Enriched environment experience overcomes the memory deficits and depressive-like behavior induced by early life stress.
Abstract
Stress in early life is believed to cause cognitive and affective disorders, and to disrupt hippocampal synaptic plasticity in adolescence into adult, but it is unclear whether exposure to enriched environment (EE) can overcome these effects. Here, we reported that housing rats in cages with limited nesting/bedding materials on postnatal days 2-21 reduced body weight gain, and this type of early life stress impaired spatial learning and memory of the Morris water maze and increased depressive-like behavior of the forced swim test in young adult rats (postnatal days 53-57). Early life stress also impaired long-term potentiation in hippocampal CA1 area of slices of young adult rats. Remarkably, EE experience on postnatal days 22-52 had no effect on spatial learning/memory and depressive-like behavior, but it significantly facilitated LTP in control rats, and completely overcame the effects of early life stress on young adult rats. These findings suggest that EE experience may be useful for clinical intervention in preventing cognitive and affective disorders during development.
Integrity signals
Registry
Cites
Statistics
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?
Environmental enrichment has been shown to successfully reverse several ELS-induced impairments in behavior, including learning and memory, anxiety, depressive-like behavior, and attention.
“Environmental enrichment has been shown to successfully reverse several ELS-induced impairments in behavior, including learning and memory, anxiety, depressive-like behavior, and attention (Francis et al., 2002; Cui et al., 2006; Vivinetto et al., 2013; Zubedat et al., 2015; Koe et al., 2016).”
From Effects of Maternal Deprivation and Complex Housing on Rat Social Behavior in Adolescence and Adulthood (2018) · cites this paper as Cui et al., 2006
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
Developments of a water-maze procedure for studying spatial learning in the rat
Morris, R. (1984) · Journal of Neuroscience Methods · doi:10.1016/0165-0270(84)90007-4 · Cited by 7,180 · see citing works
Depression: a new animal model sensitive to antidepressant treatments
PORSOLT, R. D., LE PICHON, M., & JALFRE, M. (1977) · Nature · doi:10.1038/266730a0 · Cited by 4,451 · see citing works
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 · see citing works
STRESS 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
The stressed hippocampus, synaptic plasticity and lost memories
Kim, J. J., & Diamond, D. M. (2002) · Nature Reviews Neuroscience · doi:10.1038/nrn849 · Cited by 1,543 · see citing works
Why stress is bad for your brain
Sapolsky, R. M. (1996) · Science · doi:10.1126/science.273.5276.749 · Cited by 1,306 · 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
SÁNCHEZ, M. M., LADD, C. O., & PLOTSKY, P. M. (2001) · Development and Psychopathology · doi:10.1017/s0954579401003029 · Cited by 1,003 · see citing works
Effects of environmental enrichment on gene expression in the brain
Rampon, C., Jiang, C. H., Dong, H., Tang, Y., Lockhart, D. J., Schultz, P. G., Tsien, J. Z., & Hu, Y. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.23.12880 · Cited by 614 · see citing works
Heim, C., Plotsky, P. M., & Nemeroff, C. B. (2004) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300397 · Cited by 514 · see citing works
Behavioural stress facilitates the induction of long-term depression in the hippocampus
Xu, L., Anwyl, R., & Rowan, M. J. (1997) · Nature · doi:10.1038/387497a0 · Cited by 509 · see citing works
Self-citationLeggio, M. G., Mandolesi, L., Federico, F., Spirito, F., Ricci, B., Gelfo, F., & Petrosini, L. (2005) · Behavioural Brain Research · doi:10.1016/j.bbr.2005.04.009 · Cited by 502 · see citing works
Neonatal maternal separation reduces hippocampal mossy fiber density in adult Long Evans rats
Huot, R. L., Plotsky, P. M., Lenox, R. H., & McNamara, R. K. (2002) · Brain Research · doi:10.1016/s0006-8993(02)02985-2 · Cited by 383 · see citing works
Duffy, S. N., Craddock, K. J., Abel, T. G., & Nguyen, P. (2001) · Learning & Memory · doi:10.1101/lm.36301 · Cited by 342 · see citing works
Effects of chronic stress on hippocampal long‐term potentiation
