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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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 Francis et al., 2002
The Results section (‘Enrichment reverses effects of MS on HPA function’; page not provided) reports that enrichment reversed maternal-separation effects on fearfulness and novelty-related behavioral inhibition in rats, supporting the anxiety-related part of the claim. It does not report reversal of impairments in learning and memory, depressive-like behavior, or attention. (LLM, conf=0.88)
Experimental — accuracy not yet measuredStudies 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 at the behavioural and neural levels.
“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].”
Francis et al. (2002) demonstrated reversal of early maternal separation stress effects on HPA response (corticosterone) and learning/memory in rats receiving environmental enrichment.
“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 Francis et al. (2002), effects on corticosterone and behavior could not be attributed to expected neural-level changes in primary processes influencing stress reactivity.
“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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Cites
The rat brain in stereotaxic coordinates
Palkovits, M. (1983) · Neuropeptides · doi:10.1016/0143-4179(83)90049-5 · Cited by 28,988 · see citing works
The Rat Brain in Stereotaxic Coordinates
Paxinos, G., & Watson, C. (1983) · Elsevier eBooks · doi:10.1016/c2009-0-63235-9 · Cited by 28,585 · see citing works
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 4,497 · 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-citationMeaney, M. J. (2001) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.24.1.1161 · Cited by 2,708 · see citing works
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 · see citing works
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 · see citing works
Self-citationJACOBSON, L., & SAPOLSKY, R. (1991) · Endocrine Reviews · doi:10.1210/edrv-12-2-118 · Cited by 1,739 · see citing works
Plotsky, P. M., & Meaney, M. J. (1993) · Molecular Brain Research · doi:10.1016/0169-328x(93)90189-v · Cited by 1,638 · see citing works
Self-citationDiorio, D., Viau, V, & Meaney, M. (1993) · The Journal of Neuroscience · doi:10.1523/jneurosci.13-09-03839.1993 · Cited by 1,151 · see citing works
Self-citationDNA methylation in health and disease
Robertson, K. D., & Wolffe, A. P. (2000) · Nature Reviews Genetics · doi:10.1038/35049533 · Cited by 1,056 · 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
Long-term behavioral and neuroendocrine adaptations to adverse early experience
Ladd, C. O., Huot, R. L., Thrivikraman, K. V., Nemeroff, C. B., Meaney, M. J., & Plotsky, P. M. (2000) · Progress in brain research · doi:10.1016/s0079-6123(08)62132-9 · Cited by 717 · see citing works
Self-citationInfantile Experience and Resistance to Physiological Stress
Levine, S. (1957) · Science · doi:10.1126/science.126.3270.405 · Cited by 659 · see citing works
Early intervention and early experience.
Ramey, C. T., & Ramey, S. L. (1998) · American Psychologist · doi:10.1037//0003-066x.53.2.109 · Cited by 636 · see citing works
Caldji, C. (2000) · Neuropsychopharmacology · doi:10.1016/s0893-133x(99)00110-4 · Cited by 606 · 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
(1996) · PubMed · Cited by 547 · 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
Autoregulation of Serotonin Neurons: Role in Antidepressant Drug Action
Piñeyro, G., & Blier, P. (1999) · Pharmacological Reviews · doi:10.1016/s0031-6997(24)01417-0 · Cited by 537 · see citing works
Early determinants of behaviour: evidence from primate studies
Suomi, S. J. (1997) · British Medical Bulletin · doi:10.1093/oxfordjournals.bmb.a011598 · Cited by 483 · see citing works
