Maternal care determines rapid effects of stress mediators on synaptic plasticity in adult rat hippocampal dentate gyrus
Abstract
Maternal care in the rat influences hippocampal development, synaptic plasticity and cognition. Previous studies, however, have examined animals under minimally stressful conditions. Here we tested the hypothesis that maternal care influences hippocampal function differently when this structure is exposed to corticosteroid and noradrenergic hormones, which are elevated during the early phase of a stress response. In the adult male offspring of Long-Evans dams characterised as high or low in maternal care (high LG and low LG) we (1) examined basal dendritic morphology in the dentate gyrus by Golgi staining; (2) investigated rapid modulation of in vitro long term-potentiation (LTP) in the dentate gyrus by glucocorticoid and beta-adrenergic stimulation; (3) examined hippocampal and amygdala-dependent learning under stress using contextual and cued fear conditioning. We found differences in hippocampal dentate gyrus morphology in adult offspring of high and low LG mothers, with less dendritic complexity in low LG offspring. Under basal conditions LTP was lower in slices from low compared with high LG offspring. Hippocampal LTP was rapidly increased by either corticosterone (100 nM) or isoproterenol (1.0 microM) in low LG offspring, suggesting improved dentate plasticity during stress. This was mirrored in hippocampal but not amygdala-dependent learning, as low LG offspring showed enhanced contextual but not cued fear conditioning. We suggest that decreased pup LG during postnatal life may be adaptive in high-threat environments, potentially enhancing hippocampal function in the offspring under conditions of adversity.
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The physiological and morphological changes induced by low-quality maternal care in rats enhance learning and memory under stressful conditions.
“they actually enhance learning and memory processes under stressful conditions”
From The Adaptive Calibration Model of stress responsivity (2011) · cites this paper as Bagot et al., 2009
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
Epigenetic programming by maternal behavior
Weaver, I. C. G., Cervoni, N., Champagne, F. A., D'Alessio, A. C., Sharma, S., Seckl, J. R., Dymov, S., Szyf, M., & Meaney, M. J. (2004) · Nature Neuroscience · doi:10.1038/nn1276 · Cited by 6,177 · see citing works
Self-citationHandbook of attachment: theory, research, and clinical applications
(1999) · Choice Reviews Online · doi:10.5860/choice.37-1841 · Cited by 5,386 · see citing works
Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning.
Phillips, R. G., & LeDoux, J. E. (1992) · Behavioral Neuroscience · doi:10.1037/0735-7044.106.2.274 · Cited by 3,292 · see citing works
Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning.
Phillips, R. G., & LeDoux, J. E. (1992) · Behavioral Neuroscience · doi:10.1037//0735-7044.106.2.274 · Cited by 3,262 · see citing works
Liu, D., Diorio, J., Tannenbaum, B., Caldji, C., Francis, D., Freedman, A., Sharma, S., Pearson, D., Plotsky, P. M., & Meaney, M. J. (1997) · Science · doi:10.1126/science.277.5332.1659 · Cited by 3,170 · see citing works
Self-citationLong-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
Meaney, M. J. (2001) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.24.1.1161 · Cited by 2,708 · see citing works
Self-citationSTRESS AND HIPPOCAMPAL PLASTICITY
McEwen, B. S. (1999) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.22.1.105 · Cited by 2,087 · see citing works
Maternal Effects As Adaptations
(1998) · doi:10.1093/oso/9780195111637.001.0001 · Cited by 1,673 · see citing works
Caldji, C., Tannenbaum, B., Sharma, S., Francis, D., Plotsky, P. M., & Meaney, M. J. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.9.5335 · Cited by 1,437 · see citing works
Self-citationMaternal care, hippocampal synaptogenesis and cognitive development in rats
Liu, D., Diorio, J., Day, J. C., Francis, D. D., & Meaney, M. J. (2000) · Nature Neuroscience · doi:10.1038/77702 · Cited by 1,195 · see citing works
Self-citationMetaplasticity: tuning synapses and networks for plasticity
Abraham, W. C. (2008) · Nature reviews. Neuroscience · doi:10.1038/nrn2356 · Cited by 1,119 · see citing works
Crouching as an index of fear.
