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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BackgroundSelf-citation
Effect of prenatal stress on memory, nicotine withdrawal and 5HT1A expression in raphe nuclei of adult rats
Said, N., Lakehayli, S., Khachibi, M. E., Ouahli, M. E., Nadifi, S., Hakkou, F., & Tazi, A. (2015) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2015.04.008 · Cited by 17
“They can be caused by a severe reduction in neurogenesis (Lemaire et al., 2000; Fujioka et al., 2006), volume (Martinez-Tellez et al., 2009) and granule cell number in the hippocampus (Schmitz et al., 2002).”
Background
Prenatal Activation of Toll-Like Receptor-4 Dampens Adult Hippocampal Neurogenesis in An IL-6 Dependent Manner
Mouihate, A. (2016) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2016.00173 · Cited by 17
“…of Perugia, Italy Reviewed by: Ruben J. Cauchi, University of Malta, Malta Patricia Parnet, Institut National de la Recherché Agronomique, France *Correspondence: Abdeslam Mouihate abdeslam@hsc.edu.kw Received: 28 March 2016 Accepted: 20 June 2016 Published: 30 June 2016 Citation:”
Early Postnatal Stress Impairs Cognitive Functions of Male Rats Persisting Until Adulthood
Holubová, A., Lukášková, I., Tomášová, N., Šuhajdová, M., & Šlamberová, R. (2018) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2018.00176 · Cited by 17
“Recent clinical studies have shown that maternal MA abuse increases maternal symptoms of depression and parenting stress (Liles et al., 2012).”
Background
Prenatal Stress and Adult Drug-Seeking Behavior: Interactions with Genes and Relation to Nondrug-Related Behavior
Kippin, T. E., Campbell, J. C., Ploense, K. L., Knight, C. P., & Bagley, J. R. (2014) · Advances in neurobiology · doi:10.1007/978-1-4939-1372-5_5 · Cited by 18
The Relationship Between Mastication and Cognition
Kubo, K., Chen, H., & Onozuk, M. (2013) · InTech eBooks · doi:10.5772/54911 · Cited by 17
Sleep in Prenatally Restraint Stressed Rats, a Model of Mixed Anxiety-Depressive Disorder
Mairesse, J., Camp, G. V., Gatta, E., Marrocco, J., Reynaert, M., Consolazione, M., Morley‐Fletcher, S., Nicoletti, F., & Maccari, S. (2014) · Advances in neurobiology · doi:10.1007/978-1-4939-1372-5_2 · Cited by 17
“The value of PRS rats as a model of depression is strengthened by the finding that these animals show a persistent deficit in hippocampal neurogenesis and abnormalities in transcription factors and surface receptors that have been related to the pathophysiology of depression and anxiety (Darnaudéry et al. 2006; Lemair…”
Background
Neurodevelopmental liabilities in schizophrenia and affective disorders
Palomo, T., Kostrzewa, R. M., Archer, T., & Beninger, R. J. (2002) · Neurotoxicity Research · doi:10.1080/1029842021000022061 · Cited by 17
“A recent study showed that prenatal stress resulted in inhibition of neurogenesis in the hippocampus associated with learning (Lemaire et al., 2000).”
Background
Effects of prenatal stress on anxiety-like behavior and nociceptive response in rats
Said, N., Lakehayli, S., Battas, O., Hakkou, F., & Tazi, A. (2015) · Journal of Integrative Neuroscience · doi:10.1142/s0219635215500107 · Cited by 17
Sex-Specific Effects of Prenatal Stress on Memory and Markers of Neuronal Activity in Juvenile Rats
Barbie-Shoshani, Y., Shoham, S., Bejar, C., & Weinstock, M. (2016) · Developmental Neuroscience · doi:10.1159/000446981 · Cited by 17
Prenatal Stress and Neurodevelopmental Plasticity: Relevance to Psychopathology
Pallarés, M. E., & Antonelli, M. C. (2017) · Advances in experimental medicine and biology · doi:10.1007/978-3-319-62817-2_7 · Cited by 19
“Chronic maternal restraint stress slows the acquisition of spatial learning (Lemaire et al. 2000; Son et al. 2006; Yang et al. 2006) and reduces long-term potentiation, a primary physiological model of memory (Son et al.”
Pregestational stress attenuated fertility rate in dams and increased seizure susceptibility in offspring
Mahmoodkhani, M., Saboory, E., Roshan‐Milani, S., Azizi, N., Karimipour, M., Rasmi, Y., & Gholinejad, Z. (2018) · Epilepsy & Behavior · doi:10.1016/j.yebeh.2017.12.016 · Cited by 17
Chewing during prenatal stress prevents prenatal stress-induced suppression of neurogenesis, anxiety-like behavior and learning deficits in mouse offspring
Kubo, K., Kotachi, M., Suzuki, A., Iinuma, M., & Azuma, K. (2018) · International Journal of Medical Sciences · doi:10.7150/ijms.25281 · Cited by 18
“PS leads to suppression of neurogenesis in the hippocampal dentate gyrus (DG) [2, 3, 5], and decreased in brain-derived neurotrophic factor (BDNF) expression in the hippocampus [6] in the offspring.”
