Prenatal stress produces learning deficits associated with an inhibition of neurogenesis in the hippocampus

Lemaire, V.; Koehl, M.; Le Moal, M.; Abrous, D. N.

doi:10.1073/pnas.97.20.11032

Cited by 1,044Neurogenesis and neuroplasticity mechanismsMemory and Neural MechanismsStress Responses and Cortisol

Prenatal stress produces learning deficits associated with an inhibition of neurogenesis in the hippocampus

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Lemaire, V., Koehl, M., Le Moal, M., Abrous, D. N.·2000·Proceedings of the National Academy of Sciences

DOI 10.1073/pnas.97.20.11032PMC PMC27143

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Abstract

Early experiences such as prenatal stress significantly influence the development of the brain and the organization of behavior. In particular, prenatal stress impairs memory processes but the mechanism for this effect is not known. Hippocampal granule neurons are generated throughout life and are involved in hippocampal-dependent learning. Here, we report that prenatal stress in rats induced lifespan reduction of neurogenesis in the dentate gyrus and produced impairment in hippocampal-related spatial tasks. Prenatal stress blocked the increase of learning-induced neurogenesis. These data strengthen pathophysiological hypotheses that propose an early neurodevelopmental origin for psychopathological vulnerabilities in aging.

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Prenatally stressed animals repeatedly show impaired neurogenesis and related cognitive impairment.
“Impaired neurogenesis and associated cognitive impairment have been repeatedly reported in prenatally stressed animals (Lemaire et al., 2000; Fujioka et al., 2006; Lemaire et al., 2006).”
From High pregnancy anxiety during mid-gestation is associated with decreased gray matter density in 6-9-year-old children. (2010) · cites this paper as Lemaire et al., 2000
Rodent evidence indicates prenatal stress alters rat hippocampal cytoarchitecture.
“Several lines of evidence from studies in rodents indicate that the cytoarchitecture of the rat hippocampus is altered as a consequence of prenatal stress (Hayashi et al., 1998; Gould & Tanapat, 1999; Lemaire et al., 2000).”
From High pregnancy anxiety during mid-gestation is associated with decreased gray matter density in 6-9-year-old children. (2010) · cites this paper as Lemaire et al., 2000
Chronic early stress alters neural function and connectivity within and between limbic structures, especially amygdala and hippocampus, and prefrontal cortex areas.
“Several studies (Braun, Lange, Metzger, & Poeggel, 1999; Kinnunen, Keonig, & Bilbe, 2003; Lemaire, Koehl, Le Moal, & Abrous, 2000; Liu, Diorio, Day, Frances, & Meaney, 2000) have demonstrated that chronic early stress alters neural functioning and connectivity within and between limbic structures, notably the amygdala and hippocampus, associated with emotion, rapid contextually and temporally boun”
From Stress and the development of self-regulation in context (2010) · cites this paper as Lemaire, Koehl, Le Moal, & Abrous, 2000

