Neural Mechanisms of Stress Resilience and Vulnerability

Franklin, Tamara B.; Saab, Bechara J.; Mansuy, Isabelle M.

doi:10.1016/j.neuron.2012.08.016

Cited by 500Stress Responses and CortisolResilience and Mental HealthMemory and Neural Mechanisms

Neural Mechanisms of Stress Resilience and Vulnerability

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Franklin, Tamara B., Saab, Bechara J., Mansuy, Isabelle M.·2012·Neuron

DOI 10.1016/j.neuron.2012.08.016

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Abstract

Exposure to stressful events can be differently perceived by individuals and can have persistent sequelae depending on the level of stress resilience or vulnerability of each person. The neural processes that underlie such clinically and socially important differences reside in the anatomical, functional, and molecular connectivity of the brain. Recent work has provided novel insight into some of the involved biological mechanisms that promises to help prevent and treat stress-related disorders. In this review, we focus on causal and mechanistic evidence implicating altered functions and connectivity of the neuroendocrine system, and of hippocampal, cortical, reward, and serotonergic circuits in the establishment and the maintenance of stress resilience and vulnerability. We also touch upon recent findings suggesting a role for epigenetic mechanisms and neurogenesis in these processes and briefly discuss promising avenues of future investigation.

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Epigenetic regulation of the glucocorticoid receptor in human brain associates with childhood abuse
McGowan, P. O., Sasaki, A., D'Alessio, A. C., Dymov, S., Labonté, B., Szyf, M., Turecki, G., & Meaney, M. J. (2009) · Nature Neuroscience · doi:10.1038/nn.2270 · Cited by 3,531 · see citing works
The concept of allostasis in biology and biomedicine
McEwen, B. S., & Wingfield, J. C. (2003) · Hormones and Behavior · doi:10.1016/s0018-506x(02)00024-7 · Cited by 3,302 · cited 1× · see citing works
“Allostatic load model Cumulative cost of continual adaptation to repeated predictable stress (McEwen and Wingfield, 2003; Sterling and Eyer, 1988).”
Stress signalling pathways that impair prefrontal cortex structure and function
Arnsten, A. F. T. (2009) · Nature Reviews Neuroscience · doi:10.1038/nrn2648 · Cited by 3,299 · see citing works
Maternal Care, Hippocampal Glucocorticoid Receptors, and Hypothalamic-Pituitary-Adrenal Responses to Stress
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
Chronic antidepressant treatment increases neurogenesis in adult rat hippocampus
Malberg, J. E., Eisch, A. J., Nestler, E. J., & Duman, R. S. (2000) · The Journal of Neuroscience · doi:10.1523/jneurosci.20-24-09104.2000 · Cited by 3,111 · see citing works
Adult Neurogenesis in the Mammalian Brain: Significant Answers and Significant Questions
Ming, G.-L., & Song, H. (2011) · Neuron · doi:10.1016/j.neuron.2011.05.001 · Cited by 2,651 · see citing works
Brain 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
Molecular Adaptations Underlying Susceptibility and Resistance to Social Defeat in Brain Reward Regions
Krishnan, V., Han, M.-H., Graham, D. L., Berton, O., Renthal, W., Russo, S. J., LaPlant, Q., Graham, A., Lutter, M., Lagace, D. C., et al. (2007) · Cell · doi:10.1016/j.cell.2007.09.018 · Cited by 2,307 · cited 3× · see citing works
“Moreover, they also reproduce the variability in response observed in humans since submissive behaviors and social avoidance occur in only about 50%–60% of animals (Krishnan et al., 2007; Strekalova et al., 2004).”
Impact of Gender, Menstrual Cycle Phase, and Oral Contraceptives on the Activity of the Hypothalamus-Pituitary-Adrenal Axis
