003675
PMC: PMC2629844
OpenAlex: W2105673253
Cited by: 190
References: 126
Citations by year: 2026: 5 · 2025: 3 · 2024: 3 · 2023: 6 · 2022: 6 · 2021: 6 · 2020: 12 · 2019: 13 · 2018: 14 · 2017: 17 · 2016: 15 · 2015: 12 · 2014: 14 · 2013: 10 · 2012: 9
FWCI: 5.54
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by
creativecommons.org/licenses/by/4.0/ (unspecified)
Locations: PLoS ONE (publishedVersion, cc-by)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
UvA-DARE (University of Amsterdam) (publishedVersion, cc-by)
UvA-DARE (University of Amsterdam) (submittedVersion, cc-by)
DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Data Archiving and Networked Services (DANS) (submittedVersion, other-oa)
Topics: Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Maternal Mental Health During Pregnancy and Postpartum
Keywords: maternal deprivation, early life stress, hippocampal neurogenesis, sex differences, structural plasticity, perinatal stress, hypothalamic-pituitary-adrenal axis, astrocytes, gliogenesis, maternal care
MeSH terms: Analysis of Variance, Animals, Animals, Newborn, Astrocytes, Behavior, Animal, Cell Differentiation, Cell Survival, Corticosterone, Female, Male, Maternal Deprivation, Neuroglia, Neuronal Plasticity, Sex Factors, Weight Loss, Rats, Wistar, Dentate Gyrus, Cell Proliferation, Rats, Neurogenesis

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Opposite Effects of Early Maternal Deprivation on Neurogenesis in Male versus Female Rats

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