Background
Prenatal phencyclidine exposure alters hippocampal cell proliferation in offspring rats
Tanimura, A., Liu, J., Namba, T., Seki, T., Matsubara, Y., Itoh, M., Suzuki, T., & Arai, H. (2009) · Synapse · doi:10.1002/syn.20660 · Cited by 17
“Conversely, induction of a long-term or life-long reduction in hippocampal neurogenesis has been reported following prenatal stress in rats (Lemaire et al., 2000).”
Background
Stress, immunité et physiologie du système nerveux
Jacque, C., & Thurin, J.-M. (2002) · médecine/sciences · doi:10.1051/medsci/200218111160 · Cited by 17
“Des travaux récents montrent que le stress prénatal induit des anomalies de structure persistantes de l’hippocampe et un déficit consécutif des performances d’apprentissage et de mémorisation [29].”
Background
Epigenetic landscape of stress surfeit disorders: Key role for DNA methylation dynamics
Gatta, E., Saudagar, V., Auta, J., Grayson, D. R., & Guidotti, A. (2020) · International review of neurobiology · doi:10.1016/bs.irn.2020.08.002 · Cited by 19
Steroid hormones and hippocampal neurogenesis in the adult mammalian brain
Hodges, T. E., Puri, T. A., Blankers, S. A., Qiu, W., & Galea, L. A. M. (2022) · Vitamins and hormones · doi:10.1016/bs.vh.2021.11.003 · Cited by 17
Chronic clomipramine treatment increases hippocampal volume in rats exposed to chronic unpredictable mild stress
Zhang, S., Hu, J., Liu, G., Wu, H., Li, M., Shi, C., Liu, Q., & Li, W. (2022) · Translational Psychiatry · doi:10.1038/s41398-022-02006-9 · Cited by 16
Early life adversity across different cell- types in the brain
Warhaftig, G., Almeida, D. M., & Turecki, G. (2023) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2023.105113 · Cited by 20
Selective breeding of rats for high (HAB) and low (LAB) anxiety-related behaviour: A unique model for comorbid depression and social dysfunctions
Gryksa, K., Schmidtner, A. K., Masís-Calvo, M., Rodríguez‐Villagra, O. A., Havasi, A., Wirobski, G., Maloumby, R., Jägle, H., Bosch, O. J., Slattery, D. A., et al. (2023) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2023.105292 · Cited by 20
Multigenerational prenatal stress increases the coherence of brain signaling among cortico–striatal–limbic circuits in adult rats
Skelin, I., Needham, M., Molina, L., Metz, G. A. S., & Gruber, A. J. (2015) · Neuroscience · doi:10.1016/j.neuroscience.2015.01.009 · Cited by 18
“One hypothesized mechanism of altered developmental trajectory following PNS is the maternal release of stress-related hormones, which can disrupt neuronal migration, maturation and synaptogenesis in the fetal brain (Lemaire et al., 2000; Markham and Koenig, 2011).”
Background
Epigenetic regulation of G protein coupled receptor signaling and its implications in psychiatric disorders
Dogra, S., Sona, C., Kumar, A., & Yadav, P. N. (2016) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2016.03.012 · Cited by 17
Prenatal corticosteroid exposure alters early developmental seizures and behavior
Velı́šek, L. (2011) · Epilepsy Research · doi:10.1016/j.eplepsyres.2011.01.019 · Cited by 16
Oxytocin protects against 3-NP induced learning and memory impairment in rats: sex differences in behavioral and molecular responses to the context of prenatal stress.
Moslemi, M., Khodagholi, F., Asadi, S., Rafiei, S., & Motamedi, F. (2019) · Behavioural Brain Research · doi:10.1016/j.bbr.2019.112354 · Cited by 15
An Overview of Psychological and Neurobiological Mechanisms by which Early Negative Experiences Increase Risk of Mood Disorders.
Hassel, S., McKinnon, M. C., Cusi, A. M., & MacQUEEN, G. M. (2011) · Europe PMC (PubMed Central) · Cited by 16
Effects of Korea Red Ginseng Total Saponin on Repeated Unpredictable Stress-induced Changes of Proliferation of Neural Progenitor Cells and BDNF mRNA Expression in Adult Rat Hippocampus
김동훈 (2004) · Journal of Ginseng Research · doi:10.5142/jgr.2004.28.2.094 · Cited by 16
Designing the human stress ontology: A formal framework to capture and represent knowledge about human stress
Khoozani, E. N., & Hadzic, M. (2010) · Australian Psychologist · doi:10.1080/00050061003664811 · Cited by 19
Glucocorticosteroids Effects on Brain Development in the Preterm Infant: A Role for Microglia?
Zinni, M., Pansiot, J., Billion, E., Baud, O., & Mairesse, J. (2021) · Current Neuropharmacology · doi:10.2174/1570159x19666210517112913 · Cited by 15
“1159/000488106 PMID: 29874660 [27] Lemaire, V.”
