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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Background
Prenatal loss of father during World War One is predictive of a reduced lifespan in adulthood
Todd, N., Valleron, A., & Bougneres, P. F. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1617911114 · Cited by 31
“Epigenetics, however, is only one of the many effectors of early-life stress that can act on brain development (19); for example, prenatal stress in rats induces a reduction of neurogenesis in specific brain regions (27).”
Background
The molecular neurobiology of stress – evidence from genetic and epigenetic models
Steckler, T. (2001) · Behavioural Pharmacology · doi:10.1097/00008877-200111000-00002 · Cited by 30
“Furthermore, prenatal stress induced a life-long inhibition of neurogenŽ .esis in the rat dentate gyrus Lemaire et al., 2000 .”
Background
Epigenetic Modifications of GABAergic Interneurons Contribute to Deficits in Adult Hippocampus Neurogenesis and Depression-Like Behavior in Prenatally Stressed Mice
Zhong, H., Rong, J., Zhu, C., Liang, M., Li, Y., & Zhou, R. (2020) · International Journal of Neuropsychopharmacology · doi:10.1093/ijnp/pyaa020 · Cited by 28
Differential stroke-induced proliferative response of distinct precursor cell subpopulations in the young and aged dentate gyrus
Walter, J., Keiner, S., Witte, O. W., & Redecker, C. (2010) · Neuroscience · doi:10.1016/j.neuroscience.2010.05.035 · Cited by 30
Challenges to maternal wellbeing during pregnancy impact temperament, attention, and neuromotor responses in the infant rhesus monkey
Coe, C. L., Lubach, G. R., Crispen, H. R., Shirtcliff, E. A., & Schneider, M. L. (2010) · Developmental Psychobiology · doi:10.1002/dev.20489 · Cited by 29
Very mild stress of pregnant rats reduces volume and cell number in nucleus accumbens of adult offspring: some parallels to schizophrenia
McClure, W. O., Ishtoyan, A., & Lyon, M. (2004) · Developmental Brain Research · doi:10.1016/j.devbrainres.2003.11.015 · Cited by 30
Adult neural stem cells have latent inflammatory potential that is kept suppressed by Tcf4 to facilitate adult neurogenesis
Shariq, M., Sahasrabuddhe, V., Krishna, S., Radha, S., Nruthyathi, Bellampalli, R., Dwivedi, A., Cheramangalam, R. N., Reizis, B., Hébert, J. M., et al. (2021) · Science Advances · doi:10.1126/sciadv.abf5606 · Cited by 29
“While enriched environment enhances adult neurogenesis ( 1 – 3 ), stress ( 4 – 6 ), aging, and inflammation ( 7 – 9 ) adversely affect adult neurogenesis.”
Intrauterine hyperglycemia impairs memory across two generations
Zou, K., Ren, J. T., Luo, S., Zhang, J., Zhou, C., Tan, C., Lv, P., Sun, X., Sheng, J., Liu, X., et al. (2021) · Translational Psychiatry · doi:10.1038/s41398-021-01565-7 · Cited by 28
Four-dimensional sonography in the assessment of fetal functional neurodevelopment and behavioral patterns
Salihagič-Kadić, A., Medic, M. G., Kurjak, A., Andonotopo, W., Azumendi, G., Hafner, T., & Milenković, D. (2005) · The ultrasound review of obstetrics & gynecology/Ultrasound review of obstetrics and gynecology · doi:10.1080/14722240500190640 · Cited by 28
Neural Stem Cells Show Bidirectional Experience-Dependent Plasticity in the Perinatal Mammalian Brain
Kippin, T. E., Cain, S. W., Masum, Z., & Ralph, M. R. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.0110-04.2004 · Cited by 28
Prenatal Stress Induces Long-Term Effects in Cell Turnover in the Hippocampus-Hypothalamus-Pituitary Axis in Adult Male Rats
Baquedano, E., García‐Cáceres, C., Diz-Chaves, Y., Lagunas, N., Calmarza-Font, I., Azcoitia, Í., García‐Segura, L. M., Argente, J., Chowen, J. A., & Frago, L. M. (2011) · PLoS ONE · doi:10.1371/journal.pone.0027549 · Cited by 28
“Although previous studies have shown increased cell death in neurons of the hypothalamic paraventricular nucleus in fetal rats [46], studies in adult rats show a reduction in hippocampus cell proliferation in response to prenatal restraint stress and report that it is not accompanied by an increase in pyknosis [5,47].”
Result
Gestational stress influences cognition and behavior
Sandman, C. A., & Davis, E. P. (2010) · Future Neurology · doi:10.2217/fnl.10.35 · Cited by 27
“Evidence from animal models for persistent organizational changes or programming influences on the nervous system has been growing [103] and may include changes in neurotransmitter levels [104–106], cell growth and survival [105,107–109] and adult neurogenesis [73,110–113].”
