The DOI matches its Crossref record; 48 of the 48 references it cites were found in a registry or an index.
Prenatal stress produces learning deficits associated with an inhibition of neurogenesis in the hippocampus
Open accessAbstract
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.
Overview
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In the citing paper
“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
In the citing paper
“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
In the citing paper
“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
Citations
Cites
Memory and the hippocampus: A synthesis from findings with rats, monkeys, and humans.
Squire, L. R. (1992) · Psychological Review · doi:10.1037/0033-295x.99.2.195 · Cited by 5,376
Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus
van Praag, H., Kempermann, G., & Gage, F. H. (1999) · Nature Neuroscience · doi:10.1038/6368 · Cited by 3,880
Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats
Altman, J., & Das, G. D. (1965) · Journal of Comparative Neurology · doi:10.1002/cne.901240303 · Cited by 3,592
The Neuroendocrinology of Stress: A Never Ending Story
Lightman, S. L. (2008) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2008.01711.x · Cited by 3,588
More hippocampal neurons in adult mice living in an enriched environment
Kempermann, G., Kuhn, H. G., & Gage, F. H. (1997) · Nature · doi:10.1038/386493a0 · Cited by 3,586
Kuhn, H., Dickinson-Anson, H., & Gage, F. (1996) · The Journal of Neuroscience · doi:10.1523/jneurosci.16-06-02027.1996 · Cited by 3,139
Learning enhances adult neurogenesis in the hippocampal formation
Gould, E., Beylin, A., Tanapat, P., Reeves, A., & Shors, T. J. (1999) · Nature Neuroscience · doi:10.1038/6365 · Cited by 2,157
Stress and cognition: are corticosteroids good or bad guys?
de Kloet, E. R., Oitzl, M. S., & Joëls, M. (1999) · Trends in Neurosciences · doi:10.1016/s0166-2236(99)01438-1 · Cited by 1,258
Stress and glucocorticoids impair retrieval of long-term spatial memory
de Quervain, D. J.-F., Roozendaal, B., & McGaugh, J. L. (1998) · Nature · doi:10.1038/29542 · Cited by 1,182
Unbiased Stereology: Three-Dimensional Measurement in Microscopy
Howard, C. V., & Reed, M. (1998) · Cited by 1,149
Flagged first, then by citations
Research works printed but not linked: 2
- B B Stanfield, J E Trice Exp Brain Res 72, 399–406 (1988).
- E Gould, H A Cameron, D C Daniels, C S Woolley, B S McEwen J Neuroci 12, 3642–3650 (1992).
Cited by
Sorted by citations
Items 801–900 of 999
Kanter, M. (2012) · Toxicology and Industrial Health · doi:10.1177/0748233711430982 · Cited by 6
“Prenatal stress produces learning deficits associated with inhibition of hippocampal neurogenesis (Hayashi et al., 1998; Lemaire et al., 2000).”
BackgroundEffects of prenatal stress on developmental anatomy of the brain and adult behavioural pathology
Ulupınar, E. (2009) · Anatomy (International Journal of Experimental and Clinical Anatomy) · doi:10.2399/ana.09.034 · Cited by 8
Luft, C., Levices, I. P., da Costa, M. S., de Oliveira, J. R., & Donadio, M. V. F. (2021) · Neuroscience Letters · doi:10.1016/j.neulet.2021.135659 · Cited by 6
Xu, Y., Wang, X., Wang, M.-J., Liu, Y.-Y., Xue, Z., & Chen, J. (2021) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2020.111204 · Cited by 6
Vert, P., & Daval, J. (2006) · Bulletin de l Académie Nationale de Médecine · doi:10.1016/s0001-4079(19)33330-8 · Cited by 6
Critical Age Windows for Neurodevelopmental Psychiatric Disorders: Evidence from Animal Models
Marco, E. M., Macrì, S., & Laviola, G. (2010) · Springer eBooks · doi:10.1007/978-1-4614-0785-0_26 · Cited by 7
Consequences of Uteroplacental Insufficiency on Developmental and Intellectual Performances
Gosselin, J., Fouron, J., & Amiel‐Tison, C. (2006) · NeoReviews · doi:10.1542/neo.7-4-e202 · Cited by 6
Bidgoli, F. A., Talaei, S. A., Tameh, A. A., & Salami, M. (2025) · Neurobiology of Stress · doi:10.1016/j.ynstr.2025.100736 · Cited by 5
“Prenatal stresses are reported to alter pre-and post-synaptic gene expression (Kinnunen et al., 2003), decrease synaptic density in the hippocampus (Hayashi et al., 1998), and reduce the number of granule neurons and hippocampal neurogenesis (Lemaire et al., 2000).”