Meaney, M. J., Aitken, D. H., Viau, V., Sharma, S., & Sarrieau, A. (2008) · Neuroendocrinology · doi:10.1159/000125287 · Cited by 457 · see citing works
Self-citationLiu, Caldji, Sharma, Plotsky, & Meaney (2000) · Journal of Neuroendocrinology · doi:10.1046/j.1365-2826.2000.00422.x · Cited by 451 · see citing works
Stress, Feedback and Facilitation in the Hypothalamo‐Pituitary‐Adrenal Axis
Dallman, M., Akana, S., Scribner, K. A., Bradbury, M. J., Walker, C., Strack, A. M., & Cascio, C. S. (1992) · Journal of neuroendocrinology · doi:10.1111/j.1365-2826.1992.tb00200.x · Cited by 418 · see citing works
Higley, J. D., Hasert, M. F., Suomi, S. J., & Linnoila, M. (1991) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.88.16.7261 · Cited by 368 · see citing works
Blier, P. (1999) · Neuropsychopharmacology · doi:10.1016/s0893-133x(99)00036-6 · Cited by 282 · see citing works
McCormick, J. A., Lyons, V., Jacobson, M. D., Noble, J., Diorio, J. C., Nyirenda, M., Weaver, S., Ester, W. A., Yau, J. L. W., Meaney, M. J., et al. (2000) · Molecular Endocrinology · doi:10.1210/mend.14.4.0438 · Cited by 258 · see citing works
Self-citationA sensitive open field measure of anxiolytic drug activity
Britton, D. R., & Britton, K. T. (1981) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(81)90212-4 · Cited by 250 · see citing works
Meaney, M. J., & Aitken, D. H. (1985) · Developmental Brain Research · doi:10.1016/0165-3806(85)90183-x · Cited by 234 · see citing works
Self-citationFernández‐Teruel, A., Escorihuela, R. M., Castellano, B., González, B., & Tobeña, A. (1997) · Behavior Genetics · doi:10.1023/a:1021400830503 · Cited by 207 · see citing works
Rearing environmental enrichment in two inbred strains of mice: 1. Effects on emotional reactivity
Chapillon, P., Manneché, C., Belzung, C., & Caston, J. (1999) · Behavior Genetics · doi:10.1023/a:1021437905913 · Cited by 202 · see citing works
Rasmuson, S., Olsson, T., Henriksson, B. G., Kelly, P. A. T., Holmes, M. C., Seckl, J. R., & Mohammed, A. H. S. (1998) · Molecular Brain Research · doi:10.1016/s0169-328x(97)00317-3 · Cited by 134 · see citing works
Infantile Experience and Resistance to Physiological Stress
Levine, S. (1957) · Science · doi:10.1126/science.126.3270.405.a · Cited by 123 · see citing works
Valentino, R. J., Curtis, A. L., Page, M. E., Pavcovich, L. A., & Florin-Lechner, S. M. (1997) · Advances in pharmacology · doi:10.1016/s1054-3589(08)60863-7 · Cited by 120 · see citing works
Nest temperature: Effects on maternal behavior, pup development, and interactions with handling
Jans, J. E., & Woodside, B. C. (1990) · Developmental Psychobiology · doi:10.1002/dev.420230607 · Cited by 77 · see citing works
Experimental Programming of Life Histories
Whimbey, A. E., & Denenberg, V. H. (1967) · Behaviour · doi:10.1163/156853967x00163 · Cited by 77 · see citing works
Blier, P. U., & de Montigny, C. (1999) · Neuropsychopharmacology · doi:10.1038/sj.npp.1395360 · Cited by 40 · see citing works
Neurobiological correlates of defensive behaviors
Bakshi, V. P., Shelton, S. E., & Kalin, N. H. (2000) · Progress in brain research · doi:10.1016/s0079-6123(08)62133-0 · Cited by 21 · see citing works
Bubser, M., & Deutch, A. Y. (1999) · Synapse · doi:10.1002/(sici)1098-2396(199904)32:1
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Cited by
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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 4,981 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
Psychological well-being: evidence regarding its causes and consequences
Huppert, F. A. (2009) · Applied Psychology: Health and Well-Being · doi:10.1111/j.1758-0854.2009.01008.x · Cited by 1,583 · see citing works
Hensch, T. K. (2004) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.27.070203.144327 · Cited by 1,300 · see citing works
Psychobiology and molecular genetics of resilience
Feder, A., Nestler, E. J., & Charney, D. S. (2009) · Nature Reviews Neuroscience · doi:10.1038/nrn2649 · Cited by 1,272 · see citing works
