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
Prolonged glucocorticoid exposure reduces hippocampal neuron number: implications for aging
Sapolsky, R., Krey, L., & McEwen, B. (1985) · The Journal of Neuroscience · doi:10.1523/jneurosci.05-05-01222.1985 · Cited by 1,129
Woolley, C. S., Gould, E., & McEwen, B. S. (1990) · Brain Research · doi:10.1016/0006-8993(90)90778-a · Cited by 1,020
Adult neurogenesis is regulated by adrenal steroids in the dentate gyrus
Cameron, H. A., & Gould, E. (1994) · Neuroscience · doi:10.1016/0306-4522(94)90224-0 · Cited by 999
Unbiased Stereology. Three‐Dimensional Measurement in Microscopy.
Sandau, K. (1999) · Journal of Microscopy · doi:10.1046/j.1365-2818.1999.0429a.x · Cited by 890
Stress and hippocampal neurogenesis
Gould, E., & Tanapat, P. (1999) · Biological Psychiatry · doi:10.1016/s0006-3223(99)00247-4 · Cited by 818
Spatial selectivity of unit activity in the hippocampal granular layer
Jung, M. W., & McNaughton, B. L. (1993) · Hippocampus · doi:10.1002/hipo.450030209 · Cited by 789
(1992) · Cited by 777
Nowakowski, R. S., Lewin, S. B., & Miller, M. W. (1989) · Journal of Neurocytology · doi:10.1007/bf01190834 · Cited by 755
Time-dependent reorganization of brain circuitry underlying long-term memory storage
Bontempi, B., Laurent-Demir, C., Destrade, C., & Jaffard, R. (1999) · Nature · doi:10.1038/23270 · Cited by 673
Preserved neuron number in the hippocampus of aged rats with spatial learning deficits.
Rapp, P. R., & Gallagher, M. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.18.9926 · Cited by 658
Adrenal hormones suppress cell division in the adult rat dentate gyrus
Gould, E., Cameron, H. A., Daniels, D., Woolley, C. S., & McEwen, B. (1992) · Journal of Neuroscience · doi:10.1523/jneurosci.12-09-03642.1992 · Cited by 652
Brezun, J. M., & Daszuta, A. (1999) · Neuroscience · doi:10.1016/s0306-4522(98)00693-9 · Cited by 549
Does Prenatal Stress Impair Coping and Regulation of Hypothalamic-Pituitary-Adrenal Axis?
Weinstock, M. (1997) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(96)00014-0 · Cited by 539
Prenatal Stress Increases the Hypothalamo‐Pituitary‐Adrenal Axis Response in Young and Adult Rats
Henry, C., Kabbaj, M., Simon, H., Moal, M. L., & Maccari, S. (1994) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.1994.tb00591.x · Cited by 528
Brain Aging Correlates: Retardation by Hormonal-Pharmacological Treatments
Landfield, P. W., Baskin, R. K., & Pitler, T. (1981) · Science · doi:10.1126/science.6270791 · Cited by 522
Sandi, C., Loscertales, M., & Guaza, C. (1997) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.1997.tb01412.x · Cited by 447
Neurogenesis in adulthood: a possible role in learning
Gould, E. (1999) · Trends in Cognitive Sciences · doi:10.1016/s1364-6613(99)01310-8 · Cited by 432
Evidence that granule cells generated in the dentate gyrus of adult rats extend axonal projections
Stanfield, B. B., & Trice, J. (1988) · Experimental Brain Research · doi:10.1007/bf00250261 · Cited by 431
McNaughton, B. L., Barnes, C. A., Meltzer, J., & Sutherland, R. J. (1989) · Experimental Brain Research · doi:10.1007/bf00248904 · Cited by 388
Vallée, M., Maccari, S., Dellu-Hagedorn, F., Simon, H., Moal, M. L., & Mayo, W. (1999) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.1999.00705.x · Cited by 386
Age-related production of new granule cells in the adult dentate gyrus
Seki, T., & Arai, Y. (1995) · Neuroreport · doi:10.1097/00001756-199512150-00010 · Cited by 386
Memory impaired aged rats: No loss of principal hippocampal and subicular neurons
Rasmussen, T., Schliemann, T., Sørensen, J. C. H., Zimmer, J., & West, M. J. (1996) · Neurobiology of Aging · doi:10.1016/0197-4580(95)02032-2 · Cited by 349
Effects of prenatal stress on vulnerability to stress in prepubertal and adult rats
Fride, E., Dan, Y., Feldon, J., Halevy, G., & Weinstock, M. (1986) · Physiology & Behavior · doi:10.1016/0031-9384(86)90172-1 · Cited by 295
Maternal stress induces synaptic loss and developmental disabilities of offspring