Pang, J., Hao, J., Gu, X., Zhang, L., Wang, W., Qin, Z. H., Feng, Q., Liu, C., Xie, H., Yang, S., et al. (2025) · Molecular Psychiatry · doi:10.1038/s41380-025-03258-9 · Cited by 6
Bailey, M. L., Nixon, C. J., Rusch, D. B., Buechlein, A. M., Rosvall, K. A., & Bentz, A. B. (2024) · Hormones and Behavior · doi:10.1016/j.yhbeh.2024.105561 · Cited by 5
Goudochnikov, V. I. (2023) · Journal of Endocrinological Science · doi:10.29245/2767-5157/2023/1.1125 · Cited by 5
Kurata, C., Ichihashi, Y., Onishi, M., Iinuma, M., Tamura, Y., Mori, D., & Kubo, K. (2012) · Pediatric Dental Journal · doi:10.1016/s0917-2394(12)70261-6 · Cited by 5
Perinatal effects of scorpion venoms: maternal and offspring development
Dorce, A. L. C., Martins, A. D. N., Dorce, V. A. C., & Nencioni, A. L. A. (2017) · The Journal of venomous animals and toxins including tropical diseases · doi:10.1186/s40409-017-0121-z · Cited by 5
“Several studies indicate that prenatal stress causes a significant reduction in the cellular proliferation; however, depending on the intensity of the stress, this neurogenesis can be suppressed or reinforced in specific cerebral areas [73, 74].”
BackgroundEffects of Tianeptine on Adult Rats Following Prenatal Stress
Lee, H.-Y., Kim, H., Kwon, J., Kim, Y. O., Seo, J., Lee, S., Cho, I.-H., & Kim, H. (2018) · Clinical Psychopharmacology and Neuroscience · doi:10.9758/cpn.2018.16.2.197 · Cited by 5
González, M. H., Maldonado, R., Hernández‐Arteaga, E., & Guevara, M. Á. (2021) · Stress · doi:10.1080/10253890.2021.1976140 · Cited by 5
“, 2012), learning (Lemaire et al., 2000), and memory, as a result of altered hippocampal development (Szuran et al.”
BackgroundStress périnatal et développement neuropsychologique
Cambonie, G., Novais, A. R. B., Bienfait, M., Pidoux, O., Toubin, R.-M., Picaud, J., & Barbanel, G. (2010) · Revue de médecine périnatale · doi:10.1007/s12611-010-0072-x · Cited by 5
The Effects of L-arginine on the Hippocampus of Male Rat Fetuses under Maternal Stress.
Mahmoudi, R., Enant, E., Delaviz, H., Rad, P., Roozbehi, A., Barmak, M. J., & Azizi, A. (2016) · Europe PMC (PubMed Central) · Cited by 5
Maternal Epigenetic Inheritance and Stress During Gestation
Kosten, T. A., & Nielsen, D. A. (2014) · Elsevier eBooks · doi:10.1016/b978-0-12-405944-3.00016-7 · Cited by 5
Treatment interventions following prenatal stress and neonatal cortical injury
Halliwell, C. (2011) · Open ULeth Scholarship (OPUS) (University of Lethbridge) · Cited by 5
Prenatal Programming of Depression and Schizophrenia?