Pavlides, C., Nivón, L. G., & McEwen, B. S. (2002) · Hippocampus · doi:10.1002/hipo.1116 · Cited by 316 · see citing works
Pham, T. M., Ickes, B. R., Albeck, D. S., Söderström, S., Granholm, A.-C., & Mohammed, A. H. (1999) · Neuroscience · doi:10.1016/s0306-4522(99)00316-4 · Cited by 262 · see citing works
Artola, A., von Frijtag, J. C., Fermont, P. C. J., Gispen, W. H., Schrama, L. H., Kamal, A., & Spruijt, B. M. (2006) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2005.04552.x · Cited by 253 · see citing works
Guilarte, T. R., Toscano, C. D., McGlothan, J. L., & Weaver, S. (2002) · Annals of Neurology · doi:10.1002/ana.10399 · Cited by 207 · see citing works
Dysregulation of Cellular Calcium Homeostasis in Alzheimer's Disease: Bad Genes and Bad Habits
Mattson, M. P., & Chan, S. L. (2001) · Journal of Molecular Neuroscience · doi:10.1385/jmn:17:2:205 · Cited by 178 · see citing works
Shakesby, A. C., Anwyl, R., & Rowan, M. J. (2002) · The Journal of Neuroscience · doi:10.1523/jneurosci.22-09-03638.2002 · Cited by 173 · see citing works
Avishai‐Eliner, S., Gilles, E. E., Eghbal‐Ahmadi, M., Bar‐El, Y., & Baram, T. Z. (2001) · Journal of Neuroendocrinology · doi:10.1046/j.1365-2826.2001.00698.x · Cited by 139 · see citing works
Stress and the Developing Hippocampus: A Double-Edged Sword?
Brunson, K. L., Chen, Y., Avishai‐Eliner, S., & Baram, T. Z. (2003) · Molecular Neurobiology · doi:10.1385/mn:27:2:121 · Cited by 86 · see citing works
Aleisa, A. M., Alzoubi, K. H., Gerges, N. Z., & Alkadhi, K. A. (2005) · The International Journal of Neuropsychopharmacology · doi:10.1017/s1461145705005912 · Cited by 86 · see citing works
Diamond, D. M., Campbell, A., Park, C. R., & Vouimba, R.-M. (2004) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2004.09.003 · Cited by 71 · see citing works
Yang, Y., Cao, J., Xiong, W., Zhang, J., Zhou, Q., Wei, H., Liang, C., Deng, J., Li, T., Yang, S., et al. (2003) · Journal of Endocrinology · doi:10.1677/joe.0.1780045 · Cited by 61 · see citing works
Self-citationRapid induction of intraneuronal neurofibrillary tangles in apolipoprotein E-deficient mice
Bi, X., Yong, A. P., Zhou, J., Ribak, C. E., & LYNCH, G. S. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.151253098 · Cited by 43 · see citing works
Propofol effects on excitatory synaptic efficacy in the CA1 region of the developing hippocampus
Sun, X., Zhang, J., Li, H., Zhang, Z., Yang, J., Cui, M., Zeng, B., Xu, T., Cao, J., & Xu, L. (2005) · Developmental Brain Research · doi:10.1016/j.devbrainres.2005.02.011 · Cited by 18 · see citing works
Self-citationAcute behavioural stress facilitates long-term depression in temporoammonic-CA1 pathway
Yang, J., Han, H., Cui, M., Wang, L., Cao, J., Li, L., & Xu, L. (2006) · Neuroreport · doi:10.1097/01.wnr.0000209044.66482.c5 · Cited by 10 · see citing works
Self-citation
Flagged first, then by citations
1 of the 30 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Modulation of the Hypothalamic-Pituitary-Adrenal Axis by Early Life Stress Exposure
van Bodegom, M., Homberg, J. R., & Henckens, M. J. A. G. (2017) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2017.00087 · Cited by 562 · see citing works
The impact of environmental enrichment in laboratory rats—Behavioural and neurochemical aspects
Simpson, J., & Kelly, J. P. (2011) · Behavioural Brain Research · doi:10.1016/j.bbr.2011.04.002 · Cited by 480 · see citing works
Toward understanding how early-life stress reprograms cognitive and emotional brain networks
Chen, Y., & Baram, T. Z. (2016) · Neuropsychopharmacology · doi:10.1038/npp.2015.181 · Cited by 474 · see citing works
Factors influencing behavior in the forced swim test
Bogdanova, O. V., Kanekar, S., D’Anci, K. E., & Renshaw, P. F. (2013) · Physiology & Behavior · doi:10.1016/j.physbeh.2013.05.012 · Cited by 465 · see citing works
Sensitive periods of substance abuse: Early risk for the transition to dependence
Jordan, C. J., & Andersen, S. L. (2017) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2016.10.004 · Cited by 455 · see citing works
“…pre-pubertal or adolescent periods (in the form of toys, elaborate habitats, and social housing) reverses the effects of pre-natal and post-natal early life stress on HPA axis function, spatial memory, social play and fear responses (Cui et al., 2006; Francis et al., 2002; Laviola et al., 2004).”