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Structural Plasticity and Hippocampal Function
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“In both rodents and monkeys, exposure to prenatal stress results in a persistent dampening in the production of new neurons in adulthood (Coe et al. 2003, Lemaire et al. 2000).”
BackgroundInfluential
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 · see citing works
“Subjecting pregnant rats or non-human primates to stress induces long lasting reductions in adult neurogenesis in the offspring (Lemaire et al., 2000; Coe et al., 2003; Lucassen et al., 2009a,b, but see Tauber et al., 2008).”
Background
Hippocampal Dosimetry Predicts Neurocognitive Function Impairment After Fractionated Stereotactic Radiotherapy for Benign or Low-Grade Adult Brain Tumors
Gondi, V., Hermann, B. P., Mehta, M. P., & Tomé, W. A. (2013) · International Journal of Radiation Oncology*Biology*Physics · doi:10.1016/j.ijrobp.2012.11.031 · Cited by 451 · see citing works
“Preclinical evidence has associated neurogenesis within the dentate gyrus with normal cognitive function (10).”
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Prenatal stress and risk for autism
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“Prenatally stressed rats have also shown delayed learning in a task requiring spatial memory (Lemaire et al., 2000).”
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High pregnancy anxiety during mid-gestation is associated with decreased gray matter density in 6-9-year-old children.
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“Impaired neurogenesis and associated cognitive impairment have been repeatedly reported in prenatally stressed animals (Lemaire et al., 2000; Fujioka et al., 2006; Lemaire et al., 2006).”
Influential
Intracerebroventricular infusion of insulin-like growth factor-I ameliorates the age-related decline in hippocampal neurogenesis
Lichtenwalner, R. J., Forbes, M. E., Bennett, S. A., Lynch, C. D., Sonntag, W. E., & Riddle, D. R. (2001) · Neuroscience · doi:10.1016/s0306-4522(01)00378-5 · Cited by 428 · see citing works
“…indicate that it may be the ongoing replacement of granule neurons, rather than the absolute number, that is signi¢cant for hippocampal function (Lemaire et al., 2000) and that blocking the addition of new neurons in the adult dentate gyrus decreases performance on some hippocampus-dependent…”
Background
Restraint stress in biobehavioral research: Recent developments
Buynitsky, T., & Mostofsky, D. I. (2009) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2009.05.004 · Cited by 426 · see citing works
“…et al. (2004), Hsu et al. (1998), Hunzeker et al. (2004), King et al. (2007), King et al. (2003), Kitraki et al. (2004), Lee et al. (2009), Lemaire et al. (2000, 2006), Luine et al. (1994), Madrigal et al. (2003), Munhoz et al. (2004), Pace et al. (2005), Pecoraro et al. (2004),…”
Influential
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 · see citing works
Adult-generated hippocampal and neocortical neurons in macaques have a transient existence
Gould, E., Vail, N. K., WAGERS, M. W., & Gross, C. G. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.181354698 · Cited by 400 · see citing works
Why avoid the hippocampus? A comprehensive review
Gondi, V., Tomé, W. A., & Mehta, M. P. (2010) · Radiotherapy and Oncology · doi:10.1016/j.radonc.2010.09.013 · Cited by 397 · see citing works
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 387 · see citing works
“Third, learning-induced apoptosis is followed by an increase in cell proliferation that provides the hippocampus with a new pool of young neurons [16,20].”
BackgroundSelf-citation
When neurogenesis encounters aging and disease
Lazarov, O., Mattson, M. P., Peterson, D. A., Pimplikar, S. W., & van Praag, H. (2010) · Trends in Neurosciences · doi:10.1016/j.tins.2010.09.003 · Cited by 389 · see citing works
Stress and the development of self-regulation in context
Blair, C. (2010) · Child Development Perspectives · doi:10.1111/j.1750-8606.2010.00145.x · Cited by 379 · see citing works
Adult hippocampal neurogenesis: Regulation, functional implications, and contribution to disease pathology
