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Differential effects of prenatal stress on the morphological maturation of hippocampal neurons
Abstract
The present study was designed to clarify an intensity-dependent effect of prenatal stress on the morphological development of hippocampal neurons in rats. In addition, the involvement of receptors for glucocorticoids, i.e. mineralocorticoid receptors and glucocorticoid receptors, in stress-induced changes in the morphology of hippocampal neurons was examined by an in vitro pharmacological approach. The effects of mild prenatal stress on neurogenesis and long-term potentiation in the hippocampus were also investigated in adult offspring. Prenatal stress affected the morphological development of the hippocampus in an intensity-dependent manner. Short-lasting, mild prenatal stress enhanced neonatal neurogenesis and differentiation of processes of hippocampal neurons, whereas long-lasting, severe stress impaired their morphology. Mineralocorticoid receptor was found to mediate enhancement of neurogenesis and differentiation of processes of cultured hippocampal neurons. In contrast, glucocorticoid receptor was involved in the suppression of their morphology. Short-lasting, mild prenatal stress, which has previously been shown to enhance learning performance in adult offspring, facilitated neurogenesis and long-term potentiation in the adult hippocampus. These findings suggest that prenatal stress has enhancing and suppressing effects on the development of hippocampal neurons depending on intensity, and that mineralocorticoid receptors and glucocorticoid receptors contribute to stress-induced morphological changes.
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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 Fujioka et al., 2006
In the citing paper
“Our findings are consistent with accumulating evidence from animal studies that medial temporal and prefrontal cortical regions are shaped by early experience (e.g. Coe et al., 2003; Salm et al., 2004; Fujioka et al., 2006; Murmu 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 Fujioka et al., 2006
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Cites
Bliss, T. V. P., & Gardner-Medwin, A. R. (1973) · The Journal of Physiology · doi:10.1113/jphysiol.1973.sp010274 · Cited by 7,424
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
Brain corticosteroid receptor balance in health and disease
de Kloet, E. R., Vreugdenhil, E., Oitzl, M. S., & Joëls, M. (1998) · Endocrine Reviews · doi:10.1210/edrv.19.3.0331 · Cited by 2,614
Neurogenesis in the adult is involved in the formation of trace memories
Shors, T. J., Miesegaes, G. R., Beylin, A. V., Zhao, M., Rydel, T. A., & Gould, E. (2001) · Nature · doi:10.1038/35066584 · Cited by 2,014
Adult neurogenesis produces a large pool of new granule cells in the dentate gyrus
Cameron, H. A., & Mckay, R. D. G. (2001) · Journal of Comparative Neurology · doi:10.1002/cne.1040 · Cited by 1,585
Lemaire, V., Koehl, M., Le Moal, M., & Abrous, D. N. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.20.11032 · Cited by 1,044 · cited 2×
“Recent studies have shown that stress during pregnancy interferes with hippocampal neurogenesis in adult offspring (Lemaire et al., 2000; Coe et al., 2003).”
BackgroundMirescu, C., & Gould, E. (2006) · Hippocampus · doi:10.1002/hipo.20155 · Cited by 701
Effects of Adult Neurogenesis on Synaptic Plasticity in the Rat Dentate Gyrus
Snyder, J. S., Kee, N., & Wojtowicz, J. M. (2001) · Journal of Neurophysiology · doi:10.1152/jn.2001.85.6.2423 · Cited by 633
Long-term potentiation of the perforant path-granule cell synapse in the rat hippocampus
Douglas, R. M., & Goddard, G. V. (1975) · Brain Research · doi:10.1016/0006-8993(75)90697-6 · Cited by 521
Brain damage induced by prenatal exposure to dexamethasone in fetal rhesus macaques. I. Hippocampus
Uno, H., Lohmiller, L., Thieme, C. S., Kemnitz, J. W., Engle, M. J., Roecker, E. B., & Farrell, P. M. (1990) · Developmental Brain Research · doi:10.1016/0165-3806(90)90002-g · Cited by 503
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Li, M., Li, X., Zhang, X., Ren, J., Jiang, H., Wang, Y., Ma, Y., & Cheng, W. (2014) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2014.02.004 · Cited by 10
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Briones, B. A., & Gould, E. (2019) · Elsevier eBooks · doi:10.1016/b978-0-12-813146-6.00007-2 · Cited by 9
Verma, V., Kumari, R., & Singaravel, M. (2022) · Chronobiology International · doi:10.1080/07420528.2021.2023561 · Cited by 8
Gestational protein restriction alters early amygdala neurochemistry in male offspring
Torres, D. B., Lopes, A., Rodrigues, A. J., Lopes, M. G., Ventura‐Silva, A. P., Sousa, N., Gontijo, J. A. R., & Boer, P. A. (2022) · Nutritional Neuroscience · doi:10.1080/1028415x.2022.2131064 · Cited by 7
Madhyastha, S., Somayaji, S., Bairy, K., Prakash, P., & Madhyastha, P. (2007) · Cited by 7
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Segal, D., Lin, Y.-S., Ginsberg, G., & Sonawane, B. R. (2015) · Human and Ecological Risk Assessment An International Journal · doi:10.1080/10807039.2014.992852 · Cited by 7