Early behavioral intervention, brain plasticity, and the prevention of autism spectrum disorder
Dawson, G. (2008) · Development and Psychopathology · doi:10.1017/s0954579408000370 · Cited by 1,138 · see citing works
von Borell, E., Langbein, J., Desprès, G., Hansen, S., Leterrier, C., Marchant, J. N., Marchant-Forde, R. M., Minero, M., Möhr, E., Prunier, A., et al. (2007) · Physiology & Behavior · doi:10.1016/j.physbeh.2007.01.007 · Cited by 973 · see citing works
Pubertal transitions in health
Patton, G. C., & Viner, R. (2007) · The Lancet · doi:10.1016/s0140-6736(07)60366-3 · Cited by 871 · see citing works
Epigenetic mechanisms and the transgenerational effects of maternal care
Champagne, F. A. (2008) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2008.03.003 · Cited by 812 · see citing works
Kuzawa, C. W., & Sweet, E. (2008) · American Journal of Human Biology · doi:10.1002/ajhb.20822 · Cited by 683 · see citing works
A review of adversity, the amygdala and the hippocampus: a consideration of developmental timing
Tottenham, N. (2009) · Frontiers in Human Neuroscience · doi:10.3389/neuro.09.068.2009 · Cited by 651 · see citing works
Neurobiological and psychiatric consequences of child abuse and neglect
Heim, C., Shugart, M., Craighead, W. E., & Nemeroff, C. B. (2010) · Developmental Psychobiology · doi:10.1002/dev.20494 · Cited by 613 · see citing works
Cognitive impairment associated to HPA axis hyperactivity after maternal separation in rats
Aisa, B., Tordera, R. M., Lasheras, B., Rı́o, J. D., & Ramírez, M. J. (2007) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2006.12.013 · Cited by 534 · see citing works
De Bellis, M. D. (2005) · Child Maltreatment · doi:10.1177/1077559505275116 · Cited by 531 · see citing works
Animal models of major depression: drawbacks and challenges
Planchez, B., Surget, A., & Belzung, C. (2019) · Journal of Neural Transmission · doi:10.1007/s00702-019-02084-y · Cited by 480 · see citing works
Stress and the developing adolescent brain
Eiland, L. R., & Romeo, R. D. (2012) · Neuroscience · doi:10.1016/j.neuroscience.2012.10.048 · Cited by 491 · see citing works
Early experience and the development of stress reactivity and regulation in children
Loman, M. M., & Gunnar, M. R. (2009) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2009.05.007 · Cited by 489 · 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
Treatment resistant depression: A multi-scale, systems biology approach
Akil, H., Gordon, J. A., Hen, R., Javitch, J. A., Mayberg, H. S., McEwen, B. S., Meaney, M. J., & Nestler, E. J. (2017) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2017.08.019 · Cited by 443 · see citing works
Self-citationBlair, C. (2006) · Behavioral and Brain Sciences · doi:10.1017/s0140525x06009034 · Cited by 434 · see citing works
McLaughlin, K. A., Sheridan, M. A., Tibu, F., Fox, N. A., Zeanah, C. H., & Nelson, C. A. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1423363112 · Cited by 426 · see citing works
Environment and Brain Plasticity: Towards an Endogenous Pharmacotherapy
Sale, A., Berardi, N., & Maffei, L. (2014) · Physiological Reviews · doi:10.1152/physrev.00036.2012 · Cited by 402 · see citing works
Valence is a basic building block of emotional life
Barrett, L. F. (2005) · Journal of Research in Personality · doi:10.1016/j.jrp.2005.08.006 · Cited by 402 · see citing works
Millstein, R. A., & Holmes, A. (2007) · Neuroscience and Biobehavioral Reviews · doi:10.1016/j.neubiorev.2006.05.003 · Cited by 407 · see citing works
Stress and the development of self-regulation in context
Blair, C. (2010) · Child Development Perspectives · doi:10.1111/j.1750-8606.2010.00145.x · Cited by 379 · see citing works
“The findings of Francis et al. (2002) and Bredy et al. (2003) indicate that the effects of enrichment as seen at the behavioral level are not necessarily mirrored in expected changes at the biological level (Fernandez-Teruel et al., 2002).”
