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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.
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“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).
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Diz-Chaves, Y., Pernía, O., Carrero, P., & García‐Segura, L. M. (2012) · Journal of Neuroinflammation · doi:10.1186/1742-2094-9-71 · Cited by 243
“In addition, prenatal stress produces an inhibition of neurogenesis in the dentate gyrus of the hippocampi in rats [31,32] and monkeys [45].”
BackgroundGondi, V., Hermann, B. P., Mehta, M. P., & Tomé, W. A. (2011) · International Journal of Radiation Oncology*Biology*Physics · doi:10.1016/j.ijrobp.2011.10.021 · Cited by 233
Heine, V. M., Zareno, J., Maslam, S., Joëls, M., & Lucassen, P. J. (2005) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2005.03951.x · Cited by 225
“Previous studies have firmly established a decreased proliferation in the DG of various species following short-lasting stress or GC exposure (Gould et al., 1991, 1997, 1998; Galea et al., 1997; Gould & Tanapat, 1999; Lemaire et al., 2000; Tanapat et al., 2001).”
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Levone, B. R., Cryan, J. F., & O'Leary, O. F. (2015) · Neurobiology of Stress · doi:10.1016/j.ynstr.2014.11.003 · Cited by 218
“…HPA axis activity, memory impairment (Fenoglio et al., 2006; Henry et al., 1994; Vallee et al., 1997) as well as reduced hippocampal neurogenesis in both rodents (Lucassen et al., 2009; Lemaire et al., 2000; Mandyam et al., 2008) and non-human primates (Coe et al., 2003) later in adult life.”
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Malberg, J. E. (2004) · Journal of Psychiatry and Neuroscience · doi:10.1139/jpn.0422 · Cited by 217
Cognitive side effects of cancer therapy demonstrate a functional role for adult neurogenesis
Monje, M., & Dietrich, J. (2011) · Behavioural Brain Research · doi:10.1016/j.bbr.2011.05.012 · Cited by 217
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Mueller, B. R., & Bale, T. L. (2007) · Physiology & Behavior · doi:10.1016/j.physbeh.2007.01.017 · Cited by 222
Lucassen, P. J., Stumpel, M. W., Wang, Q., & Aronica, E. (2010) · Neuropharmacology · doi:10.1016/j.neuropharm.2010.01.012 · Cited by 223
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Self-citationOwen, D., Andrews, M. H., & Matthews, S. G. (2004) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2004.10.004 · Cited by 211
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Self-citationEarly-life adversity and brain development: Is the microbiome a missing piece of the puzzle?
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BackgroundResultGlucocorticoid hormones and early brain development in schizophrenia
Ph.D., J. (2002) · Neuropsychopharmacology · doi:10.1016/s0893-133x(01)00396-7 · Cited by 199
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Dunn, G. A., Morgan, C. P., & Bale, T. L. (2011) · Hormones and Behavior · doi:10.1016/j.yhbeh.2010.05.004 · Cited by 198
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Guzmán‐Marín, R., Suntsova, N., Stewart, D. R., Gong, H., Szymusiak, R., & McGinty, D. (2003) · The Journal of Physiology · doi:10.1113/jphysiol.2003.041665 · Cited by 197
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Self-citationSon, G. H., Geum, D., Chung, S., Kim, E. J., Jo, J., Kim, C.-M., Lee, K. H., Kim, H., Choi, S., Kim, H. T., et al. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.3850-05.2006 · Cited by 185
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Lupien, S. J., Evans, A., Lord, C., Miles, J., Pruessner, M., Pike, B., & Pruessner, J. C. (2007) · NeuroImage · doi:10.1016/j.neuroimage.2006.09.041 · Cited by 167
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“Likewise, learning and running have been shown to increase the number of new neurons in the hippocampus (Gould et al., 1999a; Lemaire et al., 2000) and to improve performance on hippocampusdependent tasks (Van Praag et al.”
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“While several studies have related new neuron number and cognitive measures in aged rats (Drapeau et al., 2003, 2007; Driscoll et al., 2006; Lemaire et al., 2000), dogs (Siwak-Tapp et al., 2007), and nonhuman primates (Aizawa et al., 2009), the strength of this relationship among aged rats tested…”
2006 Curt P. Richter award winner
DeVries, A. C., Craft, T. K. S., Glasper, E. R., Neigh, G. N., & Alexander, J. K. (2007) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2007.04.007 · Cited by 153
Fournier, N. M., & Duman, R. S. (2011) · Behavioural Brain Research · doi:10.1016/j.bbr.2011.04.022 · Cited by 159
Inflammation and neuronal plasticity: a link between childhood trauma and depression pathogenesis
Cattaneo, A., Macchi, F., Plazzotta, G., Veronica, B., Bocchio-Chiavetto, L., Riva, M. A., & Pariante, C. M. (2015) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2015.00040 · Cited by 152
“Deregulation of microglia function has been associated with neurologic and psychiatric diseases and may lead to critical changes in neuronal activity and function (Beumer et al., 2012; Stertz et al., 2013; Paolicelli et al., 2014; Najjar and Pearlman, 2015).”