Joëls, M., Sarabdjitsingh, R. A., & Karst, H. (2012) · Pharmacological Reviews · doi:10.1124/pr.112.005892 · Cited by 425 · see citing works
Early-life stress has persistent effects on amygdala function and development in mice and humans
Malter Cohen, M., Jing, D., Yang, R. R., Tottenham, N., Lee, F. S., & Casey, B. J. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1310163110 · Cited by 307 · see citing works
Sculpting the hippocampus from within: stress, spines, and CRH
Maras, P. M., & Baram, T. Z. (2012) · Trends in Neurosciences · doi:10.1016/j.tins.2012.01.005 · Cited by 174 · see citing works
Chocyk, 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
Veena, J., Srikumar, B. N., Raju, T. R., & Rao, B. S. S. (2009) · Neuroscience Letters · doi:10.1016/j.neulet.2009.03.059 · Cited by 153 · see citing works
Veena, J., Srikumar, B. N., Mahati, K., Bhagya, V. R., Raju, T. R., & Rao, B. S. S. (2008) · Journal of Neuroscience Research · doi:10.1002/jnr.21907 · Cited by 152 · see citing works
Farès, R., Belmeguenaï, A., Sanchez, P. E., Kouchi, H., Bodennec, J., Morales, A., Georges, B., Bonnet, C., Bouvard, S., Sloviter, R. S., et al. (2013) · PLoS ONE · doi:10.1371/journal.pone.0053888 · Cited by 147 · see citing works
Dandi, Ε., Kalamari, A., Touloumi, O., Lagoudaki, R., Nousiopoulou, E., Simeonidou, C., Spandou, E., & Tata, D. Α. (2018) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2018.03.003 · Cited by 146 · see citing works
Yang, J., Hou, C., Ma, N., Liu, J., Zhang, Y., Zhou, J., Xu, L., & Li, L. (2007) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2006.09.001 · Cited by 127 · see citing works
Self-citationEarly life stress in rodents: Animal models of illness or resilience?
Murthy, S., & Gould, E. (2018) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2018.00157 · Cited by 120 · see citing works
Enriched environment prevents chronic stress-induced spatial learning and memory deficits
Wright, R. L., & Conrad, C. D. (2007) · Behavioural Brain Research · doi:10.1016/j.bbr.2007.08.025 · Cited by 113 · see citing works
Koe, A. S., Ashokan, A., & Mitra, R. (2016) · Translational Psychiatry · doi:10.1038/tp.2015.217 · Cited by 109 · see citing works
Bhagya, V. R., Srikumar, B. N., Veena, J., & Rao, B. S. S. (2016) · Journal of Neuroscience Research · doi:10.1002/jnr.23992 · Cited by 110 · see citing works
Neurobiological effects of neonatal maternal separation and post-weaning environmental enrichment.