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“Others have reported that spatial learning enhances the proliferation and survival of newly born hippocampal cells when they were labeled at the end of training, when the animals were near asymptotic performance (Lemaire et al., 2000; Dobrossy et al., 2003).”
Background
Radiation injury and neurogenesis
Monje, M., & Palmer, T. D. (2003) · Current Opinion in Neurology · doi:10.1097/00019052-200304000-00002 · Cited by 378 · see citing works
Hippocampal-Sparing Whole-Brain Radiotherapy: A “How-To” Technique Using Helical Tomotherapy and Linear Accelerator–Based Intensity-Modulated Radiotherapy
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Chronic psychosocial stress and concomitant repetitive transcranial magnetic stimulation: effects on stress hormone levels and adult hippocampal neurogenesis
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Cortisol Reactivity Is Positively Related to Executive Function in Preschool Children Attending Head Start
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Early age-related changes in adult hippocampal neurogenesis in C57 mice
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Epidemiology-driven neurodevelopmental animal models of schizophrenia
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“…that prenatal exposure to psychological stressors leads to long-lasting cognitive deficits, including impairments in spatial reference memory (Lemaire et al., 2000; Yang et al., 2006; Wu et al., 2007), working memory (Gué et al., 2004; Meunier et al., 2004; Son et al., 2006) and reversal…”
Background
The Consequences of Early‐Life Adversity: Neurobiological, Behavioural and Epigenetic Adaptations
Maccari, S., Krugers, H. J., Morley‐Fletcher, S., Moshe Szyf, A., & Brunton, P. J. (2014) · Journal of Neuroendocrinology · doi:10.1111/jne.12175 · Cited by 347 · see citing works
Gender Differences in the Effects of Prenatal Stress on Brain Development and Behaviour
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“In another study, fostering PS pups onto control mothers had no effect on the learning impairment or suppression of LTP seen in PS males [19].”
BackgroundInfluential
Decreased adult hippocampal neurogenesis in the PDAPP mouse model of Alzheimer's disease
Donovan, M. H., Yazdani, U., Norris, R. D., Games, D., German, D. C., & Eisch, A. J. (2006) · The Journal of Comparative Neurology · doi:10.1002/cne.20840 · Cited by 350 · see citing works
“However, several recent studies in non-AD animal models also did not find associations between alterations in neurogenesis and hippocampal volume or cell number (Lemaire et al., 2000; Yamaguchi et al., 2004).”
Result
Prenatal Restraint Stress Generates Two Distinct Behavioral and Neurochemical Profiles in Male and Female Rats
Zuena, A. R., Mairesse, J., Casolini, P., Cinque, C., Alemà, G., Morley‐Fletcher, S., Chiodi, V., Spagnoli, L. G., Gradini, R., Catalani, A., et al. (2008) · PLoS ONE · doi:10.1371/journal.pone.0002170 · Cited by 339 · see citing works
“PRS male rats in the water maze [5,6], and others reporting no”
BackgroundMethod
Modulation of hippocampal cell proliferation, memory, and amyloid plaque deposition in APPsw (Tg2576) mutant mice by isolation stress
Dong, H., Goico, B., Martin, M., Csernansky, C. A., Bertchume, A., & Csernansky, J. G. (2004) · Neuroscience · doi:10.1016/j.neuroscience.2004.05.040 · Cited by 342 · see citing works
Effects of Chronic Stress on Structure and Cell Function in Rat Hippocampus and Hypothalamus
Joëls, M., Karst, H., Alfarez, D., Heine, V. M., Qin, Y., Riel, E. V., Verkuyl, M., Lucassen, P. J., & Krugers, H. J. (2004) · Stress · doi:10.1080/10253890500070005 · Cited by 330 · see citing works
“These effects are more profound when applied early in life (Lemaire et al., 2000).”
Background
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 331 · see citing works
“In particular, there was a decrease in the number of granule neurons between 3 and 22 months of age and a marked absence of hippocampal neurogenesis in PS rats compared to control rats as a result of learning a spatial task [60].”
BackgroundInfluential
Neurogenesis and Alzheimer's disease: At the crossroads
Lazarov, O., & Marr, R. A. (2009) · Experimental Neurology · doi:10.1016/j.expneurol.2009.08.009 · Cited by 326 · see citing works