Hayashi, A., Nagaoka, M., Yamada, K., Ichitani, Y., Miake, Y., & Okado, N. (1998) · International Journal of Developmental Neuroscience · doi:10.1016/s0736-5748(98)00028-8 · Cited by 241
On the number of neurons in the dentate gyrus of the rat
Boss, B. D., Peterson, G. M., & Cowan, W. M. (1985) · Brain Research · doi:10.1016/0006-8993(85)90257-4 · Cited by 178
Behavioural trait of reactivity to novelty is related to hippocampal neurogenesis
Lemaire, V., Aurousseau, C., Moal, M. L., & Abrous, D. N. (1999) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.1999.00833.x · Cited by 150
Self-citationSchwegler, H., & Crusio, W. E. (1995) · Behavioural Brain Research · doi:10.1016/0166-4328(95)91998-3 · Cited by 132
Adrenalectomy increases neurogenesis but not PSA‐NCAM expression in aged dentate gyrus
Montaron, M., Petry, K. G., Rodriguez, J. J., Marinelli, M., Aurousseau, C., Rougon, G., Moal, M. L., & Abrous, D. N. (1999) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.1999.00579.x · Cited by 131
Self-citationSchöpke, R., Wolfer, D. P., Lipp, H., & Leisinger-Trigona, M.-C. (1991) · Hippocampus · doi:10.1002/hipo.450010322 · Cited by 121
Regulation of 5‐HT receptors by corticosteroids: where do we stand?
Chaouloff, F. (1995) · Fundamental and Clinical Pharmacology · doi:10.1111/j.1472-8206.1995.tb00289.x · Cited by 112
Rodriguez, J. J., Montaron, M., Petry, K. G., Aurousseau, C., Marinelli, M., Premier, S., Rougon, G., Moal, M. L., & Abrous, D. N. (1998) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.1998.00316.x · Cited by 96
Self-citationChapman, R. H., & Stern, J. M. (1978) · Journal of Comparative and Physiological Psychology · doi:10.1037/h0077509 · Cited by 86
Lordi, B., Protais, P., Mellier, D., & Caston, J. (1997) · Physiology & Behavior · doi:10.1016/s0031-9384(97)00261-8 · Cited by 84
Water maze performance and hippocampal weight of prenatally stressed rats
Szuran, T. F., Zimmermann, E., & Welzl, H. (1994) · Behavioural Brain Research · doi:10.1016/0166-4328(94)90100-7 · Cited by 77
Vaid, R. R., Yee, B. K., Shalev, U., Rawlins, J. N. P., Weiner, I., Feldon, J., & Totterdell, S. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-14-05599.1997 · Cited by 53
Drug-Induced Adrenal Hypertrophy Provides Evidence for Reset in the Adrenocortical System*
Akana, S. F., Shinsako, J., & Dallman, M. F. (1983) · Endocrinology · doi:10.1210/endo-113-6-2232 · Cited by 37
Adrenal axis activation by chronic social stress fails to inhibit gonadal function in male rats
Lemaire, V., Taylor, G. T., & Mormède, P. (1997) · Psychoneuroendocrinology · doi:10.1016/s0306-4530(97)00051-6 · Cited by 26
Self-citationIncremental Progress in Developmental Psychopathology: Simply Complex
Leckman, J. F. (1999) · American Journal of Psychiatry · doi:10.1176/ajp.156.10.1495 · Cited by 5
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
Effects of stress throughout the lifespan on the brain, behaviour and cognition
Lupien, S. J., McEwen, B. S., Gunnar, M. R., & Heim, C. (2009) · Nature Reviews Neuroscience · doi:10.1038/nrn2639 · Cited by 6,256
Mechanisms and Functional Implications of Adult Neurogenesis
Zhao, C., Deng, W., & Gage, F. H. (2008) · Cell · doi:10.1016/j.cell.2008.01.033 · Cited by 3,007
Functional neurogenesis in the adult hippocampus
van Praag, H., Schinder, A. F., Christie, B. R., Toni, N., Palmer, T. D., & Gage, F. H. (2002) · Nature · doi:10.1038/4151030a · Cited by 2,853
Neural consequences of enviromental enrichment
van Praag, H., Kempermann, G., & Gage, F. H. (2000) · Nature Reviews Neuroscience · doi:10.1038/35044558 · Cited by 2,468
Exercise enhances learning and hippocampal neurogenesis in aged mice
van Praag, H., Shubert, T., Zhao, C., & Gage, F. H. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.1731-05.2005 · Cited by 2,078
“In addition, exercise enhances hippocampal neurogenesis (van Praag et al., 1999a,b; Fabel et al., 2003; Farmer et al., 2004), a process that may contribute to cognition (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
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