BackgroundChampagne, F. A., & Meaney, M. J. (2007) · Behavioral Neuroscience · doi:10.1037/0735-7044.121.6.1353 · Cited by 381 · see citing works
Self-citationStress and the adolescent brain
ROMEO, R. D., & McEWEN, B. S. (2006) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1376.022 · Cited by 379 · see citing works
Ladd, C. O., Huot, R. L., Thrivikraman, K. V., Nemeroff, C. B., & Plotsky, P. M. (2004) · Biological Psychiatry · doi:10.1016/j.biopsych.2003.10.007 · Cited by 368 · see citing works
Self-citationGunnar, M. R., Frenn, K., Wewerka, S. S., & Van Ryzin, M. J. (2009) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2008.08.013 · Cited by 363 · see citing works
Environmental influence in the brain, human welfare and mental health
Tost, H., Champagne, F. A., & Meyer‐Lindenberg, A. (2015) · Nature Neuroscience · doi:10.1038/nn.4108 · Cited by 349 · see citing works
Maternal programming of steroid receptor expression and phenotype through DNA methylation in the rat
Szyf, M., Weaver, I. C. G., Champagne, F. A., Diorio, J., & Meaney, M. J. (2005) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2005.10.002 · Cited by 348 · see citing works
Self-citationExposure to postnatal depression predicts elevated cortisol in adolescent offspring
Halligan, S. L., Herbert, J., Goodyer, I. M., & Murray, L. (2004) · Biological Psychiatry · doi:10.1016/j.biopsych.2003.09.013 · Cited by 342 · see citing works
Brenhouse, H. C., & Andersen, S. L. (2011) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2011.04.013 · Cited by 340 · see citing works
Morning cortisol Levels in preschool‐aged foster children: Differential effects of maltreatment type
Bruce, J., Fisher, P. A., Pears, K. C., & Levine, S. D. (2008) · Developmental Psychobiology · doi:10.1002/dev.20333 · Cited by 340 · see citing works
Social stress, therapeutics and drug abuse: Preclinical models of escalated and depressed intake
MICZEK, K., YAP, J., & COVINGTONIII, H. (2008) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2008.07.006 · Cited by 338 · see citing works
Stress, age, and immune function: toward a lifespan approach
Graham, J. E., Christian, L. M., & Kiecolt-Glaser, J. K. (2006) · Journal of Behavioral Medicine · doi:10.1007/s10865-006-9057-4 · Cited by 329 · see citing works
Gunnar, M. R., Fisher, P. A., & THE EARLY EXPERIENCE, S. (2006) · Development and Psychopathology · doi:10.1017/s0954579406060330 · Cited by 329 · see citing works
Andersen, S. L., & Teicher, M. H. (2009) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2008.09.009 · Cited by 326 · 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-citationAdolescence: A central event in shaping stress reactivity
Romeo, R. D. (2010) · Developmental Psychobiology · doi:10.1002/dev.20437 · Cited by 325 · see citing works
Beijers, R., Buitelaar, J. K., & de Weerth, C. (2014) · European Child & Adolescent Psychiatry · doi:10.1007/s00787-014-0566-3 · Cited by 321 · see citing works
Uchida, S., Hara, K., Kobayashi, A., Funato, H., Hobara, T., Otsuki, K., Yamagata, H., McEwen, B. S., & Watanabe, Y. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.1436-10.2010 · Cited by 310 · see citing works
Morley‐Fletcher, S., Rea, M., Maccari, S., & Laviola, G. (2003) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2003.03070.x · Cited by 373 · see citing works
Resilience to Chronic Stress Is Mediated by Hippocampal Brain-Derived Neurotrophic Factor