Dafotakis, M., Vehoff, J., Korr, H., & Schmitz, C. (2002) · Neuroembryology and Aging · doi:10.1159/000063531 · Cited by 5
Bristow, G. C., Dong, E., Nwabuisi‐Heath, E., Gentile, S., Guidotti, A., & Sodhi, M. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.02.02.429408 · Cited by 5
Decreased hippocampal neurogenesis and post-stroke depression
Tang, X., Ran, L., & Li, W. (2026) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2026.1761408 · Cited by 5
Aryal, B., Maskey, D., Kim, M. J., Yang, J., & Kim, H. (2011) · Journal of Ginseng Research · doi:10.5142/jgr.2011.35.2.138 · Cited by 4
DOHaD : conséquences à long terme de la pathologie périnatale
Storme, L., Luton, D., Abdennebi‐Najar, L., & Huërou‐Luron, I. L. (2016) · médecine/sciences · doi:10.1051/medsci/20163201012 · Cited by 6
Prenatal and Early Postnatal Influences on Neurodevelopment: The Role of Epigenetics
Mariotti, V., Palumbo, S., & Pellegrini, S. (2019) · Springer eBooks · doi:10.1007/978-3-030-25816-0_6 · Cited by 5
Koehl, M., Ladevèze, E., Montcouquiol, M., & Abrous, D. N. (2022) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2022.844255 · Cited by 4
Self-citationRecio, P., Leibold, D. C., Crino, O. L., Wild, K. H., Friesen, C. R., Mauclaire, B., Peardon, A. Y., & Noble, D. W. A. (2025) · Animal Behaviour · doi:10.1016/j.anbehav.2025.123106 · Cited by 4
“Nonetheless, we cannot dismiss this possibility because dose effects can differ between tissues (Lemaire et al., 2000).”
InfluentialThe Interacting Neuroendocrine Network in Stress-Inducing Mood Disorders
Leff, P., Hernández, M. E., Becerril‐Villanueva, E., Martinez, C. B. D. R., Téllez-Santillán, C., Pérez-Tapia, M., Salazar, A., Antón, B., Berlanga, C., & Pavón, L. (2010) · The Open Neuroendocrinology Journal · doi:10.2174/1876528901003010180 · Cited by 5
“Is quite interesting that the incidence of depression occurs more frequent in females than in males, and several studies have demonstrated that estrogen hormones play a crucial role as a metabolic factor regulating cell proliferation [312].”
BackgroundTualang Honey Improves Memory and Prevents Hippocampal Changes in Prenatally Stressed Rats
Aziz, C. B. A., Hasim, H., Zakaria, R., & Ahmad, A. H. (2020) · Turkish Journal of Pharmaceutical Sciences · doi:10.4274/tjps.galenos.2019.21548 · Cited by 4
Smaga, I., Krzyżanowska, W., Pomierny, B., Maciejska, A., Skórkowska, A., Budziszewska, B., Pilc, A., & Nowak, G. (2022) · Springer eBooks · doi:10.1007/978-3-031-15080-7_176 · Cited by 5
Fňašková, M., Říha, P., Nečasová, M., Preiss, M., & Rektor, I. (2023) · Scientific Reports · doi:10.1038/s41598-023-40618-3 · Cited by 4
Interactions of Lead Exposure and Stress: Implications for Cognitive Dysfunction
Cory‐Slechta, D. A. (2005) · International review of research in mental retardation · doi:10.1016/s0074-7750(05)30003-6 · Cited by 4
The effect of chronic stress on prenatal development of the central nervous system
Giordana, L., Bozzo, A., Cots, D., Cobeta, I., Rolando, A. N., Borghi, D., Diaz, T., Gauna, H. F., & Romanini, M. (2014) · Biotechnic & Histochemistry · doi:10.3109/10520295.2014.976269 · Cited by 4
“Prenatal stress is an epigenetic factor that can cause changes in brain structure and function (Lemaire et al. 2000, Weinstock 2001).”
BackgroundLa neurogenèse dans le cerveau adulte et ses modifications en situations pathologiques
Rougier, A., & Auvergne, R. M. (2004) · Neurochirurgie · doi:10.1016/s0028-3770(04)98303-8 · Cited by 4
Maternal Chronic Stress Induces Premature Telencephalic Vesicles Development
Mugnaini, M. T., Soñez, C. A., Rolando, A. N., Romanini, M. C., Bozzo, A. A., Pastorino, I. C., Gauna, H. F., & Paz, D. A. (2006) · International Journal of Morphology · doi:10.4067/s0717-95022006000500001 · Cited by 4
“Several studies have provided powerful evidence to support a causal role for prenatal stress on alterations in the brain morphology and function (cognition, emotionality, and behavior) (Lemaire et al., 2000).”
BackgroundNeurogénesis hipocampal adulta y envejecimiento cognitivo
Moreno‐Fernández, R. D., Pedraza, C., & Gallo, M. (2013) · Escritos de Psicología / Psychological Writings · doi:10.24310/espsiescpsi.v6i3.13285 · Cited by 6
Neurogenesis: A Change of Paradigms
Mello, L. E., & Longo, B. M. (2009) · Springer eBooks · doi:10.1007/978-90-481-3375-8_2 · Cited by 4
“, 1999), hippocampal-dependent learning-tasks (Gould et al., 1999a; Lemaire et al., 2000), and voluntary physical activity (van Praag et al.”