Blanchard, R. J., & Blanchard, D. C. (1969) · Journal of Comparative and Physiological Psychology · doi:10.1037/h0026779 · Cited by 1,077 · see citing works
Champagne, F. A., Francis, D. D., Mar, A., & Meaney, M. J. (2003) · Physiology & Behavior · doi:10.1016/s0031-9384(03)00149-5 · Cited by 1,021 · see citing works
Spatial memory, recognition memory, and the hippocampus
Broadbent, N. J., Squire, L. R., & Clark, R. E. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0406344101 · Cited by 985 · see citing works
Potential role of childrearing practices in the development of anxiety and depression
Rapee, R. M. (1997) · Clinical Psychology Review · doi:10.1016/s0272-7358(96)00040-2 · Cited by 985 · see citing works
Dentate gyrus NMDA receptors mediate rapid pattern separation in the hippocampal network
McHugh, T. J., Jones, M. W., Quinn, J. J., Balthasar, N., Coppari, R., Elmquist, J. K., Lowell, B. B., Fanselow, M. S., Wilson, M. A., & Tonegawa, S. (2007) · Science · doi:10.1126/science.1140263 · Cited by 958 · see citing works
Weaver, I. C. G., Champagne, F. A., Brown, S. E., Dymov, S., Sharma, S., Meaney, M. J., & Szyf, M. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.3652-05.2005 · Cited by 905 · see citing works
Self-citationPlasticity of the Hippocampus: Adaptation to Chronic Stress and Allostatic Load
McEwen, B. S. (2001) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2001.tb05830.x · Cited by 875 · see citing works
Champagne, D. L., Bagot, R. C., van Hasselt, F., Ramakers, G., Meaney, M. J., de Kloet, E. R., Joels, M., & Krugers, H. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.0526-08.2008 · Cited by 661 · see citing works
Self-citationChampagne, F. A., & Meaney, M. J. (2006) · Biological Psychiatry · doi:10.1016/j.biopsych.2005.10.016 · Cited by 510 · see citing works
Self-citationTransgenic inhibition of synaptic transmission reveals role of CA3 output in hippocampal learning
Nakashiba, T., Young, J. Z., McHugh, T. J., Buhl, D. L., & Tonegawa, S. (2008) · Science · doi:10.1126/science.1151120 · Cited by 492 · see citing works
Behavioral stress modifies hippocampal plasticity through N-methyl-D-aspartate receptor activation.
Kim, J. J., Foy, M. R., & Thompson, R. F. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.10.4750 · Cited by 435 · see citing works
Corticosteroid effects in the brain: U-shape it
Joëls, M. (2006) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2006.03.007 · Cited by 408 · see citing works
Self-citationParental 'Affectionless Control' as an Antecedent to Adult Depression: A Risk Factor Delineated
Parker, G. (1983) · Archives of General Psychiatry · doi:10.1001/archpsyc.1983.01790080038005 · Cited by 408 · see citing works
Development of antisocial and prosocial behavior
Eysenck, H. J. (1987) · Personality and Individual Differences · doi:10.1016/0191-8869(87)90201-7 · Cited by 371 · see citing works
Protein kinase A regulates calcium permeability of NMDA receptors
Skeberdis, V. A., Chevaleyre, V., Lau, C. G., Goldberg, J. H., Pettit, D. L., Suadicani, S. O., Lin, Y., Bennett, M. V. L., Yuste, R., Castillo, P. E., et al. (2006) · Nature Neuroscience · doi:10.1038/nn1664 · Cited by 332 · see citing works
Cameron, N. M., Champagne, F. A., Parent, C., Fish, E. W., Ozaki-Kuroda, K., & Meaney, M. J. (2005) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2005.03.022 · Cited by 320 · see citing works
Self-citationMaternal Care, Gene Expression, and the Development of Individual Differences in Stress Reactivity
Francis, D. D., Champagne, F. A., Liu, D., & Meaney, M. J. (1999) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1999.tb08106.x · Cited by 291 · see citing works
Self-citationGestational stress induces post-partum depression-like behaviour and alters maternal care in rats
Smith, J. W., Seckl, J. R., Evans, A. T., Costall, B., & Smythe, J. W. (2003) · Psychoneuroendocrinology · doi:10.1016/s0306-4530(03)00025-8 · Cited by 289 · see citing works
The stress hormone corticosterone conditions AMPAR surface trafficking and synaptic potentiation
Groc, L., Choquet, D., & Chaouloff, F. (2008) · Nature Neuroscience · doi:10.1038/nn.2150 · Cited by 280 · see citing works