Taliaz, D., Loya, A., Gersner, R., Haramati, S., Chen, A., & Zangen, A. (2011) · The Journal of Neuroscience · doi:10.1523/jneurosci.5725-10.2011 · Cited by 311 · see citing works
Laviola, G., Hannan, A. J., Macrì, S., Solinas, M., & Jaber, M. (2008) · Neurobiology of Disease · doi:10.1016/j.nbd.2008.05.001 · Cited by 300 · see citing works
Cirulli, F., Berry, A., & Alleva, E. (2003) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(03)00010-1 · Cited by 303 · see citing works
Fisher, P. A., Gunnar, M. R., Dozier, M., Bruce, J., & Pears, K. C. (2006) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1376.023 · Cited by 303 · see citing works
Stress Neurobiology and Developmental Psychopathology
Gunnar, M. R., & Vázquez, D. M. (2015) · Wiley eBooks · doi:10.1002/9780470939390.ch13 · Cited by 291 · see citing works
Recognizing resilience: Learning from the effects of stress on the brain
McEwen, B. S., Gray, J. D., & Nasca, C. (2015) · Neurobiology of Stress · doi:10.1016/j.ynstr.2014.09.001 · Cited by 292 · see citing works
Fox, C., Merali, Z., & Harrison, C. R. (2006) · Behavioural Brain Research · doi:10.1016/j.bbr.2006.08.016 · Cited by 283 · see citing works
McCormick, C. M., Smith, C. L., & Mathews, I. Z. (2007) · Behavioural Brain Research · doi:10.1016/j.bbr.2007.09.005 · Cited by 278 · see citing works
McCormick, C. M., Mathews, I. Z., Thomas, C., & Waters, P. (2010) · Brain and Cognition · doi:10.1016/j.bandc.2009.06.003 · Cited by 276 · see citing works
Research Review: A neuroscience framework for pediatric anxiety disorders
Pine, D. S. (2007) · Journal of Child Psychology and Psychiatry · doi:10.1111/j.1469-7610.2007.01751.x · Cited by 277 · see citing works
Fontana, B. D., Mezzomo, N. J., Kalueff, A. V., & Rosemberg, D. B. (2017) · Experimental Neurology · doi:10.1016/j.expneurol.2017.10.004 · Cited by 275 · see citing works
Maternal neglect: oxytocin, dopamine and the neurobiology of attachment
Strathearn, L. (2011) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2011.02228.x · Cited by 268 · see citing works
Understanding the potency of stressful early life experiences on brain and body function
McEwen, B. S. (2008) · Metabolism · doi:10.1016/j.metabol.2008.07.006 · Cited by 260 · see citing works
Neighborhood matters: divergent patterns of stress-induced plasticity across the brain
Chattarji, S., Tomar, A., Suvrathan, A., Ghosh, S., & Rahman, M. M. (2015) · Nature Neuroscience · doi:10.1038/nn.4115 · Cited by 248 · see citing works
Early maternal separation: a rodent model of depression and a prevailing human condition
Vetulani, J. (2013) · Pharmacological Reports · doi:10.1016/s1734-1140(13)71505-6 · Cited by 255 · see citing works
Macrı̀, S., & Würbel, H. (2006) · Hormones and Behavior · doi:10.1016/j.yhbeh.2006.06.015 · Cited by 253 · see citing works
Prevention and treatment of drug addiction by environmental enrichment
Solinas, M., Thiriet, N., Chauvet, C., & Jaber, M. (2010) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2010.08.002 · Cited by 256 · see citing works
Gunnar, M. R., & Quevedo, K. M. (2007) · Progress in brain research · doi:10.1016/s0079-6123(07)67010-1 · Cited by 246 · see citing works
Macrı̀, S., Mason, G. J., & Würbel, H. (2004) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2004.03541.x · Cited by 240 · see citing works
The Neurobiological Toll of Child Abuse and Neglect