“…et al., 2006; Zhao et al., 2003; Saxe et al., 2006; Zhang et al., 2008a), aged rats [For review see (Bizon and Gallagher, 2005)], stress paradigms (Lemaire et al., 2000), irradiation (Rola et al., 2004; Madsen et al., 2003; Raber et al., 2004) and the DNA methylating agent methylazoxymethanol…”
Background
Role for the kinase SGK1 in stress, depression, and glucocorticoid effects on hippocampal neurogenesis
Anacker, C., Cattaneo, A., Musaelyan, K., Zunszain, P. A., Horowitz, M., Molteni, R., Luoni, A., Calabrese, F., Tansey, K., Gennarelli, M., et al. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1300886110 · Cited by 319 · see citing works
Blockade of CRF1 or V1b receptors reverses stress-induced suppression of neurogenesis in a mouse model of depression
Alonso, R., Griebel, G., Pavone, G., Stemmelin, J., Fur, G. L., & Soubrié, P. (2003) · Molecular Psychiatry · doi:10.1038/sj.mp.4001464 · Cited by 319 · see citing works
Glucocorticoid-Related Molecular Signaling Pathways Regulating Hippocampal Neurogenesis
Anacker, C., Cattaneo, A., Luoni, A., Musaelyan, K., Zunszain, P. A., Milanesi, E., Rybka, J., Berry, A., Cirulli, F., Thuret, S., et al. (2012) · Neuropsychopharmacology · doi:10.1038/npp.2012.253 · Cited by 313 · see citing works
“We have then conducted whole genome expression analysis of the rat hippocampus in animals subjected to prenatal stress, a well established animal model of depression in which glucocorticoid levels are elevated and hippocampal neurogenesis is decreased (Lemaire et al , 2000; Fumagalli et al , 2007).”
Method
Environmental enrichment during adolescence reverses the effects of prenatal stress on play behaviour and HPA axis reactivity in rats.
Morley‐Fletcher, S., Rea, M., Maccari, S., & Laviola, G. (2003) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2003.03070.x · Cited by 373 · see citing works
Genetic determinants of adult hippocampal neurogenesis correlate with acquisition, but not probe trial performance, in the water maze task
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“As strong stress down-regulates cell proliferation and net neurogenesis (Gould et al., 1997; Gould et al., 1998; Lemaire et al., 2000), animals for which a novel environment is more stressful should have decreased levels of progenitor cell proliferation in the dentate gyrus.”
Background
Dehydroepiandrosterone (DHEA) stimulates neurogenesis in the hippocampus of the rat, promotes survival of newly formed neurons and prevents corticosterone-induced suppression
Karishma, K. K., & Herbert, J. (2002) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2002.02099.x · Cited by 297 · see citing works
“Neurogenesis is also markedly reduced in rats and tree shrews exposed to psychological or social stress (Gould et al., 1997; McEwen, 1999; Lemaire et al., 2000) and decreases with age (Cameron & Gould, 1994).”
Background
Prenatal exposure to a repeated variable stress paradigm elicits behavioral and neuroendocrinological changes in the adult offspring: potential relevance to schizophrenia
Koenig, J. I., Elmer, G. I., Shepard, P. D., Lee, P. R., Mayo, C. L., Joy, B., Hercher, E., & Brady, D. L. (2004) · Behavioural Brain Research · doi:10.1016/j.bbr.2004.05.030 · Cited by 297 · see citing works
Exposure to Prenatal Psychobiological Stress Exerts Programming Influences on the Mother and Her Fetus
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Sex differences in the gut microbiome–brain axis across the lifespan
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Maternal pregnancy-specific anxiety is associated with child executive function at 6–9 years age
Buss, C., Davis, E. P., Hobel, C. J., & Sandman, C. A. (2011) · Stress · doi:10.3109/10253890.2011.623250 · Cited by 289 · see citing works
“Interestingly, the hippocampus is a brain region that is considered to be especially susceptible to adverse prenatal effects (Lemaire et al. 2000; Coe et al. 2003; Song et al. 2008; Jia et al. 2009).”
The Placenta as a Mediator of Stress Effects on Neurodevelopmental Reprogramming
Bronson, S. L., & Bale, T. L. (2015) · Neuropsychopharmacology · doi:10.1038/npp.2015.231 · Cited by 285 · see citing works
Prenatal stress-induced alterations in major physiological systems correlate with gut microbiota composition in adulthood
Golubeva, A. V., Crampton, S., Desbonnet, L., Edge, D., O'Sullivan, O., Lomasney, K. W., Zhdanov, A. V., Crispie, F., Moloney, R. D., Borre, Y. E., et al. (2015) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2015.06.002 · Cited by 283 · see citing works