A selective role for corticosterone in contextual-fear conditioning
Pugh, C. R., Tremblay, D., Fleshner, M., & Rudy, J. W. (1997) · Behavioral Neuroscience · doi:10.1037/0735-7044.111.3.503 · Cited by 272 · see citing works
Bredy, T. W., Humpartzoomian, R., Cain, D. P., & Meaney, M. J. (2003) · Neuroscience · doi:10.1016/s0306-4522(02)00918-1 · Cited by 248 · see citing works
Self-citationCaldji, C., Diorio, J. C., & Meaney, M. J. (2003) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300237 · Cited by 241 · see citing works
Self-citationBeiko, J., Lander, R., Hampson, E., Boon, F. H., & Cain, D. P. (2003) · Behavioural Brain Research · doi:10.1016/j.bbr.2003.08.019 · Cited by 229 · see citing works
Wilensky, A. E., Schafe, G. E., & LeDoux, J. E. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-24-j0006.1999 · Cited by 217 · see citing works
Diamond, D. M., Campbell, A. M., Park, C. R., Woodson, J. C., Conrad, C. D., Bachstetter, A. D., & Mervis, R. F. (2006) · Hippocampus · doi:10.1002/hipo.20188 · Cited by 213 · see citing works
A Golgi-Cox morphological analysis of neuronal changes induced by environmental enrichment
Faherty, C. J., Kerley, D. A., & Smeyne, R. J. (2003) · Developmental Brain Research · doi:10.1016/s0165-3806(02)00642-9 · Cited by 210 · see citing works
Bredy, T. W., Zhang, T. Y., Grant, R. J., Diorio, J., & Meaney, M. J. (2004) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2004.03599.x · Cited by 196 · see citing works
Roozendaal, B., Hui, G. K., HUI, I., Berlau, D. J., McGaugh, J. L., & Weinberger, N. M. (2006) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2006.03.003 · Cited by 191 · see citing works
Structural changes at dendritic spine synapses during long-term potentiation
Harris, K. M., Fiala, J. C., & Ostroff, L. (2003) · Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences · doi:10.1098/rstb.2002.1254 · Cited by 180 · see citing works
Takahashi, T., Kimoto, T., Tanabe, N., Hattori, T., Yasumatsu, N., & Kawato, S. (2002) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.2002.01251.x · Cited by 176 · see citing works
Zhang, T. Y., Chrétien, P., Meaney, M. J., & Gratton, A. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.3293-04.2005 · Cited by 174 · see citing works
Self-citationDynamics and plasticity in developing neuronal networks in vitro
van Pelt, J., Vajda, I., Wolters, P. S., et al. (2004) · Progress in brain research · doi:10.1016/s0079-6123(04)47013-7 · Cited by 170 · 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
Boekhoorn, K., Terwel, D., Biemans, B. A. M., Borghgraef, P., Wiegert, O., Ramakers, G. J. A., de Vos, K., Krugers, H. J., Tomiyama, T., Mori, H., et al. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.5425-05.2006 · Cited by 167 · see citing works
Self-citationWiegert, O., Joëls, M., & Krugers, H. (2006) · Learning & Memory · doi:10.1101/lm.87706 · Cited by 162 · see citing works
Self-citationAdrenal stress hormones, amygdala activation, and memory for emotionally arousing experiences
Roozendaal, B., Barsegyan, A., & Lee, S. (2007) · Progress in Brain Research · doi:10.1016/s0079-6123(07)67006-x · Cited by 154 · see citing works
The Role and Mechanisms of Action of Glucocorticoid Involvement in Memory Storage
Sandi, C. (1998) · Neural Plasticity · doi:10.1155/np.1998.41 · Cited by 149 · see citing works
Kavushansky, A., Vouimba, R., Cohen, H., & Richter‐Levin, G. (2006) · Hippocampus · doi:10.1002/hipo.20130 · Cited by 141 · see citing works
Leuner, B., & Shors, T. J. (2004) · Molecular Neurobiology · doi:10.1385/mn:29:2:117 · Cited by 138 · see citing works
Hernández-Rabaza, V., Hontecillas-Prieto, L., Velázquez-Sánchez, C., Ferragud, A., Pérez-Villaba, A., Arcusa, A., Barcia, J. A., Trejo, J. L., & Canales, J. J. (2008) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2008.06.008 · Cited by 114 · see citing works
Wiegert, O., Pu, Z., Shor, S., Joëls, M., & Krugers, H. (2005) · Neuroscience · doi:10.1016/j.neuroscience.2005.05.039 · Cited by 87 · see citing works