BackgroundSchmidt, B. L., Santos, M. J., Cariaga-Martínez, A. E., Hill, L., Barloese, M. C. J., & Hall, Z. J. (2017) · Cited by 4
Sex-biased transgenerational effect of maternal stress on neurodevelopment and cognitive functions
Misra, P., & Ganesh, S. (2018) · Journal of Genetics · doi:10.1007/s12041-018-0928-6 · Cited by 4
“Whereas, in other studies it has been shown that prenatal stress induces reduction in adult neurogenesis in males (Lemaire et al. 2000; Mandyam et al. 2008; Morley-Fletcher et al. 2011; Belnoue et al. 2013; Madhyastha et al. 2013), but does not seem to affect the neurogenesis in females (Mandyam et…”
BackgroundHitoshi, S., Kippin, T. E., & van der Kooy, D. (2011) · Springer eBooks · doi:10.1007/978-4-431-53945-2_10 · Cited by 4
Fetale Hirnentwicklung und Programmierung von zerebralen Funktionsstörungen
Schwab, M. G. (2007) · Der Gynäkologe · doi:10.1007/s00129-007-1969-8 · Cited by 4
“Die dadurch induzierte verstärkte negative Rückkopplung der HHN-Achse führt zu einer verminderten Stresshormonausschüttung und in deren Folge zu einer verminderten Ängstlichkeit im weiteren Leben.”
BackgroundInfluentialNeural Stem Cells in the Adult Hippocampus
Ray, J., & Peterson, D. A. (2003) · Humana Press eBooks · doi:10.1007/978-1-59259-298-2_10 · Cited by 4
Developmental Effects of Selective Breeding for an Infant Trait
Brunelli, S. A., Zimmerberg, B., & Hofer, M. A. (2010) · Wiley eBooks · doi:10.1002/9781444327632.ch10 · Cited by 4
Traumatic Stress from a Multiple‐Levels‐of‐Analysis Perspective
Bremner, J. D. (2015) · Wiley eBooks · doi:10.1002/9780470939390.ch16 · Cited by 4
Neurogenesis in Human Hippocampus: Implications for Alzheimer Disease Pathogenesis
Castellani, R. J., Zhu, X., Lee, H., Perry, G. L., Smith, M. A., & Casadesús, G. (2006) · Neuroembryology and Aging · doi:10.1159/000118927 · Cited by 4
Cognitive processes are robust to early environmental conditions in two lizard species
Recio, P., Leibold, D. C., Crino, O. L., Wild, K. H., Friesen, C. R., Mauclaire, B., Peardon, A. Y., & Noble, D. W. A. (2025) · Behavioral Ecology · doi:10.1093/beheco/araf048 · Cited by 3
Prenatal stress alters transcription of NMDA-type glutamate receptors in the hippocampus
Buck, T. G., Dong, E., McCarthy, M., Guidotti, A., & Sodhi, M. (2024) · Neuroscience Letters · doi:10.1016/j.neulet.2024.137886 · Cited by 5
Flatt, E., & Alderman, S. L. (2024) · Journal of Experimental Biology · doi:10.1242/jeb.248020 · Cited by 3
Krank durch chronischen Stress
Krähenmann, R., & Seifritz, E. (2019) · DNP - Der Neurologe und Psychiater · doi:10.1007/s15202-019-2113-z · Cited by 3
“Dies sind vor allem der Hippocampus, die Amygdala, der anteriore cinguläre Kortex sowie der orbitofrontale Kortex [19, 20, 21].”
BackgroundInfluentialCan Adult Neurogenesis Be Considered as Neuroplasticity?
Famitafreshi, H., & Karimian, M. (2019) · Archives of Neuroscience · doi:10.5812/ans.79812 · Cited by 3
“The evidence that supports this theory is that many stress-exposed animals will eventually develop anxiety-related disorders (35).”
