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

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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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T‐817MA, a neurotrophic agent, ameliorates the deficits in adult neurogenesis and spatial memory in rats infused i.c.v. with amyloid‐β peptide
Kimura, T., Nguyen, P. T., Ho, S. A., Tran, A. H., Ono, T., & Nishijo, H. (2009) · British Journal of Pharmacology · doi:10.1111/j.1476-5381.2009.00141.x · Cited by 44
“…are positive regulators, whereas adrenal steroids, excitatory inputs and stressful experiences have negative effects (Ambrogini et al., 2000; Lemaire et al., 2000; Snyder et al., 2001; Malberg and Duman, 2003; Rizk et al., 2006; Correspondence: Dr Hisao Nishijo, System Emotional Science,…”
Sexual experience restores age‐related decline in adult neurogenesis and hippocampal function
Glasper, E. R., & Gould, E. (2013) · Hippocampus · doi:10.1002/hipo.22090 · Cited by 52
“…dogs, marmosets, and macaques (Seki and Arai, 1995; Kuhn et al., 1996; Kempermann et al., 1998; Cameron and McKay, 1999; Gould et al., 1999a; Lemaire et al., 2000; Jin et al., 2003; Nacher et al., 2003; Heine et al., 2004; McDonald and Wojtowicz, 2005; Simon et al., 2005; Kronenberg et al.,…”
Background
Stress-induced suppression of hippocampal neurogenesis in adult male rats is altered by prenatal ethanol exposure
Sliwowska, J. H., Barker, J. M., Barha, C. K., Lan, N., Weinberg, J., & Galea, L. A. M. (2010) · Stress · doi:10.3109/10253890903531582 · Cited by 46
“Exposure to acute or chronic stress in prenatal life (Lemaire et al. 2000, 2006; Mandyam et al. 2008) or in adulthood (Holmes and Galea 2002; Mirescu et al. 2004; Mirescu and Gould 2006) suppresses both cell proliferation and cell survival in the hippocampus of adult male rats.”
Background
A Baldwin interpretation of adult hippocampal neurogenesis: from functional relevance to physiopathology
Abrous, D. N., Koehl, M., & Lemoine, M. (2021) · Molecular Psychiatry · doi:10.1038/s41380-021-01172-4 · Cited by 51
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Programming effects of antenatal dexamethasone in the developing mesolimbic pathways
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“The inhibitory actions of CS on neuronal proliferation in the postnatal brain, especially in the hippocampus (Gould et al., 1991), have been extensively described, but their ability to interfere with neurogenesis during prenatal life have been recognized only recently (Lemaire et al., 2000).”
Background
Prenatal Bystander Stress Alters Brain, Behavior, and the Epigenome of Developing Rat Offspring
Mychasiuk, R., Schmold, N., Ilnytskyy, S., Kovalchuk, O., Kolb, B. E., & Gibb, R. L. (2011) · Developmental Neuroscience · doi:10.1159/000330034 · Cited by 47
“The perinatal brain is extremely plastic and consequently very susceptible to environmental influences [”
Background
Associations between prenatal, childhood, and adolescent stress and variations in white-matter properties in young men
Jensen, S. K. G., Pangelinan, M., Björnholm, L., Klasnja, A., Leemans, A., Drakesmith, M., Evans, C. J., Barker, E. D., & Paus, T. (2018) · NeuroImage · doi:10.1016/j.neuroimage.2017.10.033 · Cited by 44
“Prenatal maternal stress in particular, but also early postnatal stress has been associated with reduced neurogenesis and enhanced apoptosis in the hippocampus in rodents (Lemaire et al., 2000; Lemaire et al., 2006; Mirescu et al., 2004; Van den Hove et al., 2006) and non-human primates (Coe et al.”