Vivinetto, A. L., Suárez, M. M., & Rivarola, M. A. (2013) · Behavioural Brain Research · doi:10.1016/j.bbr.2012.11.014 · Cited by 103 · see citing works
Early life stress in epilepsy: A seizure precipitant and risk factor for epileptogenesis
van Campen, J. S., Jansen, F. E., Graan, P. N. E. D., Braun, K. P. J., & Joëls, M. (2013) · Epilepsy & Behavior · doi:10.1016/j.yebeh.2013.09.029 · Cited by 101 · see citing works
Microglial Function in the Effects of Early-Life Stress on Brain and Behavioral Development
Catale, C., Gironda, S. C., Iacono, L. L., & Carola, V. (2020) · Journal of Clinical Medicine · doi:10.3390/jcm9020468 · Cited by 99 · see citing works
Sensorimotor modulation of mood and depression: An integrative review
Canbeyli, R. S. (2009) · Behavioural Brain Research · doi:10.1016/j.bbr.2009.11.002 · Cited by 98 · see citing works
Konkle, A. T. M., Kentner, A. C., Baker, S. L., Stewart, A., & Bielajew, C. H. (2010) · PubMed Central · Cited by 94 · see citing works
Hui, J., Zhang, Z., Liu, S., Xi, G., Zhang, X.-R., Teng, G., Chan, K. C., Wu, E. X., Nie, B., Shan, B., et al. (2010) · Behavioural Brain Research · doi:10.1016/j.bbr.2010.10.014 · Cited by 91 · see citing works
Hutchinson, K. M., McLaughlin, K. J., Wright, R. L., Ortiz, J. B., Anouti, D. P., Mika, A., Diamond, D. M., & Conrad, C. D. (2012) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2012.01.003 · Cited by 91 · see citing works
Why and how the early-life environment affects development of coping behaviours
Langenhof, M. R., & Komdeur, J. (2018) · Behavioral Ecology and Sociobiology · doi:10.1007/s00265-018-2452-3 · Cited by 90 · see citing works
Mahati, K., Bhagya, V. R., Christofer, T., Sneha, A., & Rao, B. S. S. (2016) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2016.08.017 · Cited by 74 · see citing works
White, J. D., & Kaffman, A. (2019) · Frontiers in Neuroscience · doi:10.3389/fnins.2019.01082 · Cited by 73 · see citing works
Stevens, J. S., van Rooij, S. J. H., & Jovanović, T. (2016) · Current topics in behavioral neurosciences · doi:10.1007/7854_2016_38 · Cited by 73 · see citing works
Eckert, M. J., & Abraham, W. C. (2012) · Current topics in behavioral neurosciences · doi:10.1007/7854_2012_215 · Cited by 73 · see citing works
Early life stress as an influence on limbic epilepsy: a hypothesis whose time has come?
Koe, A. S. (2009) · Frontiers in Behavioral Neuroscience · doi:10.3389/neuro.08.024.2009 · Cited by 71 · see citing works
Prolonged maternal separation disturbs the serotonergic system during early brain development
Ohta, K., Miki, T., Warita, K., Suzuki, S., Kusaka, T., Yakura, T., Liu, J., Tamai, M., & Takeuchi, Y. (2014) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2013.10.007 · Cited by 68 · see citing works
McOmish, C. E., & Hannan, A. J. (2007) · Expert Opinion on Therapeutic Targets · doi:10.1517/14728222.11.7.899 · Cited by 65 · see citing works
Chocyk, A., Przyborowska, A., Makuch, W., Majcher‐Maślanka, I., Dudys, D., & Wędzony, K. (2014) · Behavioural Brain Research · doi:10.1016/j.bbr.2014.01.040 · Cited by 63 · see citing works
Framework for sex differences in adolescent neurobiology: A focus on cannabinoids
Viveros, M., Marco, E. M., López‐Gallardo, M., García‐Segura, L. M., & Wagner, E. J. (2010) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2010.09.005 · Cited by 58 · see citing works
Rocha, M., Wang, D., Avila-Quintero, V. J., Bloch, M. H., & Kaffman, A. (2021) · Translational Psychiatry · doi:10.1038/s41398-021-01352-4 · Cited by 56 · see citing works