BackgroundKoo, J. W., Park, C. H., Choi, S. H., Kim, N. J., Kim, H., Choe, J. C., & Suh, Y. (2003) · The FASEB Journal · doi:10.1096/fj.02-1032fje · Cited by 155
“Experimental animal models have shown that prenatal stress has longlasting effects on cognitive function of adult offspring throughout the entire life of the animals, by inducing structural and morphological changes in the brain ( 11 , 16).”
BackgroundInfluentialLee, S. W., Clemenson, G. D., & Gage, F. H. (2011) · Behavioural Brain Research · doi:10.1016/j.bbr.2011.10.009 · Cited by 164
Yun, J., Koike, H., Ibi, D., Tóth, E., Mizoguchi, H., Nitta, A., Yoneyama, M., Ogita, K., Yoneda, Y., Nabeshima, T., et al. (2010) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2010.06893.x · Cited by 158
“1999), it is generally accepted that stress impairs memory in rodents and the increased levels of circulating glucocorticoids inhibit memory in rodents (Lemaire et al. 2000; Montaron et al. 2006).”
BackgroundGABAA receptor-acting neurosteroids: a role in the development and regulation of the stress response
Gunn, B. G., Cunningham, L., Mitchell, S. G., Swinny, J. D., Lambert, J. J., & Belelli, D. (2015) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2014.06.001 · Cited by 149
“Thus, various models of prenatal stress exhibit cognitive and emotional deficits that associate with a long lasting impairment of hippocampal neurogenesis (Lemaire et al., 2000; Lucassen et al., 2009; Korosi et al., 2012).”
Epigenetic effects of stress and corticosteroids in the brain
Hunter, R. G. (2012) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2012.00018 · Cited by 150
“…produce exaggerated corticosterone responses to stress and a number of deficits in hippocampal structure and function (Fujioka et al., 1999; Lemaire et al., 2000; Coe et al., 2003), while milder exposures produce a more resilient phenotype, resembling neonatal handling (Fujioka et al.,…”
BackgroundBlondeau, N., Nguemeni, C., Debruyne, D. N., Piens, M., Wu, X., Pan, H., Hu, X., Gandin, C., Lipsky, R. H., Plumier, J.-C., et al. (2009) · Neuropsychopharmacology · doi:10.1038/npp.2009.84 · Cited by 154
“…that the mechanisms of antidepressants are related to several mechanisms of neuroplasticity, ranging from changes in gene expression (including neurotrophic mechanisms) to synaptic transmission and plasticity, and neurogenesis (Lemaire et al, 2000; Shors et al, 2001; Racagni and Popoli, 2008).”
Background3D neuronal mitochondrial morphology in axons, dendrites, and somata of the aging mouse hippocampus
Faitg, J., Lacefield, C., Davey, T., White, K., Laws, R., Kosmidis, S., Reeve, A. K., Kandel, E. R., Vincent, A. E., & Picard, M. A. (2021) · Cell Reports · doi:10.1016/j.celrep.2021.109509 · Cited by 139
“, 2006), whereas with aging the DG exhibits a decline in the neurogenesis of granule cells (Bondareff and Geinisman, 1976; Lemaire et al., 2000).”
Learning and adult neurogenesis: Survival with or without proliferation?
Prickaerts, J. (2003) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2003.09.001 · Cited by 149
Stress and Anxiety Across the Lifespan: Structural Plasticity and Epigenetic Regulation
Hunter, R. G., & McEwen, B. S. (2013) · Epigenomics · doi:10.2217/epi.13.8 · Cited by 142
Critical age windows for neurodevelopmental psychiatric disorders: evidence from animal models
Marco, E. M., Macrì, S., & Laviola, G. (2011) · Neurotoxicity Research · doi:10.1007/s12640-010-9205-z · Cited by 144
Low-dose or low-dose-rate ionizing radiation–induced bioeffects in animal models
Tang, F. R., Loke, W. K., & Khoo, B. C. (2016) · Journal of Radiation Research · doi:10.1093/jrr/rrw120 · Cited by 143
“At different maturation stages, newly generated neurons in the dentate gyrus have distinct contributions to learning and memory, and events that decrease neurogenesis impair animal performance in learning and memory [36, 37] (Table 3).”