Background
Decreased Bdnf expression and reduced social behavior in periadolescent rats following prenatal stress
Berry, A., Panetta, P., Luoni, A., Bellisario, V., Capoccia, S., Riva, M. A., & Cirulli, F. (2015) · Developmental Psychobiology · doi:10.1002/dev.21297 · Cited by 46
Memory development: implications for adults recalling childhood experiences in the courtroom
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Enriched environment treatment counteracts enhanced addictive and depressive-like behavior induced by prenatal chronic stress
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Influenza vaccination during early pregnancy contributes to neurogenesis and behavioral function in offspring
Xia, Y., Qi, F., Zou, J., Yang, J., & Yao, Z. (2014) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2014.06.202 · Cited by 43
“inhibition of neurogenesis and behavioral abnormalities in offspring (French et al., 2013; Lemaire et al., 2000; Zhao et al., 2008) is surpassed by the results of the present study.”
Result
Effects of prenatal protein malnutrition and acute postnatal stress on granule cell genesis in the fascia dentata of neonatal and juvenile rats
King, R. S., DeBassio, W. A., Kemper, T. L., Rosene, D. L., Tonkiss, J., Galler, J. R., & Blatt, G. J. (2004) · Developmental Brain Research · doi:10.1016/j.devbrainres.2004.02.002 · Cited by 44
Chronic ethanol consumption transiently reduces adult neural progenitor cell proliferation
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Neuronal number, volume, and apoptosis of the left dentate gyrus of chronically stressed pigs correlate negatively with basal saliva cortisol levels
van der Beek, E. M., Wiegant, V. M., Schouten, W. G. P., Eerdenburg, F. J. C. M. V., Loijens, L. W. S., van der Plas, C., Benning, M. A., de Vries, H., de Kloet, E. R., & Lucassen, P. J. (2004) · Hippocampus · doi:10.1002/hipo.10213 · Cited by 49
“Moreover, the impact of stress on many parameters, including adult neurogenesis, is more severe when applied early in life (Weaver et al., 2000a; Lemaire et al., 2000; Brunson et al., 2001; Coe et al., 2003).”
Background
Resetting the Dynamic Range of Hypothalamic‐Pituitary‐Adrenal Axis Stress Responses Through Pregnancy
Brunton, P. J. (2010) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2010.02067.x · Cited by 43
A selective role for ARMS/Kidins220 scaffold protein in spatial memory and trophic support of entorhinal and frontal cortical neurons
Duffy, Á., Schaner, M. J., Wu, S. H., Staniszewski, A., Kumar, A. R., Arévalo, J. C., Arancio, O., Chao, M. V., & Scharfman, H. E. (2011) · Experimental Neurology · doi:10.1016/j.expneurol.2011.03.008 · Cited by 44
“One reason to suggest this is that pyknosis and weak NeuN-ir are often found when there is oxidative stress (Lemaire et al., 2000; Ünal-Çevik et al., 2004; Portiansky et al., 2006; Buckingham et al., 2008).”
Mature granule cells of the dentate gyrus—Passive bystanders or principal performers in hippocampal function?
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Mild, non-lesioning transient hypoxia in the newborn rat induces delayed brain neurogenesis associated with improved memory scores
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Glucocorticoid Receptors in Hippocampal Neurons that Do Not Engage Proteasomes Escape from Hormone-Dependent Down-Regulation but Maintain Transactivation Activity
Wang, X., Pongrac, J. L., & DeFranco, D. B. (2002) · Molecular Endocrinology · doi:10.1210/me.2001-0287 · Cited by 43
“However, excessive fetal glucocorticoid exposure, which can either result from prenatal stress (47, 48) or antenatal administration of metabolically stable synthetic glucocorticoids such as dexamethasone, may have detrimental effects on brain development (49, 50).”
Background
Individual vulnerability to substance abuse and affective disorders: Role of early environmental influences
Koehl, M., Lemaire, V., Mayo, W., Abrous, D. N., Maccari, S., Piazza, P. V., Moal, M. L., & Vallée, M. (2002) · Neurotoxicity Research · doi:10.1080/1029842021000010866 · Cited by 44
“Finally, we examined whether the reduction in cell proliferation in the dentate gyrus had an impact on spatial memory (Lemaire et al., 2000).”