Ravenelle, R., Santolucito, H. B., Byrnes, E. M., BYRNES, J. J., & Donaldson, S. T. (2014) · Neuroscience · doi:10.1016/j.neuroscience.2014.03.060 · Cited by 56 · see citing works
Maniam, J., Antoniadis, C. P., Le, V., & Morris, M. J. (2016) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2016.03.007 · Cited by 56 · see citing works
Macartney, E. L., Lagisz, M., & Nakagawa, S. (2022) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2022.104554 · Cited by 58 · see citing works
Heun‐Johnson, H., & Levitt, P. R. (2016) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2016.00142 · Cited by 55 · see citing works
Herpfer, I., Hezel, H., Reichardt, W., Clark, K., Geiger, J., Gross, C. M., Heyer, A., Neagu, V., Bhatia, H. S., Atas, H. C., et al. (2012) · PLoS ONE · doi:10.1371/journal.pone.0046004 · Cited by 51 · see citing works
Chen, Y., Mao, Y., Zhou, D., Hu, X., Wang, J., & Ma, Y. (2010) · Behavioural Brain Research · doi:10.1016/j.bbr.2010.03.033 · Cited by 49 · see citing works
Fuentes, S., Daviu, N., Gagliano, H., Garrido, P., Zelena, D., Monasterio, N., Armario, A., & Nadal, R. A. (2014) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2014.00056 · Cited by 44 · see citing works
Peay, D. N., Saribekyan, H. M., Parada, P. A., Hanson, E. M., Badaruddin, B. S., Judd, J. M., Donnay, M. E., Padilla-Garcia, D., & Conrad, C. D. (2020) · Behavioural Brain Research · doi:10.1016/j.bbr.2020.112519 · Cited by 44 · see citing works
Griva, M., Lagoudaki, R., Touloumi, O., Nousiopoulou, E., Karalis, F., Georgiou, T., Kokaraki, G., Simeonidou, C., Tata, D. Α., & Spandou, E. (2017) · Brain Research · doi:10.1016/j.brainres.2017.05.004 · Cited by 43 · see citing works
Cao, X., Huang, S., & Ruan, D. (2008) · Developmental Psychobiology · doi:10.1002/dev.20287 · Cited by 43 · see citing works
Sensorimotor Modulation of Mood and Depression: In Search of an Optimal Mode of Stimulation
Canbeyli, R. (2013) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2013.00428 · Cited by 42 · see citing works
Adverse effects of early-life stress: focus on the rodent neuroendocrine system
Lee, S. H., & Jung, E. (2023) · Neural Regeneration Research · doi:10.4103/1673-5374.377587 · Cited by 43 · see citing works
Kentrop, J., Smid, C. R., Achterberg, E. J. M., van IJzendoorn, M. H., Bakermans-Kranenburg, M. J., Joëls, M., & van der Veen, R. (2018) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2018.00193 · Cited by 41 · see citing works
“Environmental enrichment has been shown to successfully reverse several ELS-induced impairments in behavior, including learning and memory, anxiety, depressive-like behavior, and attention (Francis et al., 2002; Cui et al., 2006; Vivinetto et al., 2013; Zubedat et al., 2015; Koe et al., 2016).”
Anderson, L. S., & Heyne, L. A. (2012) · Therapeutic Recreation Journal · Cited by 41 · see citing works
Zeeni, N., Bassil, M. S., Fromentin, G., Chaumontet, C., Darcel, N., Tomé, D., & Daher, C. F. (2014) · Physiology & Behavior · doi:10.1016/j.physbeh.2014.11.003 · Cited by 41 · see citing works
Henderson, Y. O., Victoria, N. C., Inoue, K., Murphy, A. Z., & Parent, M. B. (2014) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2014.10.010 · Cited by 40 · see citing works
Sparling, J. E., Barbeau, K., Boileau, K., & Konkle, A. T. M. (2020) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2020.172997 · Cited by 40 · see citing works