Background
Early‐life stress diminishes the increase in neurogenesis after exercise in adult female mice
Abbink, M. R., Naninck, E. F. G., Lucassen, P. J., & Kőrösi, A. (2017) · Hippocampus · doi:10.1002/hipo.22745 · Cited by 30
Astrocyte-derived lactate in stress disorders
Chamaa, F., Magistretti, P. J., & Fiumelli, H. (2024) · Neurobiology of Disease · doi:10.1016/j.nbd.2024.106417 · Cited by 31
“…Tanti et al., 2013), chronic social defeat (Lehmann et al., 2013), and chronic immobilization (Ramirez et al., 2015) to prenatal (Coe et al., 2003; Lemaire et al., 2000) and early life stress (Mirescu et al., 2004) downregulate neurogenesis in rodents and nonhuman primates (Perera et al., 2007;…”
Stress-induced alterations in 5-HT1A receptor transcriptional modulators NUDR and Freud-1
Szewczyk, B., Kotarska, K., Daigle, M., Misztak, P., Sowa-Kućma, M., Rafało-Ulińska, A., Curzytek, K., Kubera, M., Basta‐Kaim, A., Nowak, G., et al. (2014) · The International Journal of Neuropsychopharmacology · doi:10.1017/s146114571400100x · Cited by 28
Does Chronic Unpredictable Stress during Adolescence Affect Spatial Cognition in Adulthood?
Chaby, L. E., Sheriff, M. J., Hirrlinger, A. M., Lim, J. B., Fetherston, T. B., & Braithwaite, V. A. (2015) · PLoS ONE · doi:10.1371/journal.pone.0141908 · Cited by 27
“The effects of exposure to stress on spatial ability appear to be dependent upon age at exposure [17], [18]; spatial abilities can be impaired by exposure to stress during prenatal development [19], [20] or in the first few weeks of postnatal life [16].”
Background
Stress and prefrontal cortical plasticity in the developing brain
Kolb, B. E., Harker, A., Mychasiuk, R., de Melo, S. R., & Gibb, R. L. (2017) · Cognitive Development · doi:10.1016/j.cogdev.2017.01.001 · Cited by 30
A reward increases running-wheel performance without changing cell proliferation, neuronal differentiation or cell death in the dentate gyrus of C57BL/6 mice
Klaus, F., Hauser, T., Slomianka, L., Lipp, H., & Amrein, I. (2009) · Behavioural Brain Research · doi:10.1016/j.bbr.2009.06.002 · Cited by 27
“Changes in the extent of adult hippocampal neurogenesis are associated with changes in the performance of animals in hippocampus-dependent behavioral tasks [7-11], and a recent study of conditional TLX knockout mice, a gene expressed by adult neural stem cells, suggest a causal link between the performance in specific…”
Background
Effect of agomelatine on adult hippocampus apoptosis and neurogenesis using the stress model of rats
Yücel, A., Yücel, N., Özkanlar, S., Polat, E., Kara, A., Özcan, H., & Güleç, M. (2016) · Acta Histochemica · doi:10.1016/j.acthis.2016.02.007 · Cited by 27
Insights into the Biology and Therapeutic Applications of Neural Stem Cells
Harris, L., Zalucki, O. H., Piper, M., & Heng, J. I. (2016) · Stem Cells International · doi:10.1155/2016/9745315 · Cited by 26
“For example, many studies report a significant age-related decline in cell proliferation [199, 200, 202–205].”
How is prenatal stress transmitted from the mother to the fetus?
Sze, Y., & Brunton, P. J. (2024) · Journal of Experimental Biology · doi:10.1242/jeb.246073 · Cited by 31
Maternal dexamethasone exposure ameliorates cognition and tau pathology in the offspring of triple transgenic AD mice
Meco, A. D., Joshi, Y. B., Lauretti, E., & Praticò, D. (2015) · Molecular Psychiatry · doi:10.1038/mp.2015.78 · Cited by 27
Examination of granule layer cell count, cell density, and single‐pulse brdu incorporation in rat organotypic hippocampal slice cultures with respect to culture medium, septotemporal position, and time in vitro
Sadgrove, M. P., Laskowski, A., & Gray, W. (2006) · The Journal of Comparative Neurology · doi:10.1002/cne.21000 · Cited by 26
“© 2006 WILEY-LISS, INC. sponses to stress in adulthood (Lemaire et al., 2000; Schmitz et al., 2002).”
Background
Antenatal maternal stress alters functional brain responses in adult offspring during conditioned fear
Sadler, T. R., Nguyen, P. T., Yang, J., Givrad, T. K., Mayer, E. A., Maarek, J. I., Hinton, D. R., & Holschneider, D. P. (2011) · Brain Research · doi:10.1016/j.brainres.2011.01.104 · Cited by 26
“…M anuscript N IH -PA Author M anuscript N IH -PA Author M anuscript reports suggesting effects of MS on the HPC, including inhibition of neurogenesis in the dentate gyrus, learning deficits (Lemaire et al., 2000, Odagiri et al., 2008), as well as altered c-fos expression (Viltart et al., 2006).”
Background
Gestational or acute restraint in adulthood reduces levels of 5α-reduced testosterone metabolites in the hippocampus and produces behavioral inhibition of adult male rats
Walf, A. A., & Frye, C. A. (2012) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2012.00040 · Cited by 26
“In support, gestationally stressed female rats have poorer performance in the inhibitory avoidance task compared to their non-stressed controls (Walf and Frye, 2007) and gestationally stressed male rats have poorer spatial performance (Lemaire et al., 2000; Zagron and Weinstock, 2006).”