Neigh, G. N., Gillespie, C. F., & Nemeroff, C. B. (2009) · Trauma Violence & Abuse · doi:10.1177/1524838009339758 · Cited by 240 · see citing works
Gowland, R. L. (2015) · American Journal of Physical Anthropology · doi:10.1002/ajpa.22820 · Cited by 232 · see citing works
Mother and newborn baby: Mutual regulation of physiology and behavior— A selective review
Winberg, J. (2005) · Developmental Psychobiology · doi:10.1002/dev.20094 · Cited by 232 · see citing works
Hannan, A. J. (2014) · Neuropathology and Applied Neurobiology · doi:10.1111/nan.12102 · Cited by 240 · see citing works
Stress during development: Impact on neuroplasticity and relevance to psychopathology
Fumagalli, F., Molteni, R., Racagni, G., & Riva, M. A. (2007) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2007.01.002 · Cited by 218 · see citing works
How social experiences influence the brain
Champagne, F. A., & Curley, J. P. (2005) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2005.10.001 · Cited by 217 · see citing works
Cummings, E. M., & Valentino, K. (2015) · Wiley eBooks · doi:10.1002/9781118963418.childpsy115 · Cited by 214 · see citing works
Ford, J. D. (2005) · Psychiatric Annals · doi:10.3928/00485713-20050501-07 · Cited by 211 · see citing works
Gunnar, M. R., DePasquale, C. E., Reid, B. M., Donzella, B., & Miller, B. S. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1909699116 · Cited by 207 · see citing works
Arco, A. D., & Mora, F. (2009) · Journal of Neural Transmission · doi:10.1007/s00702-009-0243-8 · Cited by 201 · see citing works
Silk, J. S., Vanderbilt‐Adriance, E., Shaw, D. S., Forbes, E. E., Whalen, D. J., Ryan, N. D., & Dahl, R. E. (2007) · Development and Psychopathology · doi:10.1017/s0954579407000417 · Cited by 202 · see citing works
Kanitz, E., Tuchscherer, M., Puppe, B., Tuchscherer, A., & Stabenow, B. (2004) · Brain, Behavior, and Immunity · doi:10.1016/s0889-1591(03)00085-0 · Cited by 200 · see citing works
Maternal separation alters drug intake patterns in adulthood in rats
Moffett, M. C., Vicentic, A., Kozel, M. A., Plotsky, P. M., Francis, D. D., & Kuhar, M. J. (2006) · Biochemical Pharmacology · doi:10.1016/j.bcp.2006.08.003 · Cited by 200 · see citing works
Self-citationSteinberg, L., Dahl, R., Keating, D., Kupfer, D., Masten, A., & Pine, D. (2015) · Wiley eBooks · doi:10.1002/9780470939390.ch18 · Cited by 160 · see citing works
Social influences on neurobiology and behavior: Epigenetic effects during development
Curley, J. P., Jensen, C. L., Rahia Mashoodh, A., & Champagne, F. A. (2010) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2010.06.005 · Cited by 195 · see citing works
Cellular and molecular mechanisms of immunomodulation in the brain through environmental enrichment
Singhal, G., Jaehne, E. J., Corrigan, F., & Baune, B. T. (2014) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2014.00097 · Cited by 186 · see citing works
Epigenetic mechanisms mediating vulnerability and resilience to psychiatric disorders
Dudley, K. J., Li, X., Kobor, M. S., Kippin, T. E., & Bredy, T. W. (2011) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2010.12.016 · Cited by 180 · see citing works
Maternal separation produces lasting changes in cortisol and behavior in rhesus monkeys
Feng, X., Wang, L., Yang, S., Qin, D., Wang, J., Li, C., Lv, L., Ma, Y., & Hu, X. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1010943108 · Cited by 181 · see citing works
Individual development and evolution: Experiential canalization of self-regulation.