Río-Álamos, C., Piludu, M. A., Gerbolés, C., Barroso, D., Oliveras, I., Sánchez-González, A., Cañete, T., Tapias-Espinosa, C., Sampedro-Viana, D., Torrúbia, R., et al. (2018) · Behavioural Brain Research · doi:10.1016/j.bbr.2018.12.033 · Cited by 38 · see citing works
Perry, R. E., Rincón‐Cortés, M., Braren, S. H., Brandes-Aitken, A. N., Opendak, M. M., Pollonini, G., Chopra, D., Raver, C. C., Alberini, C. M., Blair, C., et al. (2019) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2019.100716 · Cited by 40 · see citing works
Perry, R. E., Braren, S. H., Rincón‐Cortés, M., Brandes-Aitken, A. N., Chopra, D., Opendak, M. M., Alberini, C. M., Sullivan, R. M., & Blair, C. (2019) · Frontiers in Psychology · doi:10.3389/fpsyg.2019.02472 · Cited by 38 · see citing works
The impact of environmental and social factors on learning abilities: a meta‐analysis
Lambert, C. T., & Guillette, L. M. (2021) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1111/brv.12783 · Cited by 39 · see citing works
Xu, Z., Zhang, Y., Hou, B., Gao, Y., Wu, Y., & Zhang, C. (2010) · Journal of Affective Disorders · doi:10.1016/j.jad.2010.11.005 · Cited by 31 · see citing works
Long-Term Impact of Early-Life Stress on Hippocampal Plasticity: Spotlight on Astrocytes
Çalışkan, G., Müller, A., & Albrecht, A. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21144999 · Cited by 32 · see citing works
Arndt, D. L., Peterson, C. J., & Cain, M. E. (2015) · PLoS ONE · doi:10.1371/journal.pone.0131709 · Cited by 34 · see citing works
Avital, A., Dolev, T., Aga‐Mizrachi, S., & Zubedat, S. (2011) · PLoS ONE · doi:10.1371/journal.pone.0022059 · Cited by 33 · see citing works
Hoffman, A. N., Armstrong, C. E., Hanna, J. J., & Conrad, C. (2010) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2010.08.010 · Cited by 34 · see citing works
Sahafi, E., Peeri, M., Hosseini, M.-J., & Azarbyjani, M. A. (2018) · Physiology & Behavior · doi:10.1016/j.physbeh.2017.10.022 · Cited by 32 · see citing works
Simpson, J., & Kelly, J. P. (2012) · Behavioural Brain Research · doi:10.1016/j.bbr.2012.06.015 · Cited by 32 · see citing works
Reconsidering depression as a risk factor for substance use disorder: Insights from rodent models
Rappeneau, V., & Bérod, A. (2017) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2017.04.001 · Cited by 32 · see citing works
Sakhaie, N., Sadegzadeh, F., Mohammadnia, A., Dadkhah, M., & Saadati, H. (2020) · International Journal of Developmental Neuroscience · doi:10.1002/jdn.10038 · Cited by 31 · see citing works
Possamai, F., dos Santos, J., Walber, T., Marcon, J. C., dos Santos, T. S., & de Oliveira, C. L. (2014) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2014.10.017 · Cited by 31 · see citing works
Mohammadian, J., Najafi, M., & Miladi‐Gorji, H. (2018) · Developmental Psychobiology · doi:10.1002/dev.21808 · Cited by 30 · see citing works
Sifonios, L. L., Trinchero, M. F., Cereseto, M., Ferrero, A., Cladouchos, M. L., Macedo, G. F., Reinés, A. G., & Wikinski, S. (2009) · Neuroscience · doi:10.1016/j.neuroscience.2009.08.059 · Cited by 28 · see citing works
Environment and early life: Decisive factors for stress-resilience and vulnerability
Hegde, A., & Mitra, R. (2020) · International review of neurobiology · doi:10.1016/bs.irn.2019.12.002 · Cited by 28 · see citing works
Electrophysiological insights into the enduring effects of early life stress on the brain