Background
The reduction in glutamate release is predictive of cognitive and emotional alterations that are corrected by the positive modulator of AMPA receptors S 47445 in perinatal stressed rats
Morley‐Fletcher, S., Zuena, A. R., Mairesse, J., Gatta, E., Camp, G. V., Bouwalerh, H., Riozzi, B., Battaglia, G., Pittaluga, A., Olivero, G., et al. (2018) · Neuropharmacology · doi:10.1016/j.neuropharm.2018.03.018 · Cited by 28
“, 2015) and episodic spatial memory (Lemaire et al., 2000).”
Effects of Aβ25–35on neurogenesis in the adult mouse subventricular zone and dentate gyrus
Li, X., & Zuo, P. (2005) · Neurological Research · doi:10.1179/016164105x35585 · Cited by 26
Causality of stem cell based neurogenesis and depression – To be or not to be, is that the question?
Feldmann, R. E., Sawa, A., & Seidler, G. H. (2006) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2006.06.007 · Cited by 26
“Events such as intruder stress, predator odor, footshock stress, prenatal stress, and glucocorticoids have been shown to decrease NG, cause atrophy of hippocampal neurons and alter learning and memory function (Cameron et al., 1998; Gould et al., 1992; Gould et al., 1997; Gould et al., 1998; Lemaire et al., 2000; Malb…”
Background
From Vulnerability to Neurotoxicity: A Developmental Approach to the Effects of Stress on the Brain and Behavior
LUPIEN, S. J., Ouellet‐Morin, I., Herba, C. M., Juster, R., & McEwen, B. S. (2016) · Epigenetics and human health · doi:10.1007/978-3-319-24493-8_1 · Cited by 29
Mechanistic Insight into Neurotoxicity Induced by Developmental Insults
Tamm, C., & Ceccatelli, S. (2017) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2016.10.087 · Cited by 28
Perceptions of challenge: the role of catastrophe theory in piano learning
Bugos, J. A., & Lee, W. (2014) · Music Education Research · doi:10.1080/14613808.2014.899334 · Cited by 25
Theoretical and practical considerations behind the use of laboratory animals for the study of Tourette syndrome
Macrı̀, S., Onori, M. P., & Laviola, G. (2013) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2013.03.014 · Cited by 26
Electrophysiological insights into the enduring effects of early life stress on the brain
Ali, I. Y., Salzberg, M. R., French, C. R., & Jones, N. C. (2010) · Psychopharmacology · doi:10.1007/s00213-010-2125-z · Cited by 27
“Early life stress exposures, either prenatal (Coe et al. 2003; Lemaire et al. 2000; Lucassen et al. 2009; Mandyam et al. 2008) or postnatal (Lemaire et al.”
SARS-CoV-2 (COVID-19) as a possible risk factor for neurodevelopmental disorders
Dubey, H., Sharma, R. K., Krishnan, S., & Knickmeyer, R. C. (2022) · Frontiers in Neuroscience · doi:10.3389/fnins.2022.1021721 · Cited by 27
Prenatal corticosteroid impact on hippocampus: Implications for postnatal outcomes
Velı́šek, L. (2005) · Epilepsy & Behavior · doi:10.1016/j.yebeh.2005.04.008 · Cited by 24
“Daily prenatal stress from E15 to delivery leads to decreased neurogenesis of granule cells in the dentate gyrus associated with an impairment of hippocampus-related spatial learning in the water maze in the offspring throughout their lives [51].”
Background
Effect of postnatal treadmill exercise on c-Fos expression in the hippocampus of rat pups born from the alcohol-intoxicated mothers
Sim, Y.-J., Kim, H. K., Shin, M., Chang, H., Shin, M.-C., Ko, I., Kim, K.-J., Kim, T.-S., Kim, B.-K., Rhim, Y.-T., et al. (2007) · Brain and Development · doi:10.1016/j.braindev.2007.07.003 · Cited by 25
“Prenatal stresses, such as noise stress and restrained stress during pregnancy, have been documented to suppress the formation of hippocampal granule cells in a variety of mammalian species [8,9].”
Background
Disrupted Circadian Rhythm as a Common Player in Developmental Models of Neuropsychiatric Disorders
Marco, E. M., Velarde, E., Llorente, R., & Laviola, G. (2015) · Current topics in behavioral neurosciences · doi:10.1007/7854_2015_419 · Cited by 25
Effects of combined IUGR and prenatal stress on the development of the hippocampus in a fetal guinea pig model
Cumberland, A. L., Palliser, H. K., Rani, P., Walker, D. W., & Hirst, J. J. (2017) · Journal of Developmental Origins of Health and Disease · doi:10.1017/s2040174417000307 · Cited by 25
Early Childhood Self-Regulation in Context: Parental and Familial Environmental Influences
Kiss, M., Fechete, G. L., Pop, M., & Susa, G. (2014) · Cognitie, Creier, Comportament · Cited by 25

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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