BackgroundElibol, B., Beker, M., Jakubowska-Doğru, E., & Kılıç, Ü. (2020) · The American Journal of Drug and Alcohol Abuse · doi:10.1080/00952990.2020.1780601 · Cited by 3
Koehl, M., Moal, M. L., & Abrous, D. N. (2011) · Springer eBooks · doi:10.1007/978-4-431-53945-2_4 · Cited by 2
Self-citationRole of Neurotoxicity in Depression
Smaga, I., Krzyżanowska, W., Pomierny, B., Budziszewska, B., Pilc, A., & Nowak, G. (2014) · Springer eBooks · doi:10.1007/978-1-4614-5836-4_176 · Cited by 3
Alterations of proliferation and differentiation of hippocampal cells in prenatally stressed rats
Sun, H., Su, Q., Zhang, H., Liu, W., Zhang, H., Ding, D., Zhu, Z., & Li, H. (2014) · Brain and Development · doi:10.1016/j.braindev.2014.09.007 · Cited by 3
Khoshnazar, A. K., Jahanshahi, M., & Azami, N. (2012) · International Journal of Morphology · doi:10.4067/s0717-95022012000100026 · Cited by 3
“There are so much data claiming importance of neurogenesis as it relates to the hippocampal functions of learning and memory (Kempermann, 2002; Lemaire et al., 2000; Leuner et al., 2006; Prickaerts et al., 2002; Shors et al., 2001; Snyder et al., 2005; Van Praag et al., 1999; Wiskott et al., 2006).”
BackgroundStudies of the Delayed Effects of Acute Prenatal Stress Evoked by Forced Swimming
Volodina, M. A., Sebentsova, E. A., Levitskaya, N. G., & Каменский, А. А. (2012) · Neuroscience and Behavioral Physiology · doi:10.1007/s11055-012-9575-1 · Cited by 3
“found negative influences with chronic prenatal stress on animals’ ability to learn [10, 12, 16, 21, 22].”
BackgroundTanaka, T., Wang, L., Kimura, M., Abe, H., Mizukami, S., Yoshida, T., & Shibutani, M. (2014) · Toxicological Sciences · doi:10.1093/toxsci/kfu266 · Cited by 3
Melatonin, a Neuroprotective Agent: Relevance for Stress-Induced Neuropsychiatric Disorders
Govitrapong, P., Ekthuwapranee, K., Ruksee, N., & Boontem, P. (2016) · Springer eBooks · doi:10.1007/978-81-322-2803-5_8 · Cited by 3
Mohammadi, M., Rohani, A. H., Yaghmaei, P., & Sahraei, M. (2021) · Basic and Clinical Neuroscience Journal · doi:10.32598/bcn.2021.15.12 · Cited by 3
“This deficit was accompanied by inhibiting neurogenesis in the hippocampus (Lemaire et al., 2000).”
BackgroundNeurogenesis in adult brain: understanding its mechanism and regulation
Zhao, X., Schaffer, D. V., & Gage, F. H. (2004) · Research and perspectives in neurosciences · doi:10.1007/978-3-642-18883-1_1 · Cited by 3
Lucassen, P. J., Scheper, W., & Someren, E. J. W. V. (2009) · Sleep Medicine Reviews · doi:10.1016/j.smrv.2008.12.004 · Cited by 3
Adult neurogenesis in rodents and primates: functional implications
(2005) · Techniques in the behavioral and neural sciences · doi:10.1016/s0921-0709(05)80038-0 · Cited by 3
When Genetic and Environmental Factors Meet in Modelling Autism
Pettie, M. A. (2020) · Open Access Victoria University of Wellington | Te Herenga Waka (Figshare) · doi:10.26686/wgtn.17148212.v1 · Cited by 4
Advance in the mechanisms underlying prenatal stress-induced depressive-like behavior in offspring
Xu, K., Song, D., Li, H., Lu, Y., & Zhu, Z. (2025) · Brain Behavior and Immunity Integrative · doi:10.1016/j.bbii.2025.100108 · Cited by 2
Pathological Mechanisms of Irradiation‐Induced Neurological Deficits in the Developing Brain
Richard, S. A. (2025) · European Journal of Neuroscience · doi:10.1111/ejn.70070 · Cited by 2
“Also, a decrease in the quantity of newly produced neurons in the hippocampus triggered learning and memory deficits (Czurkó et al. 1997; Lemaire et al. 2000).”