Effect of corticosterone on developing hippocampus: Short‐term and long‐term outcomes
He, W., Zhao, M., Machida, T., & Chen, N. (2008) · Hippocampus · doi:10.1002/hipo.20523 · Cited by 7
Jameie, S. B., Mousavi, M., Farhadi, M., Mehraein, F., Ababzadeh, S., Soleimani, M., Kerdari, M., & Jalilpouraghdam, M. (2015) · Thrita · doi:10.5812/thrita.36420 · Cited by 6
Fan, X., Zhao, Z., Huang, Z., Wu, M., Wang, D., & Xiao, J. (2022) · The World Journal of Biological Psychiatry · doi:10.1080/15622975.2022.2082524 · Cited by 6
Semenoff-Segundo, A., Semenoff, T. A. D. V., Borges, Á. H., Pedro, F. L. M., Caporossi, L. S., & Bosco, Á. F. (2011) · Archives of Oral Biology · doi:10.1016/j.archoralbio.2011.10.018 · Cited by 6
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Çelik, K., Bilim, P., Garip, G., Durmaz, B., Sözmen, E. Y., & Baka, M. (2021) · International Journal of Developmental Neuroscience · doi:10.1002/jdn.10162 · Cited by 5
Gutierrez, V. A., Carrillo, A. A., Boersma, G. J., Tamashiro, K. L., Moran, T. H., Iñiguez, S. D., & Treesukosol, Y. (2022) · Neuroscience Letters · doi:10.1016/j.neulet.2022.136818 · Cited by 9
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Schmidt, B. L., Santos, M. J., Cariaga-Martínez, A. E., Hill, L., Barloese, M. C. J., & Hall, Z. J. (2017) · Cited by 4
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Pereira, S. P., Grilo, L. F., Tavares, R. S., Gomes, R. M., Ramalho‐Santos, J., Ozanne, S. E., & Matafome, P. N. (2022) · Elsevier eBooks · doi:10.1016/b978-0-12-823761-8.00031-8 · Cited by 1
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Cleary-Gaffney, M. (2015) · Maynooth University ePrints and eTheses Archive (Maynooth University)
No relationship between vertebral column shifts and limb fluctuating asymmetry in human foetuses
ten Broek, C. M. A., Bots, J., Bugiani, M., Galis, F. F., & Dongen, S. V. (2017) · PeerJ · doi:10.7717/peerj.3359
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Paric, A. (2014) · Carleton University's Institutional Repository (MacOdrum Library, Carleton University) · doi:10.22215/etd/2014-10435
MicroRNAs and the Response to Stress
Hollins, S. L., & Cairns, M. J. (2020) · Elsevier eBooks · doi:10.1016/b978-0-12-813156-5.00003-0
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Aguilera, M. D. L. Á. G. (2012) · doi:10.24275/uami.0r967389h
Lafuente, J. V., & Argandoña, E. (2013) · Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature · doi:10.3410/f.718163818.793486163
Changes in the Hippocampus of the Bank Vole Due to Population Density Dynamics
Yaskin, V. A. (2022) · Biology Bulletin · doi:10.1134/s1062359022020157
86th SIBS National Congress | Palermo, Italy, 24-25 October 2013
Editors, T. (2015) · Journal of Biological Research - Bollettino della Società Italiana di Biologia Sperimentale · doi:10.4081/jbr.2015.5161
Grigoletti-Lima, G. B., Boer, P. A., & Gontijo, J. A. R. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.05.30.596620
Alcigir, M. E., Ozkan, O., Demirel, M. A., Turkmen, M. B., & Fatih (2024) · Indian Journal of Experimental Biology · doi:10.56042/ijeb.v62i08.4976
Laaradia, M. A., Oufquir, S., Laadraoui, J., Gabbas, Z. E., Tazart, Z., Daoudi, M., Yazouli, L. E., & Chait, A. (2025) · Toxicon · doi:10.1016/j.toxicon.2025.108328
Functions of the Mineralocorticoid Receptor in the Hippocampus.
Rozeboom, A. M. (2008) · Deep Blue (University of Michigan)
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Grilo, L. F., Mota, S. I., Cox, L. A., & Oliveira, P. J. (2026) · Elsevier eBooks · doi:10.1016/b978-0-443-33841-0.00005-1
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Metadata
- Authors
- Fujioka, A., Fujioka, T., Ishida, Y., Maekawa, T., & Nakamura, S.
- Affiliations
- Yamaguchi University (JP)
- Corresponding author
- Fujioka, T.
- Nakamura, S.
- Venue
- Neuroscience
- Publisher
- Elsevier BV
- Published
- 2006
- Volume
- 141
- Issue
- 2
- Pages
- 907-915
- ISSN
- 0306-4522 (ISSN-L)
- OpenAlex
- W2051951421
- Cited by
- 165
- References
- 33
- Citations by year
- 2026: 2 · 2025: 3 · 2024: 3 · 2023: 1 · 2022: 9 · 2021: 7 · 2020: 6 · 2019: 3 · 2018: 4 · 2017: 15 · 2016: 9 · 2015: 14 · 2014: 18 · 2013: 8 · 2012: 12
- FWCI
- 3.55
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Keywords
- prenatal stress, hippocampal neurons, neuronal morphology, neurogenesis, mineralocorticoid receptor, glucocorticoid receptor, glucocorticoids, long-term potentiation, stress intensity, adult offspring, learning performance, hippocampal development
- MeSH terms
- Animals, Bromodeoxyuridine, Cell Differentiation, Cells, Cultured, Electric Stimulation, Embryo, Mammalian, Female, Glucocorticoids, Hippocampus, Immunohistochemistry, Microtubule-Associated Proteins, Neurons, Phosphopyruvate Hydratase, Pregnancy, Prenatal Exposure Delayed Effects, Stress, Physiological, Time Factors, Tubulin, Silver Staining, Rats, Sprague-Dawley, Long-Term Potentiation, Cell Size, Rats
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