BackgroundSelf-citation
Effects of duration and timing of prenatal stress on hippocampal myelination and synaptophysin expression
Xu, J., Yang, B., Yan, C., Hu, H., Cai, S., Liu, J., Wu, M., Ouyang, F., & Shen, X. (2013) · Brain Research · doi:10.1016/j.brainres.2013.06.025 · Cited by 42
The Neurotransmitter VIP Expands the Pool of Symmetrically Dividing Postnatal Dentate Gyrus Precursors via VPAC2 Receptors or Directs Them Toward a Neuronal Fate via VPAC1 receptors
Zaben, M., Sheward, W. J., Shtaya, A., Abbosh, C., Harmar, A. J., Pringle, A. K., & Gray, W. (2009) · Stem Cells · doi:10.1002/stem.184 · Cited by 42
Altered brain morphology and functional connectivity reflect a vulnerable affective state after cumulative multigenerational stress in rats
McCreary, J. K., Truica, L. S., Friesen, B., Yao, Y., Olson, D. M., Kovalchuk, I., Cross, A. R., & Metz, G. A. S. (2016) · Neuroscience · doi:10.1016/j.neuroscience.2016.05.046 · Cited by 45
“For example, prenatal stress may reduce hippocampal neurogenesis, alter dendritic morphology, and diminish hippocampal volume (Lemaire et al., 2000; Lui et al., 2011; Mychasiuk et al., 2012) along with global increases in cerebral blood flow and changes in energy metabolism (Bryan, 1990).”
Background
Insult-induced aberrant hippocampal neurogenesis: Functional consequences and possible therapeutic strategies
Bielefeld, P., Durá, I., Danielewicz, J., Lucassen, P. J., Baekelandt, V., Abrous, D. N., Encinas, J. M., & Fitzsimons, C. P. (2019) · Behavioural Brain Research · doi:10.1016/j.bbr.2019.112032 · Cited by 42
“The production of newborn neurons decreases slowly with age [10,23 – 25] possibly due to changes in the vasculature or neurogenic niche [26,27], the systemic environment [28], or the limited regenerative capacity of NSCs [29].”
Self-citation
The partial 5-HT1A receptor agonist buspirone enhances neurogenesis in the opossum (Monodelphis domestica)
Grabiec, M., Turlejski, K., & Djavadian, R. L. (2009) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2009.01.013 · Cited by 42
“Several authors found that newly generated cells contribute to elaboration of some forms of hippocampus-dependent memory, especially the spatial memory (Lemaire et al., 2000; Olariu et al., 2005; Snyder et al., 2005).”
Background
Prenatal stress alters the negative correlation between neuronal activation in limbic regions and behavioral responses in rats exposed to high and low anxiogenic environments
Mairesse, J., Viltart, O., Salomé, N., Giuliani, A., Catalani, A., Casolini, P., Morley‐Fletcher, S., Nicoletti, F., & Maccari, S. (2007) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2007.03.013 · Cited by 42
“, 1988) and the decreased hippocampal neurogenesis (Lemaire et al., 2000) of PS rats.”
Background
Dietary choline supplementation to dams during pregnancy and lactation mitigates the effects of in utero stress exposure on adult anxiety-related behaviors
Schulz, K. M., Pearson-Smith, J. N., Gasparrini, M. E., Brooks, K. F., Drake-Frazier, C., Zajkowski, M. E., Kreisler, A. D., Adams, C. E., Leonard, S. S., & Stevens, K. E. (2014) · Behavioural Brain Research · doi:10.1016/j.bbr.2014.03.031 · Cited by 41
“For example, prenatal stress significantly reduces hippocampal neurogenesis [43], whereas prenatal choline supplementation increases hippocampal neurogenesis in offspring [44, 45].”