Hippocampal atrophy is associated with hearing loss in cognitively normal adults
Shim, Y. J., Jung, W. H., Billig, A. J., Sedley, W., & Song, J. (2023) · Frontiers in Neuroscience · doi:10.3389/fnins.2023.1276883 · Cited by 16
Scatter hoarding and hippocampal cell proliferation in Siberian chipmunks
Pan, Y., Li, M., Yi, X., Zhao, Q., Lieberwirth, C., Wang, Z., & Zhang, Z. (2013) · Neuroscience · doi:10.1016/j.neuroscience.2013.09.065 · Cited by 15
“The rates of hippocampal cell proliferation and survival are affected by many factors including environmental complexity, locomotor activity, and the expression of other behaviors (Kempermann et al., 1997, 1998a,b; van Praag et al., 1999; Lemaire et al., 2000; Fowler et al., 2002; Mitra et al., 2006; Olson et al., 200…”
Background
Prenatal stress puzzle, the oxytocin piece: Prenatal stress alters the behaviour and autonomic regulation in piglets, insights from oxytocin
Rault, J., Mack, L. A., Carter, C. S., Garner, J. P., Marchant, J. N., Richert, B. T., & Lay, D. C., Jr. (2013) · Applied Animal Behaviour Science · doi:10.1016/j.applanim.2013.07.001 · Cited by 15
“Schneider, 1993), physical (Lemaire et al., 2000), or physiological (Haussmann et al.”
Background
Multifactorial determinants of cognition — Thyroid function is not the only one
Moncayo, R., & Ortner, K. (2015) · BBA Clinical · doi:10.1016/j.bbacli.2015.04.002 · Cited by 16
Adult Neurogenesis, Chronic Stress and Depression
Lucassen, P. J., Oomen, C. A., Schouten, M., Encinas, J. M., & Fitzsimons, C. P. (2016) · Elsevier eBooks · doi:10.1016/b978-0-12-801977-1.00008-8 · Cited by 15
“…the developmental stage during which the organism experienced stress (Coe et al., 2003; Galea, 2008; Kim et al., 2013; Korosi et al., 2012; Lemaire et al., 2000; Loi, Koricka, Lucassen, & Joëls, 2014; Lucassen et al., 2009; Lucassen, Naninck, et al., 2013; Mirescu et al., 2004; Naninck et…”
HCNP precursor protein transgenic mice display a depressive-like phenotype in old age
Matsukawa, N., Furuya, Y., Ogura, H., & Ojika, K. (2010) · Brain Research · doi:10.1016/j.brainres.2010.06.041 · Cited by 15
“…resulting in atrophy of postsynaptic dendritic spines in CA1, while an antidepressant of the selective serotonin uptake inhibitor (SSRI) class can induce the phosphorylation of Erk in the hippocampus and ameliorate the depressive mood in the animal model (Gourley et al., 2008; Li et al., 2009).”
Early life low intensity stress experience modifies acute stress effects on juvenile brain cell proliferation of European sea bass ( D. Labrax )
Fokos, S., Pavlidis, M. A., Yiotis, T., Tsalafouta, A., Papandroulakis, N., & Dermon, C. R. (2016) · Behavioural Brain Research · doi:10.1016/j.bbr.2016.09.026 · Cited by 15
“Decreased proliferation and neurogenesis in hippocampus have also been reported following maternal separation [22] and prenatal stress [21], pointing out the importance of the stress protocol applied and the developmental period of early stressful experiences that may lead to long lasting structural and functional cha…”
Prenatal immobilization stress and postnatal maternal separation cause differential neuroendocrine responses to fasting stress in adult male rats
Roque, A., Ruiz‐González, R., Pineda, E., Torner, L., & Lajud, N. (2019) · Developmental Psychobiology · doi:10.1002/dev.21947 · Cited by 14
The effects of prenatal and postnatal environmental interaction: Prenatal environmental adaptation hypothesis
Lee, Y.-A., & Goto, Y. (2013) · Journal of Physiology-Paris · doi:10.1016/j.jphysparis.2013.04.007 · Cited by 14
“…exposed to prolonged, repeated restraint stress [for examples (Bustamante et al., 2010; Lui et al., 2011; Szuran et al., 1994; Vallee et al., 1999; Lemaire et al., 2000; Son et al., 2006; Hosseini-Sharifabad and Hadinedoushan, 2007; Yaka et al., 2007)], whereas there are also several studies…”
Spatial learning and memory deficits induced by prenatal glucocorticoid exposure depend on hippocampal CRHR1 and CXCL5 signaling in rats
Zheng, Y., Zhang, Y.-M., Tang, Z., Du, J.-K., Guo, D., Xu, Y., Sheng, H., Lu, J., & Ni, X. (2021) · Journal of Neuroinflammation · doi:10.1186/s12974-021-02129-8 · Cited by 17
“Epidemiological studies have indicated that prenatal exposure to GCs by either maternal stress or sGC treatment leads to increased susceptibility to cardiovascular, metabolic, and neuropsychiatric disorders in adulthood [4–7], which has been confirmed by many studies in animals [8–11].”
BackgroundInfluential

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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