Self-citationKomatsuzaki, Y., Murakami, G., Tsurugizawa, T., Mukai, H., Tanabe, N., Mitsuhashi, K., Kawata, M., Kimoto, T., Ooishi, Y., & Kawato, S. (2005) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2005.07.173 · Cited by 87 · see citing works
Pu, Z., Krugers, H. J., & Joëls, M. (2007) · Learning & Memory · doi:10.1101/lm.527207 · Cited by 72 · see citing works
Self-citationVouimba, R., Yaniv, D., & Richter‐Levin, G. (2006) · Neuropharmacology · doi:10.1016/j.neuropharm.2006.07.007 · Cited by 70 · see citing works
Toki, S., Morinobu, S., Imanaka, A., Yamamoto, S., Yamawaki, S., & Honma, K. (2007) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2007.05288.x · Cited by 69 · see citing works
MENARD, J., & Hakvoort, R. A. (2006) · Behavioural Brain Research · doi:10.1016/j.bbr.2006.10.014 · Cited by 62 · see citing works
Potential role of synaptopodin in spine motility by coupling actin to the spine apparatus
Deller, T., Mundel, P. H., & Frotscher, M. (2000) · Hippocampus · doi:10.1002/1098-1063(2000)10:5 · Cited by 61 · see citing works
Schenberg, E. E., & Oliveira, M. G. M. (2008) · Hippocampus · doi:10.1002/hipo.20475 · Cited by 40 · see citing works
Ray, D. L., de Sevilla, D. F., Porto-Pazos, A. B., et al. (2004) · Hippocampus · doi:10.1002/hipo.20021 · Cited by 40 · see citing works
Alfarez, D. N., Karst, H., Velzing, E. H., Joëls, M., & Krugers, H. J. (2007) · Hippocampus · doi:10.1002/hipo.20360 · Cited by 39 · see citing works
Self-citationVos, P., Kaufmann, D., Hand, P. J., et al. (1990) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.87.13.5114 · Cited by 15 · see citing works
Ratzliff, A., & Soltész, I. (2000) · Hippocampus · doi:10.1002/(sici)1098-1063(2000)10:2 · Cited by 14 · see citing works
Wiegert, O., Joëls, M., & Krugers, H. J. (2007) · Progress in brain research · doi:10.1016/s0079-6123(07)67021-6 · Cited by 12 · see citing works
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The Adaptive Calibration Model of stress responsivity
Del Giudice, M., Ellis, B. J., & Shirtcliff, E. A. (2011) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2010.11.007 · Cited by 1,373 · see citing works
Epigenetics and the biological definition of gene×environment interactions
Meaney, M. J. (2010) · Child Development · doi:10.1111/j.1467-8624.2009.01381.x · Cited by 1,239 · see citing works
Self-citationThe evolutionary basis of risky adolescent behavior: Implications for science, policy, and practice.
Ellis, B. J., Del Giudice, M., Dishion, T. J., Figueredo, A. J., Gray, P., Griskevicius, V., Hawley, P. H., Jacobs, W. J., James, J., Volk, A. A., et al. (2012) · Developmental Psychology · doi:10.1037/a0026220 · Cited by 745 · see citing works
Pathogenesis of depression: Insights from human and rodent studies
Ménard, C., Hodes, G. E., & Russo, S. J. (2016) · Neuroscience · doi:10.1016/j.neuroscience.2015.05.053 · Cited by 593 · see citing works
Daskalakis, N. P., Bagot, R. C., Parker, K. J., Vinkers, C. H., & de Kloet, E. R. (2013) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2013.06.008 · Cited by 579 · see citing works
Self-citationEpigenetics and the environmental regulation of the genome and its function
Zhang, T.-Y., & Meaney, M. J. (2010) · Annual Review of Psychology · doi:10.1146/annurev.psych.60.110707.163625 · Cited by 565 · see citing works
Self-citationEarly life stress and development: potential mechanisms for adverse outcomes
Smith, K. E., & Pollak, S. D. (2020) · Journal of Neurodevelopmental Disorders · doi:10.1186/s11689-020-09337-y · Cited by 500 · see citing works
Mismatch or cumulative stress: Toward an integrated hypothesis of programming effects
Nederhof, E., & Schmidt, M. V. (2012) · Physiology & Behavior · doi:10.1016/j.physbeh.2011.12.008 · Cited by 363 · see citing works
Perinatal iron deficiency and neurocognitive development
Radlowski, E. C., & Johnson, R. W. (2013) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2013.00585 · Cited by 315 · see citing works
“This process is not restricted to early developmental periods because it is also necessary for reshaping neural circuitry during experience-dependent learning throughout life (i.e., synaptic plasticity; Figure 1; Bagot et al., 2009).”
