The DOI matches its Crossref record; 39 of the 39 references it cites were found in a registry or an index.
Environmental Enrichment Reverses the Effects of Maternal Separation on Stress Reactivity
Open accessAbstract
Postnatal maternal separation increases hypothalamic corticotropin-releasing factor (CRF) gene expression and hypothalamic-pituitary-adrenal (HPA) and behavioral responses to stress. We report here that environmental enrichment during the peripubertal period completely reverses the effects of maternal separation on both HPA and behavioral responses to stress, with no effect on CRF mRNA expression. We conclude that environmental enrichment leads to a functional reversal of the effects of maternal separation through compensation for, rather than reversal of, the neural effects of early life adversity.
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In the citing paper
“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 Francis et al., 2002
Experimental — accuracy not yet measuredIn the citing paper
“Studies in humans and animals models show that environmental enrichment can reduce or reverse some of the effects of deprivation, non-normative stimulation and even acute or chronic stress [122,123] at the behavioural and neural levels [109,[124][125][126].”
In the citing paper
“For example, Francis, Diorio, Plotsky, and Meaney (2002) demonstrated reversal of the effect of early stress associated with maternal separation during the neonatal period on the HPA response to stress, as indicated by corticosterone levels, and on learning and memory among rats receiving environmental enrichment.”
From Stress and the development of self-regulation in context (2010) · cites this paper as Francis, Diorio, Plotsky, and Meaney, 2002
In the citing paper
“Effects on corticosterone and behavior, however, could not be attributed to expected changes at the neural level in terms of primary processes that influence stress reactivity.”
From Stress and the development of self-regulation in context (2010) · cites this paper as Francis et al., 2002
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Citations
Cites
The rat brain in stereotaxic coordinates
Palkovits, M. (1983) · Neuropeptides · doi:10.1016/0143-4179(83)90049-5 · Cited by 28,959
The Rat Brain in Stereotaxic Coordinates
Paxinos, G., & Watson, C. (1983) · Elsevier eBooks · doi:10.1016/c2009-0-63235-9 · Cited by 28,585
AChE-stained horizontal sections of the rat brain in stereotaxic coordinates
Paxinos, G., WATSON, C. R. R., & Emson, P. C. (1980) · Journal of Neuroscience Methods · doi:10.1016/0165-0270(80)90021-7 · Cited by 4,501
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
Self-citationMeaney, M. J. (2001) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.24.1.1161 · Cited by 2,708
Self-citationBrain 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
Nongenomic Transmission Across Generations of Maternal Behavior and Stress Responses in the Rat
Francis, D., Diorio, J., Liu, D., & Meaney, M. J. (1999) · Science · doi:10.1126/science.286.5442.1155 · Cited by 1,965
Self-citationJACOBSON, L., & SAPOLSKY, R. (1991) · Endocrine Reviews · doi:10.1210/edrv-12-2-118 · Cited by 1,739
Plotsky, P. M., & Meaney, M. J. (1993) · Molecular Brain Research · doi:10.1016/0169-328x(93)90189-v · Cited by 1,638
Self-citationDiorio, D., Viau, V, & Meaney, M. (1993) · The Journal of Neuroscience · doi:10.1523/jneurosci.13-09-03839.1993 · Cited by 1,151
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Physiology and neurobiology of stress and adaptation: central role of the brain
McEwen, B. S. (2007) · Physiological Reviews · doi:10.1152/physrev.00041.2006 · Cited by 5,429
Cognitive and affective development in adolescence
Steinberg, L. (2005) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2004.12.005 · Cited by 2,978
The neurobiology of stress and development.
Gunnar, M., & Quevedo, K. (2007) · Annual Review of Psychology · doi:10.1146/annurev.psych.58.110405.085605 · Cited by 2,011
Sensitive periods in the development of the brain and behavior
Knudsen, E. I. (2004) · Journal of Cognitive Neuroscience · doi:10.1162/0898929042304796 · Cited by 1,842
Enriched environments, experience-dependent plasticity and disorders of the nervous system
Nithianantharajah, J., & Hannan, A. J. (2006) · Nature Reviews Neuroscience · doi:10.1038/nrn1970 · Cited by 1,771
Metadata
- Authors
- Francis, D. D., Diorio, J., Plotsky, P. M., & Meaney, M. J.
- Affiliations
- Douglas Mental Health University Institute (CA)
- Emory University (US)
- ORCID
- Meaney, Michael J.
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2002-09-15
- Volume
- 22
- Issue
- 18
- Pages
- 7840-7843
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6758090
- OpenAlex
- W2144859742
- Cited by
- 663
- References
- 39
- Citations by year
- 2026: 9 · 2025: 13 · 2024: 6 · 2023: 10 · 2022: 18 · 2021: 26 · 2020: 32 · 2019: 23 · 2018: 31 · 2017: 34 · 2016: 37 · 2015: 35 · 2014: 31 · 2013: 34 · 2012: 35
- FWCI
- 9.08
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Journal of Neuroscience (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute of Mental Health
- Topics
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Neuroendocrine regulation and behavior
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Keywords
- environmental enrichment, maternal separation, postpartum stress, stress reactivity, corticotropin-releasing factor, hypothalamic-pituitary-adrenal axis, childhood adversity, peripubertal period, behavioral stress response, neural compensation
- MeSH terms
- Animals, Appetitive Behavior, Behavior, Animal, Brain, Brain Chemistry, Corticotropin-Releasing Hormone, Exploratory Behavior, Handling, Psychological, Hypothalamo-Hypophyseal System, Maternal Deprivation, Pituitary-Adrenal System, Receptors, Glucocorticoid, RNA, Messenger, Social Environment, Stress, Physiological, In Situ Hybridization, Rats, Long-Evans, Rats
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