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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“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
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
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“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
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Maternal pregnancy-specific anxiety is associated with child executive function at 6–9 years age
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“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).”
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Prenatal stress-induced alterations in major physiological systems correlate with gut microbiota composition in adulthood
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“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 295
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
“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
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Prenatal stress: Role in psychotic and depressive diseases
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“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 274
Suppressed proliferation and apoptotic changes in the rat dentate gyrus after acute and chronic stress are reversible
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Prenatal Social Stress in the Rat Programmes Neuroendocrine and Behavioural Responses to Stress in the Adult Offspring: Sex‐Specific Effects
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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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BackgroundResult
Effects of prenatal restraint stress on the hypothalamus–pituitary–adrenal axis and related behavioural and neurobiological alterations
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“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 279
“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 266
“, 2006); decreased hippocampal neurogenesis (Lemaire et al., 2000); reduction in dendritic arborization and synaptic loss in the hippocampus (Barros et al.”
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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).”
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Glucocorticoids, developmental ‘programming’ and the risk of affective dysfunction
Seckl, J. R. (2007) · Progress in Brain Research · doi:10.1016/s0079-6123(07)67002-2 · Cited by 245
Epigenetic modifications of GABAergic interneurons are associated with the schizophrenia-like phenotype induced by prenatal stress in mice
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Sex, Hormones and Neurogenesis in the Hippocampus: Hormonal Modulation of Neurogenesis and Potential Functional Implications
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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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