BackgroundEarly-life experience, epigenetics, and the developing brain
Kundakovic, M., & Champagne, F. A. (2015) · Neuropsychopharmacology · doi:10.1038/npp.2014.140 · Cited by 304 · see citing works
Beyond allostatic load: Rethinking the role of stress in regulating human development
Ellis, B. J., & Del Giudice, M. (2014) · Development and Psychopathology · doi:10.1017/s0954579413000849 · Cited by 290 · see citing works
Epigenetic Mechanisms of Depression and Antidepressant Action
Vialou, V., Feng, J., Robison, A. J., & Nestler, E. J. (2013) · Annual Review of Pharmacology and Toxicology · doi:10.1146/annurev-pharmtox-010611-134540 · Cited by 277 · see citing works
DNA methylation and childhood maltreatment: From animal models to human studies
Lutz, P.-E., & Turecki, G. (2014) · Neuroscience · doi:10.1016/j.neuroscience.2013.07.069 · Cited by 236 · see citing works
Maternal high fat diet consumption during the perinatal period programs offspring behavior
Sullivan, E. L., Nousen, E. K., & Chamlou, K. A. (2014) · Physiology & Behavior · doi:10.1016/j.physbeh.2012.07.014 · Cited by 217 · see citing works
Early-life stress mediated modulation of adult neurogenesis and behavior
Korosi, A., Naninck, E. F. G., Oomen, C. A., Schouten, M., Krugers, H., Fitzsimons, C., & Lucassen, P. J. (2012) · Behavioural Brain Research · doi:10.1016/j.bbr.2011.07.037 · Cited by 194 · see citing works
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Georgieff, M. K., Brunette, K. E., & Tran, P. V. (2015) · Development and Psychopathology · doi:10.1017/s0954579415000061 · Cited by 177 · see citing works
Epigenetics and the Biological Basis of Gene × Environment Interactions
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Self-citationChocyk, A., Bobula, B., Dudys, D., Przyborowska, A., Majcher-Maślanka, I., Hess, G., & Wędzony, K. (2013) · European Journal of Neuroscience · doi:10.1111/ejn.12208 · Cited by 153 · see citing works
Silvers, J. A., Lumian, D. S., Gabard-Durnam, L., Gee, D. G., Goff, B., Fareri, D. S., Caldera, C., Flannery, J., Telzer, E. H., Humphreys, K. L., et al. (2016) · The Journal of Neuroscience · doi:10.1523/jneurosci.0038-16.2016 · Cited by 140 · see citing works
Liu, D., Tang, H., Li, X.-Y., Deng, M.-F., Wei, N., Wang, X., Zhou, Y.-F., Wang, D.-Q., Fu, P., Wang, J.-Z., et al. (2017) · Molecular Therapy · doi:10.1016/j.ymthe.2017.01.018 · Cited by 127 · see citing works
Environmental programming of susceptibility and resilience to stress in adulthood in male mice
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Self-citationOpendak, M., Gould, E., & Sullivan, R. (2017) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2017.02.002 · Cited by 94 · see citing works
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- Authors
- Bagot, R. C., van Hasselt, F. N., Champagne, D. L., Meaney, M. J., Krugers, H. J., & Joëls, M.
- Affiliations
- Douglas Mental Health University Institute (CA)
- Leiden University Medical Center (NL)
- University of Amsterdam (NL)
- Corresponding author
- Bagot, Rosemary C.
- Venue
- Neurobiology of Learning and Memory
- Publisher
- Elsevier BV
- Published
- 2009-10
- Volume
- 92
- Issue
- 3
- Pages
- 292-300
- ISSN
- 1074-7427 (ISSN-L)
- OpenAlex
- W2165533945
- Cited by
- 216
- References
- 66
- Citations by year
- 2026: 5 · 2025: 3 · 2024: 6 · 2023: 10 · 2022: 7 · 2021: 5 · 2020: 12 · 2019: 10 · 2018: 10 · 2017: 14 · 2016: 13 · 2015: 25 · 2014: 17 · 2013: 18 · 2012: 19
- FWCI
- 7.75
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Neurobiology of Learning and Memory (publishedVersion)
- PubMed (publishedVersion)
- UvA-DARE (University of Amsterdam) (publishedVersion)
- Data Archiving and Networked Services (DANS) (submittedVersion)
- Topics
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- maternal care, dentate gyrus, synaptic plasticity, long-term potentiation, glucocorticoids, corticosterone, beta-adrenergic stimulation, isoproterenol, dendritic morphology, fear conditioning, contextual fear, cued fear, stress response, Long-Evans rats
- MeSH terms
- Adrenergic beta-Agonists, Animals, Conditioning, Classical, Corticosterone, Cues, Dendrites, Fear, Glucocorticoids, Isoproterenol, Learning, Male, Maternal Behavior, Neurons, Stress, Psychological, Synapses, Time Factors, Long-Term Potentiation, Dentate Gyrus, Rats, Long-Evans, 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 ›
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