BackgroundMorley‐Fletcher, S., Mairesse, J., Soumier, A., Banasr, M., Fagioli, F., Gabriel, C., Mocaër, E., Daszuta, A., McEwen, B. S., Nicoletti, F., et al. (2011) · Psychopharmacology · doi:10.1007/s00213-011-2280-x · Cited by 149
“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 (Darnaudery et al. 2006; Koehl…”
Neurodevelopmental damage after prenatal infection: role of oxidative stress in the fetal brain
Lanté, F., Meunier, J., Guiramand, J., Maurice, T., Cavalier, M., de Jesus Ferreira, M.-C., Aimar, R., Cohen-Solal, C., Vignes, M., & Barbanel, G. (2007) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2007.01.027 · Cited by 140
“Indeed, severe immobilization stress to pregnant rats produced deficits in spatial learning [67] and in LTP [68] in the offspring, together with a remodeling of NMDA receptors, with a relative decrease in the NR2B and increase in the NR2A subunits.”
BackgroundKodas, E., Vancassel, S., Lejeune, B., Guilloteau, D., & Chalon, S. (2002) · Journal of Lipid Research · doi:10.1194/jlr.m200132-jlr200 · Cited by 146
“esis has already been proposed for various environmental agents such as early exposure to neurotoxic agents (53) or to stress (54).”
BackgroundLucassen, P. J., Bosch, O. J., Jousma, E., Krömer, S. A., Andrew, R., Seckl, J. R., & Neumann, I. D. (2008) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2008.06543.x · Cited by 140
“For example, PS chronically programs exaggerated responses to stress, including HPA axis hyper-reactivity (Henry et al., 1994), increased anxiety, and impaired social and cognitive behaviors (Lemaire et al., 2000; Weinstock, 2007).”
BackgroundInfluentialMechanisms of Shared Vulnerability to Post-traumatic Stress Disorder and Substance Use Disorders
Maria-Rios, C. E., & Morrow, J. D. (2020) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2020.00006 · Cited by 164
Schmitz, C., Rhodes, M. E., Bludau, M., Kaplan, S., Ong, P., Ueffing, I., Vehoff, J., Korr, H., & Frye, C. A. (2002) · Molecular Psychiatry · doi:10.1038/sj.mp.4001118 · Cited by 140
Docosahexaenoic Acid and Arachidonic Acid Nutrition in Early Development
Carlson, S. E., & Colombo, J. A. (2016) · Advances in Pediatrics · doi:10.1016/j.yapd.2016.04.011 · Cited by 139
“Maternal environment can meaningfully affect even the earliest processes of central nervous system development, including neurogenesis [51], neuronal migration [52], and synaptogenesis [53].”
How age, sex and genotype shape the stress response
Novais, A., Monteiro, S., Roque, S., Correia‐Neves, M., & Sousa, N. (2016) · Neurobiology of Stress · doi:10.1016/j.ynstr.2016.11.004 · Cited by 152
“Prenatally stressed males exhibit impairments on learning-induced neurogenesis (Lemaire et al., 2000), and reduced hippocampal long-term potentiation (LTP), together with increased long-term depression (LTD) (Yang et al., 2006), which potentially correlates with the alterations reported on…”
Learning by embryos and the ghost of predation future
Mathis, A., Ferrari, M. C. O., Windel, N. L., Messier, F., & Chivers, D. P. (2008) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2008.0754 · Cited by 136
Stem Cell Review Series: Role of neurogenesis in age‐related memory disorders
Drapeau, E., & Abrous, D. N. (2008) · Aging Cell · doi:10.1111/j.1474-9726.2008.00369.x · Cited by 148
“(Lemaire et al., 2000) Rat SD Male 1, 3, 10, 22 months DG #BrdU cells: 1 m > 3 m > 10 m > 22 m”
BackgroundInfluentialSelf-citationIshiwata, H., Shiga, T., & Okado, N. (2005) · Neuroscience · doi:10.1016/j.neuroscience.2005.03.048 · Cited by 138
Kim, H. K., Lee, S., Kim, S., Yoo, J. B., & Kim, C. (2007) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2007.03.003 · Cited by 138
“Recent studies suggested that prenatal stress during pregnancy decreases spatial memory of the offspring (Lemaire et al., 2000; Kim et al., 2006).”
BackgroundMandyam, C. D., & Koob, G. F. (2012) · Trends in Neurosciences · doi:10.1016/j.tins.2011.12.005 · Cited by 139
Yeh, C.-M., Huang, C., & Hsu, K. (2011) · The Journal of Physiology · doi:10.1113/jphysiol.2011.222042 · Cited by 130
“We focused specifically on the hippocampus because it is a primary target brain area for PS (Uno et al. 1989; Lemaire et al. 2000).”
BackgroundFukuda, A., Fukuda, H., Swanpalmer, J., Hertzman, S., Lannering, B., Márky, I., Björk‐Eriksson, T., & Blomgren, K. (2004) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2004.02894.x · Cited by 135
“It has been suggested that a reduction in the number of newly generated neurons in the hippocampus induces learning and memory deficits (Czurko et al. 1997; Lemaire et al. 2000; Shors et al. 2001).”
Background
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
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