Prenatal conditions do not affect brain physiology and learning in a lizard
Recio, P., Leibold, D. C., Crino, O. L., Friesen, C. R., & Noble, D. W. A. (2025) · Journal of Experimental Biology · doi:10.1242/jeb.250716 · Cited by 2
“Factors such as age, sex or early-life conditions can have important effects on learning abilities (Amiel and Shine, 2012; Amiel et al., 2014; Carazo et al., 2014; Lemaire et al., 2000; Noble et al., 2014; Szuran et al., 1994; Zhu et al., 2004).”
Structural and Functional Brain Alterations Induced by Noise Exposure: A Comprehensive Review
Venegas-Mora, H. V., Ispanixtlahuatl-Meráz, O., Martínez-Fernández, D. E., Aguilar-García, I. G., & Fernández-Quezada, D. (2026) · NeuroSci · doi:10.3390/neurosci7040075 · Cited by 3
“This vulnerability is further exacerbated by early-life stress, which has been shown to accelerate age-related declines in hippocampal plasticity and cellular proliferation [24].”
Hormone Regulation of Neurogenesis Across the Lifespan
Duarte‐Guterman, P., Yagi, S., Epp, J. R., Brummelte, S., Wainwright, S. R., Barha, C. K., Chow, C., Barker, J. M., & Galea, L. A. M. (2016) · Elsevier eBooks · doi:10.1016/b978-0-12-803592-4.00108-5 · Cited by 2
Prenatal Influences on Cognitive Aging
de Rooij, S. R. (2020) · Cambridge University Press eBooks · doi:10.1017/9781108552684.027 · Cited by 2
Parental enriched environment: A look through key temporary windows
Mir, F. R., Renard, G. M., & Rivarola, M. A. (2023) · Journal of Neuroendocrinology · doi:10.1111/jne.13308 · Cited by 4
Iribarne, J., Brachetta, V., Kittlein, M. J., Schleich, C. E., & Zenuto, R. R. (2023) · Animal Cognition · doi:10.1007/s10071-023-01822-w · Cited by 3
“…and other hormones released by the mother in response to stress during pregnancy and lactation, as well as variations in maternal care, can negatively influence brain development in areas involved in spatial learning and memory (Lemaire et al. 2000; Yang et al. 2006; Lupien et al. 2009).”
Stress during first pregnancy increases seizure threshold in adult male offspring.
Pajand, P., Salmani, M. E., Shajiee, H., Abiri, H., Goudarzi, I., & Abrari, K. (2014) · Europe PMC (PubMed Central) · Cited by 2
Mobilization of Neural Stem Cells in the Adult Central Nervous System
Babu, H., Palmer, T. D., & Gage, F. H. (2012) · Springer eBooks · doi:10.1007/978-1-4614-3801-4_12 · Cited by 2
CNS Aspects of Prenatal Drug Exposure
Velı́šek, L. (2006) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1369.057 · Cited by 2
Densidad Neuronal en la Corteza Visual Primaria (Área 17), en Ratas Sometidas a Estrés Crónico
Olivares, R., Toledo, C., Vera, Y., Morgan, C., Pérez, H., Ortíz, A., Henríquez, M., Hernández, A., & Cifuentes, F. (2010) · International Journal of Morphology · doi:10.4067/s0717-95022010000300030 · Cited by 2
“Adicionalmente, se ha demostrado el rol del estrés prenatal, sobre eventuales alteraciones en la morfología cerebral y en funciones cognitivas, emocionales y conductuales (Lemaire et al., 2000).”