“In contrast to our findings, social anxiety levels were previously shown to be enhanced by PNS (Lemaire et al., 2000; Schulz et al., 2011).”
BackgroundResult
Adult Hippocampal Neurogenesis, Synaptic Plasticity and Memory: Facts and Hypotheses
Bruel‐Jungerman, E., Rampon, C., & Laroche, S. (2007) · Reviews in the Neurosciences · doi:10.1515/revneuro.2007.18.2.93 · Cited by 281 · see citing works
Exploring the Role of Neuroplasticity in Development, Aging, and Neurodegeneration
Marzola, P., Melzer, T., Pavesi, E., Gil-Mohapel, J., & Brocardo, P. S. (2023) · Brain Sciences · doi:10.3390/brainsci13121610 · Cited by 281 · see citing works
“For example, exposure to stress hormones during gestation has been shown to alter the timing of neurogenesis and the migration of new neurons, leading to changes in brain structure and function [91].”
Background
Investigations of HPA function and the enduring consequences of stressors in adolescence in animal models
McCormick, C. M., Mathews, I. Z., Thomas, C., & Waters, P. (2010) · Brain and Cognition · doi:10.1016/j.bandc.2009.06.003 · Cited by 276 · see citing works
Prenatal stress: Role in psychotic and depressive diseases
Markham, J. A., & Koenig, J. I. (2010) · Psychopharmacology · doi:10.1007/s00213-010-2035-0 · Cited by 274 · see citing works
“Lemaire and colleagues reported in 2000 that rats exposed to a prenatal restraint stress regimen during the final week of pregnancy, showed reduced spatial memory in the Morris water maze as adults (Lemaire et al. 2000).”
Exercise increases hippocampal neurogenesis to high levels but does not improve spatial learning in mice bred for increased voluntary wheel running.
Rhodes, J. S., van Praag, H., Jeffrey, S., Girard, I., Mitchell, G. S., Garland, T., & Gage, F. H. (2003) · Behavioral Neuroscience · doi:10.1037/0735-7044.117.5.1006 · Cited by 269 · see citing works
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 · see citing works
Prenatal Social Stress in the Rat Programmes Neuroendocrine and Behavioural Responses to Stress in the Adult Offspring: Sex‐Specific Effects
Brunton, P. J., & Russell, J. A. (2010) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2010.01969.x · Cited by 264 · see citing works
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
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“Interestingly, our data show that apoptosis decreases with age, although at a slightly different rate than proliferation, even though other studies reported increased [56] or stable [12] numbers of dying cells with age.”
BackgroundResult
Effects of prenatal restraint stress on the hypothalamus–pituitary–adrenal axis and related behavioural and neurobiological alterations
Maccari, S., & Morley-Fletcher, S. (2007) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2007.06.005 · Cited by 302 · see citing works
“Interestingly, PRS induces a life span reduction of hippocampal neurogenesis in male rats (Lemaire et al., 2000, 2006) but not in females (Darnaudéry et al., 2006), and a chronic agomelatine treatment increases hippocampal neurogenesis especially in the ventral part of the hippocampus of male rats…”
Background
Review: adult neurogenesis contributes to hippocampal plasticity
Toda, T., & Gage, F. H. (2017) · Cell and Tissue Research · doi:10.1007/s00441-017-2735-4 · Cited by 262 · see citing works
“It has been shown that hippocampal adult neurogenesis is very sensitive to the effects of stress from the perinatal period to adulthood (Gould et al. 1997; Lehmann et al. 2013; Lemaire et al. 2000; Mirescu et al. 2004), and that adult neurogenesis is required for some of the beneficial effects of antidepressants throu…”
Background
Research Review: Maternal prenatal distress and poor nutrition – mutually influencing risk factors affecting infant neurocognitive development
Monk, C. E., Georgieff, M., & Osterholm, E. A. (2012) · Journal of Child Psychology and Psychiatry · doi:10.1111/jcpp.12000 · Cited by 260 · see citing works
“, 2006); decreased hippocampal neurogenesis (Lemaire et al., 2000); reduction in dendritic arborization and synaptic loss in the hippocampus (Barros et al.”
Brain Plasticity Mechanisms and Memory: A Party of Four
