Effect of varied gestational stress on acquisition of spatial memory, hippocampal LTP and synaptic proteins in juvenile male rats
Abstract
Some but not other forms of prenatal stress have been shown to impair spatial memory in adult male offspring. It is not clear if this is because of the intensity of the stress, age of rats, or the way in which learning is assessed. We examined the effect of daily varied prenatal stress consisting of 30 min restraint, saline injections and 15 min forced swim on day 17-21 of gestation on spatial learning, synaptic plasticity and the expression of key proteins of the post synaptic density (PSD) in the hippocampus of males aged 4-5 weeks. Prenatal stress impaired spatial learning in the Morris water maze and induced a significant decrease in long-term potentiation (LTP) in hippocampal slices. There was no change in the paired pulse facilitation ratio but there was a significant reduction in the expression of the NR2B subunit of the glutamate type NMDA receptor and the GluR1 subunit of the AMPA receptor, both of which are important modulators of LTP. These changes were accompanied by a remarkable increase in the scaffolding protein PSD95, which interacts with the intracellular carboxy terminal domains of the NR2 subunits. The high levels of PSD95 may have contributed to the impairment of LTP by disrupting the clustering of NMDA receptors in CA1 synapses. The alteration by prenatal stress in the relative amounts of scaffolding proteins and those which compose glutamate receptors could explain the depression of LTP and impairment in the acquisition of spatial learning.
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Prenatal stress can alter synaptic plasticity by impairing long-term potentiation and facilitating long-term depression.
“Furthermore, prenatal stress has the potential to alter synaptic plasticity by impairing long-term potentiation but facilitating long-term depression (Yaka et al., 2007; Yang et al., 2007).”
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 Yaka et al., 2007
Cites
A synaptic model of memory: long-term potentiation in the hippocampus
Bliss, T. V. P., & Collingridge, G. L. (1993) · Nature · doi:10.1038/361031a0 · Cited by 11,566 · see citing works
Malenka, R. C., & Bear, M. F. (2004) · Neuron · doi:10.1016/j.neuron.2004.09.012 · Cited by 3,968 · see citing works
Monyer, H., Burnashev, N., Laurie, D. J., Sakmann, B., & Seeburg, P. H. (1994) · Neuron · doi:10.1016/0896-6273(94)90210-0 · Cited by 2,989 · see citing works
Long-Term Potentiation--A Decade of Progress?
Malenka, R. C., & Nicoll, A. R. A. (1999) · Science · doi:10.1126/science.285.5435.1870 · Cited by 2,729 · see citing works
Domain Interaction Between NMDA Receptor Subunits and the Postsynaptic Density Protein PSD-95
Kornau, H., Schenker, L. T., Kennedy, M. B., & Seeburg, P. H. (1995) · Science · doi:10.1126/science.7569905 · Cited by 1,882 · see citing works
Genetic enhancement of learning and memory in mice
Tang, Y., Shimizu, E., Dubé, G., Rampon, C., Kerchner, G. A., Zhuo, M., Liu, G., & Tsien, J. Z. (1999) · Nature · doi:10.1038/43432 · Cited by 1,867 · see citing works
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 · see citing works
Shi, S.-H., Hayashi, Y., Esteban, J. A., & Malinow, R. (2001) · Cell · doi:10.1016/s0092-8674(01)00321-x · Cited by 1,094 · see citing works
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 · see citing works
Alterations induced by gestational stress in brain morphology and behaviour of the offspring
Weinstock, M. (2001) · Progress in Neurobiology · doi:10.1016/s0301-0082(01)00018-1 · Cited by 791 · see citing works
Self-citationImportance of AMPA Receptors for Hippocampal Synaptic Plasticity But Not for Spatial Learning
Zamanillo, D., Sprengel, R., Hvalby, Ø., Jensen, V., Burnashev, N., Rozov, A., Kaiser, K. M. M., Köster, H. J., Borchardt, T., Worley, P., et al. (1999) · Science · doi:10.1126/science.284.5421.1805 · Cited by 791 · see citing works
Vallée, M., Mayo, W., Dellu-Hagedorn, F., Moal, M. L., Simon, H., & Maccari, S. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-07-02626.1997 · Cited by 772 · see citing works
Postsynaptic signaling and plasticity mechanisms
Sheng, M., & Kim, M. J. (2002) · Science · doi:10.1126/science.1075333 · Cited by 731 · see citing works
Weinstock, M. (2005) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2004.09.006 · Cited by 706 · see citing works
Self-citationFunctional and Pharmacological Differences Between Recombinant N -Methyl- d -Aspartate Receptors