Background
Modulation of Adult Hippocampal Neurogenesis by Sleep: Impact on Mental Health
Navarro-Sanchis, C., Brock, O., Winsky‐Sommerer, R., & Thuret, S. (2017) · Frontiers in Neural Circuits · doi:10.3389/fncir.2017.00074 · Cited by 43
“, 2004; Mirescu and Gould, 2006) or disrupted (Kuhn et al., 1996; Diamond et al., 1999; Eisch et al., 2000; Gross, 2000; Lemaire et al., 2000; Drapeau et al., 2003; Scerri et al., 2006) hippocampal-dependent learning and memory.”
Background
The opioid system in stress-induced memory disorders: From basic mechanisms to clinical implications in post-traumatic stress disorder and Alzheimer's disease
Torres‐Berrío, A., & Nava-Mesa, M. O. (2018) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2018.08.011 · Cited by 41
“dependent memories, and induces structural and functional alterations in the HPC (Conrad et al., 1996; Kleen et al., 2006; Lemaire et al., 2000; Magarinos et al., 1997).”
Pregnenolone Sulfate and Aging of Cognitive Functions: Behavioral, Neurochemical, and Morphological Investigations
Mayo, W., Moal, M. L., & Abrous, D. N. (2001) · Hormones and Behavior · doi:10.1006/hbeh.2001.1677 · Cited by 43
Self-citation
Preweaning enrichment has no lasting effects on adult hippocampal neurogenesis in four‐month‐old mice
Kohl, Z., Kuhn, H. G., Cooper‐Kuhn, C. M., Winkler, J., Aigner, L., & Kempermann, G. (2002) · Genes Brain & Behavior · doi:10.1046/j.1601-1848.2001.00009.x · Cited by 40
“As it has been shown that prenatal stress has lasting effects on adult hippocampal neurogenesis (Lemaire et al. 2000) as does postnatal stress (Gould et al. 1997), it is likely that any presumed stress the animals might have experienced in the present study was below the threshold to cause…”
BackgroundInfluential
More Is Less: Neurogenesis and Age-Related Cognitive Decline in Long-Evans Rats
Bizon, J. L., & Gallagher, M. (2005) · Science of Aging Knowledge Environment · doi:10.1126/sageke.2005.7.re2 · Cited by 44
Maternal diet rich in omega-6 polyunsaturated fatty acids during gestation and lactation produces autistic-like sociability deficits in adult offspring
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“In addition, daily maternal restraint during the last week of gestation resulted in a significant decrease in cell proliferation in the dentate gyrus in male adult offspring (Lemaire et al., 2000; Fujioka et al., 2006).”
Background
Ancestral Exposure to Stress Generates New Behavioral Traits and a Functional Hemispheric Dominance Shift
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Gene therapy with the TRF 1 telomere gene rescues decreased TRF 1 levels with aging and prolongs mouse health span
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Depleting adult dentate gyrus neurogenesis increases cocaine-seeking behavior
Deroche‐Gamonet, V., Revest, J., Fiancette, J.-F., Balado, É., Koehl, M., Grosjean, N., Abrous, D. N., & Piazza, P. (2018) · Molecular Psychiatry · doi:10.1038/s41380-018-0038-0 · Cited by 45
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Recovery of Chronic Noise Exposure Induced Spatial Learning and Memory Deficits in Young Male Sprague‐Dawley Rats
Chen, C., Tang, Y. M., Xuejun, J., Li, X., Youbin, Q., & Tu, B. (2011) · Journal of Occupational Health · doi:10.1539/joh.l10125 · Cited by 40
Neurocognitive Impairment and Dementia in Mood Disorders
Pfennig, A., Littmann, E., & Bauer, M. (2007) · Journal of Neuropsychiatry · doi:10.1176/jnp.2007.19.4.373 · Cited by 40

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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