Ali, I. Y., Salzberg, M. R., French, C. R., & Jones, N. C. (2010) · Psychopharmacology · doi:10.1007/s00213-010-2125-z · Cited by 25 · see citing works
Rule, L., Yang, J. M. K., Watkin, H., Hall, J., & Brydges, N. M. (2020) · Molecular Psychiatry · doi:10.1038/s41380-020-0718-4 · Cited by 25 · see citing works
Self-citationZhang, J., Abdallah, C. G., Chen, Y., Huang, T., Huang, Q., Chong-tao, X., Xiao, Y., Liu, Y., Ding, Y., & Wu, R. (2013) · Neuroscience Letters · doi:10.1016/j.neulet.2013.04.035 · Cited by 24 · see citing works
Self-citationSarapultsev, A., Komelkova, M. V., Lookin, O. N., Khatsko, S. L., Gusev, E., Трофимов, А. Н., Tokay, T., & Hu, D. (2024) · Pathophysiology · doi:10.3390/pathophysiology31040051 · Cited by 23 · see citing works
Grace, J. K., Martin-Gousset, L., & Angelier, F. (2017) · Physiology & Behavior · doi:10.1016/j.physbeh.2017.04.018 · Cited by 22 · see citing works
Joushi, S., Esmaeilpour, K., Masoumi‐Ardakani, Y., Esmaeili‐Mahani, S., & Sheibani, V. (2021) · Journal of Neuroscience Research · doi:10.1002/jnr.24974 · Cited by 23 · see citing works
Learning of a T-maze by rat pups when contact with the mother is either permitted or denied
Panagiotaropoulos, T. I., Diamantopoulou, A., Stamatakis, A., Dimitropoulou, M., & Stylianopoulou, F. (2008) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2008.09.007 · Cited by 23 · see citing works
Influence of housing variables on the development of stress-sensitive behaviors in the rat
Sakhai, S. A., Preslik, J. M., & Francis, D. D. (2013) · Physiology & Behavior · doi:10.1016/j.physbeh.2013.08.003 · Cited by 23 · see citing works
Hui, J., Zhang, Z., Liu, S., Xi, G., Zhang, X., Teng, G., Chan, K. C., Wu, E. X., Nie, B., Shan, B., et al. (2010) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2010.08.010 · Cited by 23 · see citing works
Bhaskar, R., Mishra, A. K., & Mohanty, B. (2017) · Basic & Clinical Pharmacology & Toxicology · doi:10.1111/bcpt.12767 · Cited by 23 · see citing works
Housing environment influences stress-related hippocampal substrates and depression-like behavior
Ashokan, A., Hegde, A., Balasingham, A., & Mitra, R. (2018) · Brain Research · doi:10.1016/j.brainres.2018.01.021 · Cited by 23 · see citing works
Ramírez-Rodríguez, G. B., Gutiérrez-Vera, B., Ortíz‐López, L., Vega‐Rivera, N. M., Juan, D. M.-S., Granados-Juárez, A., Aquino, D. V. C.-D., Castro-García, M., & Ramos, M. F. (2022) · Physiology & Behavior · doi:10.1016/j.physbeh.2022.113878 · Cited by 22 · see citing works
Singhal, G., Morgan, J., Jawahar, M. C., Corrigan, F., Jaehne, E. J., Toben, C. G., Breen, J., Pederson, S., Hannan, A. J., & Baune, B. T. (2019) · Cognitive Affective & Behavioral Neuroscience · doi:10.3758/s13415-019-00743-x · Cited by 20 · see citing works
Olesen, M. V., Wörtwein, G., & Pakkenberg, B. (2014) · Hippocampus · doi:10.1002/hipo.22351 · Cited by 21 · see citing works
Effects of Environmental Enrichment in Maternally Separated Rats: Age and Sex-Specific Outcomes
Doreste-Méndez, R., Ríos-Ruiz, E. J., Rivera-López, L. L., Gutierrez, A., & Torres-Reverón, A. (2019) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2019.00198 · Cited by 21 · see citing works
Effects of Early Life Adversities upon Memory Processes and Cognition in Rodent Models
Alves, J., Pereira, N. D. S. C., de Lima, R. M. S., Quillfeldt, J. A., & Dalmaz, C. (2022) · Neuroscience · doi:10.1016/j.neuroscience.2022.04.023 · Cited by 23 · see citing works
Novelty-induced enhancement in spatial memory: Is infancy a critical period?