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Differential effects of learning on neurogenesis: learning increases or decreases the number of newly born cells depending on their birth date
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A computational principle for hippocampal learning and neurogenesis
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“Neurogenesis is suppressed by adrenal hormones (Gould et al., 1992), and stress (Gould et al., 1998; Lemaire et al., 2000; McEwen and Magarinos, 2001) as well as in depression (Jacobs et al., 2000), which is associated with a loss of hippocampal volume (MacQueen et al., 2003).”
Background
Glucocorticoids, developmental ‘programming’ and the risk of affective dysfunction
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Epigenetic modifications of GABAergic interneurons are associated with the schizophrenia-like phenotype induced by prenatal stress in mice
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“In rats, exposure to stress during gestation induces marked changes in the behavior of the offspring that are reminiscent of the positive, negative and cognitive symptoms present in SZ and BP disorder patients (Lemaire et al., 2000; Koenig et al., 2005).”
Background
Sex, Hormones and Neurogenesis in the Hippocampus: Hormonal Modulation of Neurogenesis and Potential Functional Implications
Galea, L. A. M., Wainwright, S. R., Roes, M., Duarte‐Guterman, P., Chow, C., & Hamson, D. K. (2013) · Journal of Neuroendocrinology · doi:10.1111/jne.12070 · Cited by 238 · see citing works
Sex differences in prenatal epigenetic programing of stress pathways
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“ciated with poor learning ability (34, 35), but rats do not have differential strain-dependent learning abilities dependent on adult neurogenesis (36).”
Disruption of Neurogenesis in the Subventricular Zone of Adult Mice,and in Human Cortical Neuronal Precursor Cells in Culture, by Amyloid β-Peptideby Amyloid β-Peptide
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“Conversely, neurogenesis can be impaired by prenatal stress (Lemaire et al., 2000) and by exposure to methamphetamine (Teuchert-Noodt et al.”
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Modification of hippocampal neurogenesis and neuroplasticity by social environments
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Prenatal Deficits in Neurogenesis and Later Improvement: An Animal Study
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Stress in early life inhibits neurogenesis in adulthood
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Authors: Lemaire, V., Koehl, M., Le Moal, M., & Abrous, D. N.
Affiliations: Université de Bordeaux (FR)
Laboratoire de Psychobiologie des Comportement Adaptatifs, Institut National de la Santé et de la Recherche Médicale Unit 259, Université de Bordeaux II, Domaine de Carreire, Rue Camille Saint Saëns, 33077 Bordeaux Cedex, France
ORCID: Koehl, M.
Abrous, D. N.
Venue: Proceedings of the National Academy of Sciences
Publisher: National Academy of Sciences
Published: 2000-09-26
Volume: 97
Issue: 20
Pages: 11032-11037
ISSN: 0027-8424 (ISSN-L)
1091-6490
DOI: 10.1073/pnas.97.20.11032
PMC: PMC27143
OpenAlex: W2142525943
Cited by: 1,044
References: 48
Citations by year: 2026: 18 · 2025: 15 · 2024: 18 · 2023: 23 · 2022: 23 · 2021: 31 · 2020: 25 · 2019: 31 · 2018: 35 · 2017: 46 · 2016: 56 · 2015: 63 · 2014: 55 · 2013: 59 · 2012: 48
FWCI: 5.35
Type: journal article
Language: en
Open access: green
europepmc.org
Locations: Proceedings of the National Academy of Sciences (publishedVersion)
Europe PMC (PubMed Central) (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
HAL (submittedVersion)
Topics: Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
Keywords: prenatal stress, hippocampal neurogenesis, dentate gyrus, learning deficits, spatial learning, hippocampal-dependent memory, brain development, aging, psychopathology
MeSH terms: Animals, Cell Differentiation, Female, Hippocampus, Learning Disabilities, Neurons, Pregnancy, Prenatal Exposure Delayed Effects, Stress, Psychological, Rats, Sprague-Dawley, Rats

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Prenatal stress produces learning deficits associated with an inhibition of neurogenesis in the hippocampus

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