Blair, C., & Raver, C. C. (2012) · Developmental Psychology · doi:10.1037/a0026472 · Cited by 174 · see citing works
Evolution and ontogeny of stress response to social challenges in the human child
FLINN, M. (2006) · Developmental Review · doi:10.1016/j.dr.2006.02.003 · Cited by 173 · see citing works
Early life stress in fathers improves behavioural flexibility in their offspring
Gapp, K., Soldado-Magraner, S., Álvarez-Sánchez, M., Bohacek, J., Vernaz, G., Shu, H., Franklin, T. B., Wolfer, D. P., & Mansuy, I. M. (2014) · Nature Communications · doi:10.1038/ncomms6466 · Cited by 170 · see citing works
Maniam, J., & Morris, M. J. (2009) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2009.10.013 · Cited by 173 · see citing works
A Systematic Review of the Valproic-Acid-Induced Rodent Model of Autism
Chaliha, D. R., Albrecht, M. A., Vaccarezza, M., Takechi, R., Lam, V., Al‐Salami, H., & Mamo, J. C. L. (2020) · Developmental Neuroscience · doi:10.1159/000509109 · Cited by 173 · see citing works
Del Arco, A., & Mora, F. (2008) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2008.04.011 · Cited by 163 · see citing works
Fabricius, K., Wörtwein, G., & Pakkenberg, B. (2008) · Brain Structure and Function · doi:10.1007/s00429-007-0169-6 · Cited by 165 · see citing works
Cicchetti, D., Rogosch, F. A., Toth, S. L., & Sturge-Apple, M. L. (2011) · Development and Psychopathology · doi:10.1017/s0954579411000307 · Cited by 168 · see citing works
Priebe, K., Brake, W. G., Romeo, R. D., Sisti, H. M., Mueller, A., McEwen, B. S., & Francis, D. D. (2005) · Developmental Psychobiology · doi:10.1002/dev.20098 · Cited by 168 · see citing works
Self-citationPrimary parental preoccupation: circuits, genes, and the crucial role of the environment
Leckman, J. F., Feldman, R., Swain, J. E., Eicher, V. W., Thompson, N., & Mayes, L. C. (2004) · Journal of Neural Transmission · doi:10.1007/s00702-003-0067-x · Cited by 168 · see citing works
Lajud, N., Roque, A., Cajero, M., Gutiérrez‐Ospina, G., & Torner, L. (2011) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2011.07.011 · Cited by 162 · see citing works
The impact of gestational stress and prenatal growth on emotional problems in offspring: a review
Rice, F. J., Jones, I. R., & Thapar, A. (2006) · Acta Psychiatrica Scandinavica · doi:10.1111/j.1600-0447.2006.00895.x · Cited by 164 · see citing works
Trauma, Proximity, and Developmental Psychopathology: The Effects of War and Terrorism on Children
Pine, D. S., Costello, J. E., & Masten, A. S. (2005) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300814 · Cited by 165 · see citing works
The anxiolytic effect of environmental enrichment is mediated via amygdalar CRF receptor type 1
Sztainberg, Y., Kuperman, Y., Tsoory, M., Lebow, M., & Chen, A. (2010) · Molecular Psychiatry · doi:10.1038/mp.2009.151 · Cited by 159 · see citing works
Leuner, B., Glasper, E. R., & Gould, E. (2010) · Trends in Neurosciences · doi:10.1016/j.tins.2010.07.003 · Cited by 159 · see citing works
Ancient origins of human developmental plasticity
Crespi, E. J., & Denver, R. J. (2004) · American Journal of Human Biology · doi:10.1002/ajhb.20098 · Cited by 153 · see citing works
Human amygdala development in the absence of species‐expected caregiving
Tottenham, N. (2012) · Developmental Psychobiology · doi:10.1002/dev.20531 · Cited by 149 · see citing works
- 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
- Social Sciences › Psychology › Social Psychology › 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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