Vicini, S., Wang, J. F., Li, J. H., Zhu, W. J., Wang, Y. H., Luo, J. H., Wolfe, B. B., & Grayson, D. R. (1998) · Journal of Neurophysiology · doi:10.1152/jn.1998.79.2.555 · Cited by 674 · see citing works
Adoption reverses the long-term impairment in glucocorticoid feedback induced by prenatal stress
Maccari, S., Piazza, P., Kabbaj, M., Barbazanges, A., Simon, H., & Moal, M. L. (1995) · Journal of Neuroscience · doi:10.1523/jneurosci.15-01-00110.1995 · Cited by 574 · see citing works
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 · see citing works
Self-citationPrenatal stress and long-term consequences: implications of glucocorticoid hormones
Maccari, S., Darnaudéry, M., Morley‐Fletcher, S., Zuena, A. R., Cinque, C., & Reeth, O. V. (2003) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(03)00014-9 · Cited by 529 · see citing works
Behavioral stress impairs long-term potentiation in rodent hippocampus
Foy, M. R., Stanton, M. E., Levine, S., & Thompson, R. F. (1987) · Behavioral and Neural Biology · doi:10.1016/s0163-1047(87)90664-9 · Cited by 436 · see citing works
Identification of PSD-95 as a Regulator of Dopamine-Mediated Synaptic and Behavioral Plasticity
Yao, W., Gainetdinov, R. R., Arbuckle, M. I., Sotnikova, T. D., Cyr, M., Beaulieu, J., Torres, G. E., Grant, S. G. N., & Caron, M. G. (2004) · Neuron · doi:10.1016/s0896-6273(04)00048-0 · Cited by 380 · see citing works
Isgor, C., Kabbaj, M., Akil, H., & Watson, S. J. (2004) · Hippocampus · doi:10.1002/hipo.10207 · Cited by 341 · see citing works
Src Activation in the Induction of Long-Term Potentiation in CA1 Hippocampal Neurons
Lu, Y. M., Roder, J., Davidow, J. S., & Salter, M. W. (1998) · Science · doi:10.1126/science.279.5355.1363 · Cited by 328 · see citing works
A developmental switch in the signaling cascades for LTP induction
Yasuda, H., Barth, A. L., Stellwagen, D., & Malenka, R. C. (2003) · Nature Neuroscience · doi:10.1038/nn985 · Cited by 325 · see citing works
NMDA receptors: from genes to channels
Sucher, N. J., Awobuluyi, M., Choi, Y., & Lipton, S. A. (1996) · Trends in Pharmacological Sciences · doi:10.1016/s0165-6147(96)80008-3 · Cited by 316 · see citing works
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 · see citing works
Self-citationMurmu, M. S., Salomon, S., Biala, Y., Weinstock, M., Braun, K., & Bock, J. (2006) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2006.05024.x · Cited by 278 · see citing works
Self-citationClayton, D. A., Mesches, M. H., Álvarez, E., Bickford, P. C., & Browning, M. D. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-09-03628.2002 · Cited by 258 · see citing works
Szuran, T. F., Pliška, V., Pokorny, J., & Welzl, H. (2000) · Physiology & Behavior · doi:10.1016/s0031-9384(00)00351-6 · Cited by 253 · see citing works
Wyllie, D. J. A., Béhé, P., & Colquhoun, D. (1998) · The Journal of Physiology · doi:10.1111/j.1469-7793.1998.001bz.x · Cited by 235 · see citing works
Son, 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 · see citing works
Köhr, G., Jensen, V., Koester, H. J., Mihaljević, A. L., Utvik, J. K., Kvello, A., Ottersen, O. P., Seeburg, P. H., Sprengel, R., & Hvalby, Ø. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-34-10791.2003 · Cited by 181 · see citing works
A Facilitative Role for Corticosterone in the Acquisition of a Spatial Task Under Moderate StressPreprint
Akirav, I., Kozenicky, M., Tal, D., Sandi, C., Venero, C., & Richter‐Levin, G. (2004) · Learning & Memory · doi:10.1101/lm.61704 · Cited by 170 · see citing works
Differential effects of prenatal stress on the morphological maturation of hippocampal neurons
Fujioka, A., Fujioka, T., Ishida, Y., Maekawa, T., & Nakamura, S. (2006) · Neuroscience · doi:10.1016/j.neuroscience.2006.04.046 · Cited by 165 · see citing works
Richardson, H. N., Zorrilla, E. P., Mandyam, C. D., & RIVIER, C. L. (2006) · Endocrinology · doi:10.1210/en.2005-1054 · Cited by 161 · see citing works
Prenatal stress modifies hippocampal synaptic plasticity and spatial learning in young rat offspring
Yang, J., Han, H., Cao, J., Li, L., & Xu, L. (2006) · Hippocampus · doi:10.1002/hipo.20181 · Cited by 161 · see citing works
Scaffolding of Fyn Kinase to the NMDA Receptor Determines Brain Region Sensitivity to Ethanol
Yaka, R., Phamluong, K., & Ron, D. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-09-03623.2003 · Cited by 141 · see citing works
Self-citationEffects of maternal stress during pregnancy on forced swimming test behavior of the offspring