BackgroundBeneficial Effects of Flaxseed Oil (n-3 Fatty Acids) on Neurological Disorders
Farooqui, A. A. (2012) · Springer eBooks · doi:10.1007/978-1-4614-3804-5_3 · Cited by 2
Kriengwatana, B. P. (2013) · Scholarship@Western (Western University) · Cited by 2
Cortisol Reactivity Is Positively Related to Executive Function in Preschool
Blair, C., Granger, D. A., & Razza, R. A. (2005) · Cited by 2
Ramírez-Rodríguez, G. B., Ocaña-Fernández, M. D. Á., & Ortíz‐López, L. (2018) · Neural Plasticity · doi:10.1155/2018/4960869 · Cited by 2
Epigenetics and fructose metabolism: A new mechanism of fructose effects
Munetsuna, E., Yamazaki, M., Ohashi, K., & Yamada, H. (2019) · Elsevier eBooks · doi:10.1016/b978-0-12-849886-6.00010-0 · Cited by 2
Effect of Prenatal Stress on Offspring's Learning, Memory and Coping Strategies
Aghighi, F., Salami, M., & Talaei, S. A. (2019) · The Neuroscience Journal of Shefaye Khatam · doi:10.29252/shefa.7.4.106 · Cited by 2
Bhat, S., Shivappa, P., Pinto, J. R. T., Bernhardt, G. V., & Bernhardt, L. K. (2022) · Journal of South Asian Federation of Obstetrics and Gynaecology · doi:10.5005/jp-journals-10006-2072 · Cited by 2
Glucocorticoids and motivated behaviour
Lemaire, V., Piazza, P. V., & Moal, M. L. (2005) · Techniques in the behavioral and neural sciences · doi:10.1016/s0921-0709(05)80020-3 · Cited by 2
Self-citationGale, T., Garratt, M., & Brooks, R. C. (2019) · Physiology & Behavior · doi:10.1016/j.physbeh.2019.112678 · Cited by 2
Santoso, A. (2009) · Elektronische Hochschulschriften der LMU München (Ludwig-Maximilians-Universität München) · doi:10.5282/edoc.10676 · Cited by 2
Elevated glucocorticoid alters the developmental dynamics of hypothalamic neurogenesisPreprint
Eachus, H., Choi, M., Tochwin, A., Kaspareit, J., Ho, M., & Ryu, S. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.01.27.525966 · Cited by 2
Outcomes for Kittens Born to Free-Roaming Unowned Cats
Halls, V., Ellis, S. L. H., & Bessant, C. (2023) · Journal of Shelter Medicine and Community Animal Health · doi:10.56771/jsmcah.v2.57 · Cited by 1
Potapova, S., Isakov, Y., Tyulkova, E. I., & Vetrovoy, O. V. (2026) · International Journal of Molecular Sciences · doi:10.3390/ijms27062873 · Cited by 2
Role of hippocampal dentate granule cells in memory: neuronal birth timing matters
Blin, N., & Abrous, D. N. (2026) · Molecular Psychiatry · doi:10.1038/s41380-026-03745-7 · Cited by 1
Self-citationThe Logic of Developmental Psychoneuroimmunology
Coe, C. L., & Lubach, G. R. (2012) · Oxford University Press eBooks · doi:10.1093/oxfordhb/9780195394399.013.0002 · Cited by 1
Sharifabad, M. H., & Sabahi, A. A. R. (2014) · Europe PMC (PubMed Central) · Cited by 1
Un nouveau chapitre dans le domaine de la mémoire: la néo-neurogenèse hippocampique
Dupret, D., & Abrous, D. N. (2010) · Biologie Aujourd hui · doi:10.1051/jbio/2010004 · Cited by 2
Self-citationThe impact of prefertilization chronic mild stress on postnatal morphometric development
Cankara, N., Malas, M. A., Evcil, E. H., & Desdicioğlu, K. (2011) · The Journal of Maternal-Fetal & Neonatal Medicine · doi:10.3109/14767058.2011.566947 · Cited by 1
Adult neurogenesis in the dentate gyrus of the hippocampus: relationship to learning and memory
Escámez, F. A. N., & Moreno, M. (2011) · Archivos de Neurociencias · Cited by 1
Critical Age Windows for Neurodevelopmental Psychiatric Disorders: Evidence from Animal Models
Marco, E. M., Macrì, S., & Laviola, G. (2013) · Springer eBooks · doi:10.1007/978-1-4614-7264-3_31 · Cited by 1
Kempermann, G. (2010) · Oxford University Press eBooks · doi:10.1093/med/9780199729692.003.0009 · Cited by 1
Iribarne, J., Brachetta, V., Zenuto, R. R., Kittlein, M. J., & Schleich, C. E. (2023) · Behavioural Processes · doi:10.1016/j.beproc.2023.104981 · Cited by 1
Yanai, J., & Pinkas, A. (2010) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2010.04.010 · Cited by 1
IMPACT OF EARLY LIFE STRESS ON ANTI-DEPRESSANT SENSITIVITY
Vokina, V. A. (2021) · Ulyanovsk Medico-biological Journal · doi:10.34014/2227-1848-2021-1-123-132 · Cited by 1
Goran, M. I. (2016) · CRC Press eBooks · doi:10.1201/9781315370958-25 · Cited by 1
Metadata
- 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
- 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
- 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
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review