Yang, Z., & Tang, A. C. (2010) · Behavioural Brain Research · doi:10.1016/j.bbr.2010.12.020 · Cited by 20 · see citing works
The differential effects of brief environmental enrichment following social isolation in rats
Guven, E. B., Pranic, N. M., & Ünal, G. (2022) · Cognitive Affective & Behavioral Neuroscience · doi:10.3758/s13415-022-00989-y · Cited by 19 · see citing works
Effects of early life stress on rodent hippocampal synaptic plasticity: a systematic review
Derks, N. A. V., Krugers, H. J., Hoogenraad, C. C., Joëls, M., & Sarabdjitsingh, R. A. (2017) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2017.03.005 · Cited by 18 · see citing works
Joushi, S., Taherizadeh, Z., Esmaeilpour, K., & Sheibani, V. (2021) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2021.173318 · Cited by 18 · see citing works
Möhrle, D., Yuen, M., Zheng, A., Haddad, F. L., Allman, B. L., & Schmid, S. (2023) · Genes Brain & Behavior · doi:10.1111/gbb.12841 · Cited by 18 · see citing works
Pati, S., Saba, K., Salvi, S. S., Tiwari, P., Chaudhari, P. R., Verma, V., Mukhopadhyay, S., Kapri, D., Suryavanshi, S., Clement, J. P., et al. (2020) · eLife · doi:10.7554/elife.56171 · Cited by 17 · see citing works
Kentrop, J., van der Tas, L., Loi, M., van IJzendoorn, M. H., Bakermans-Kranenburg, M. J., Joëls, M., & van der Veen, R. (2016) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2016.00122 · Cited by 16 · see citing works
Does Stress Trigger Seizures? Evidence from Experimental Models
Reddy, D. S., Thompson, W. J., & Calderara, G. (2020) · Current topics in behavioral neurosciences · doi:10.1007/7854_2020_191 · Cited by 17 · see citing works
Tip60 HAT Action Mediates Environmental Enrichment Induced Cognitive Restoration
Xu, S., Panikker, P., Iqbal, S., & Elefant, F. (2016) · PLoS ONE · doi:10.1371/journal.pone.0159623 · Cited by 16 · see citing works
Touchant, M., & Labonté, B. (2022) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2022.845491 · Cited by 14 · see citing works
Zühlsdorff, K., López‐Cruz, L., Dutcher, E. G., Jones, J. A., Pama, C., Sawiak, S. J., Khan, S. A., Milton, A. L., Robbins, T. W., Bullmore, E. T., et al. (2022) · Neurobiology of Stress · doi:10.1016/j.ynstr.2022.100507 · Cited by 15 · see citing works
Hajheidari, S., Miladi‐Gorji, H., & Bigdeli, I. (2017) · PubMed Central · Cited by 14 · see citing works
Fontana, B. D., Cleal, M., Norton, W., & Parker, M. O. (2021) · Physiology & Behavior · doi:10.1016/j.physbeh.2021.113526 · Cited by 13 · see citing works
Early Enriched Environment Prevents Epigenetic p11 Gene Changes Induced by Adulthood Stress in Mice
Seo, M. K., Choi, A., Seog, D., Lee, J. G., & Park, S. W. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22041928 · Cited by 14 · see citing works
- Authors
- Cui, M., Yang, Y., Yang, J., Zhang, J., Han, H., Ma, W., Li, H., Mao, R., Xu, L., Hao, W., & Cao, J.
- Affiliations
- Central South University (CN)
- Kunming Institute of Zoology (CN)
- Corresponding author
- Hao, Wei
- Cao, Jun
- Venue
- Neuroscience Letters
- Publisher
- Elsevier BV
- Published
- 2006-08
- Volume
- 404
- Issue
- 1-2
- Pages
- 208-212
- ISSN
- 0304-3940 (ISSN-L)
- OpenAlex
- W2045905702
- Cited by
- 153
- References
- 30
- Citations by year
- 2026: 4 · 2025: 4 · 2024: 6 · 2023: 6 · 2022: 10 · 2021: 9 · 2020: 12 · 2019: 6 · 2018: 12 · 2017: 11 · 2016: 10 · 2015: 3 · 2014: 13 · 2013: 10 · 2012: 9
- FWCI
- 2.10
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Neuroscience Letters (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Keywords
- environmental enrichment, early life stress, memory impairment, depression-like behavior, spatial learning and memory, long-term potentiation, hippocampal CA1, hippocampal synaptic plasticity, nesting material, developmental intervention
- MeSH terms
- Aging, Animals, Animals, Newborn, Depression, Disease Models, Animal, Electrophysiology, Environment, Hippocampus, Housing, Animal, Learning, Male, Memory, Memory Disorders, Stress, Psychological, Long-Term Potentiation, Maze Learning, 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