Alonso, S. J., Arévalo, R., Afonso, D., & Rodrı́guez, M. (1991) · Physiology & Behavior · doi:10.1016/0031-9384(91)90538-y · Cited by 135 · see citing works
Proteomics of the nervous system
Husi, H., & Grant, S. G. N. (2001) · Trends in Neurosciences · doi:10.1016/s0166-2236(00)01792-6 · Cited by 134 · see citing works
Mild prenatal stress enhances learning performance in the non-adopted rat offspring
Fujioka, T., Fujioka, A., Tan, N., Chowdhury, G. M. I., Mouri, H., Sakata, Y., & Nakamura, S. (2001) · Neuroscience · doi:10.1016/s0306-4522(00)00582-0 · Cited by 130 · see citing works
Lateral amygdaloid nucleus expansion in adult rats is associated with exposure to prenatal stress
Salm, A. K., Pavelko, M., Krouse, E. M., Webster, W., Kraszpulski, M., & Birkle, D. L. (2004) · Developmental Brain Research · doi:10.1016/j.devbrainres.2003.11.005 · Cited by 125 · see citing works
Corticosterone shifts different forms of synaptic potentiation in opposite directions
Krugers, H. J., Alfarez, D. N., Karst, H., Parashkouhi, K., van Gemert, N., & Joëls, M. (2005) · Hippocampus · doi:10.1002/hipo.20092 · Cited by 88 · see citing works
Cannizzaro, C., Plescia, F., Martire, M., Gagliano, M., Cannizzaro, G., Mantia, G., & Cannizzaro, E. (2006) · Behavioural Brain Research · doi:10.1016/j.bbr.2005.12.010 · Cited by 85 · see citing works
Chronic Prenatal Stress Affects Development and Behavioral Depression in Rats
Secoli, S. R., & Teixeira, N. A. (1998) · Stress · doi:10.3109/10253899809167291 · Cited by 80 · see citing works
PSD‐95 is a negative regulator of the tyrosine kinase Src in the NMDA receptor complex
Kalia, L. V., Pitcher, G. M., Pelkey, K. A., et al. (2006) · The EMBO Journal · doi:10.1038/sj.emboj.7601342 · Cited by 72 · see citing works
Fast NMDA Receptor–Mediated Synaptic Currents in Neurons From Mice Lacking the ε2 (NR2B) Subunit
Tovar, K. R., Sprouffske, K., & Westbrook, G. L. (2000) · Journal of Neurophysiology · doi:10.1152/jn.2000.83.1.616 · Cited by 70 · see citing works
Kamphuis, P. J. G. H., Gardoni, F., Kamal, A., Croiset, G., Bakker, J. M., Cattabeni, F., Gispen, W. H., van Bel, F., Luca, M. D., & Wiegant, V. M. (2003) · The FASEB Journal · doi:10.1096/fj.02-0333fje · Cited by 66 · see citing works
Meunier, J., Gué, M., Récasens, M., & Maurice, T. (2004) · British Journal of Pharmacology · doi:10.1038/sj.bjp.0705835 · Cited by 49 · see citing works
Poltyrev, T., & Weinstock, M. (1999) · Stress · doi:10.3109/10253899909001114 · Cited by 15 · see citing works
Self-citationThe role of prenatal stress in the programming of behavior
Weinstock, M. (2005) · CRC Press eBooks · doi:10.1201/b14625-24 · Cited by 13 · see citing works
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Schwabe, L., Joëls, M., Roozendaal, B., Wolf, O. T., & Oitzl, M. S. (2012) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2011.07.002 · Cited by 714 · see citing works
Buss, C., Davis, E. P., Muftuler, L. T., Head, K., & Sandman, C. A. (2010) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2009.07.010 · Cited by 435 · see citing works
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Weinstock, M. (2017) · Neurobiology of Stress · doi:10.1016/j.ynstr.2016.08.004 · Cited by 264 · see citing works
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- Authors
- Yaka, R., Salomon, S., Matzner, H., & Weinstock, M.
- Affiliations
- Hebrew University of Jerusalem (IL)
- Corresponding author
- Weinstock, Marta
- Venue
- Behavioural Brain Research
- Publisher
- Elsevier BV
- Published
- 2007-04
- Volume
- 179
- Issue
- 1
- Pages
- 126-132
- ISSN
- 0166-4328 (ISSN-L)
- OpenAlex
- W2003772211
- Cited by
- 120
- References
- 49
- Citations by year
- 2025: 5 · 2024: 2 · 2023: 4 · 2022: 4 · 2021: 2 · 2020: 3 · 2019: 6 · 2018: 5 · 2017: 6 · 2016: 11 · 2015: 7 · 2014: 10 · 2013: 11 · 2012: 6
- FWCI
- 3.58
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Behavioural Brain Research (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Keywords
- prenatal stress, spatial learning, hippocampus, long-term potentiation, synaptic plasticity, postsynaptic density, PSD-95, NR2B subunit, glutamate receptors, restraint stress, forced swim test, Morris water maze
- MeSH terms
- Analysis of Variance, Animals, Critical Period, Psychological, Cytoskeletal Proteins, Female, Hippocampus, Male, Neuronal Plasticity, Pregnancy, Prenatal Exposure Delayed Effects, Random Allocation, Reaction Time, Spatial Behavior, Stress, Psychological, Synapses, Rats, Wistar, Receptors, Glutamate, Long-Term Potentiation, Maze Learning, Rats
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