Kirschbaum, C., Kudielka, B. M., Gaab, J., Schommer, N. C., & Hellhammer, D. H. (1999) · Psychosomatic Medicine · doi:10.1097/00006842-199903000-00006 · Cited by 1,890 · cited 1× · see citing works
“Review sex bias in response to stress is reminiscent to observations in human (Kirschbaum et al., 1999).”
Neural mechanisms of the cognitive model of depression.
Disner, S. G., Beevers, C. G., Haigh, E. A. P., & Beck, A. T. (2011) · Nature Reviews Neuroscience · doi:10.1038/nrn3027 · Cited by 1,718 · see citing works
Missing heritability and strategies for finding the underlying causes of complex disease
Eichler, E. E., Flint, J., Gibson, G. C., Kong, A., Leal, S. M., Moore, J. H., & Nadeau, J. H. (2010) · Nature Reviews Genetics · doi:10.1038/nrg2809 · Cited by 1,671 · see citing works
Early, postnatal experience alters hypothalamic corticotropin-releasing factor (CRF) mRNA, median eminence CRF content and stress-induced release in adult rats
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
Mouse genomic variation and its effect on phenotypes and gene regulation.
Keane, T. M., Goodstadt, L., Danecek, P., White, M. A., Wong, K., Yalcin, B., Heger, A., Agam, A., Slater, G., Goodson, M., et al. (2011) · Nature · doi:10.1038/nature10413 · Cited by 1,580 · see citing works
Differential projections of the infralimbic and prelimbic cortex in the rat
Vertes, R. P. (2004) · Synapse · doi:10.1002/syn.10279 · Cited by 1,550 · see citing works
Coping Resources, Coping Processes, and Mental Health
Taylor, S. E., & Stanton, A. L. (2007) · Annual Review of Clinical Psychology · doi:10.1146/annurev.clinpsy.3.022806.091520 · Cited by 1,462 · see citing works
Allostasis: A New Paradigm to Explain Arousal Pathology
Sterling, P., & Eyer, J. (1988) · Zenodo · doi:10.5281/zenodo.13537700 · Cited by 1,450 · see citing works
Handbook of Life Stress, Cognition and Health
PASTOR, L. H. (1989) · American Journal of Psychiatry · doi:10.1176/ajp.146.10.1347 · Cited by 1,402 · see citing works
The stressed synapse: the impact of stress and glucocorticoids on glutamate transmission
Popoli, M., Yan, Z., McEwen, B. S., & Sanacora, G. (2012) · Nature Reviews Neuroscience · doi:10.1038/nrn3138 · Cited by 1,393 · see citing works
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
Reduced caudate and nucleus accumbens response to rewards in unmedicated individuals with major depressive disorder
Pizzagalli, D. A., Holmes, A. J., Dillon, D. G., Goetz, E. L., Birk, J. L., Bogdan, R., Dougherty, D. D., Iosifescu, D. V., Rauch, S. L., & Fava, M. (2009) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2008.08081201 · Cited by 1,232 · see citing works
The role of the medial prefrontal cortex (cingulate gyrus) in the regulation of hypothalamic-pituitary-adrenal responses to stress
Diorio, 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
Epigenetic transmission of the impact of early stress across generations
Franklin, T. B., Russig, H., Weiss, I. C., Gräff, J., Linder, N., Michalon, A., Vizi, S., & Mansuy, I. M. (2010) · Biological Psychiatry · doi:10.1016/j.biopsych.2010.05.036 · Cited by 1,125 · cited 3× · see citing works
“This progeny, but also the following, show multiple stress-related symptoms such as depressive-like behaviors, and social anxiety (Franklin et al., 2011; Franklin et al., 2010; Weiss et al., 2011).”
Self-citation
The reactive scope model — A new model integrating homeostasis, allostasis, and stress
Romero, L. M., Dickens, M. J., & Cyr, N. E. (2009) · Hormones and Behavior · doi:10.1016/j.yhbeh.2008.12.009 · Cited by 1,096 · see citing works
Towards a glutamate hypothesis of depression
Sanacora, G., Treccani, G., & Popoli, M. (2012) · Neuropharmacology · doi:10.1016/j.neuropharm.2011.07.036 · Cited by 1,036 · see citing works
Ablation of hippocampal neurogenesis impairs contextual fear conditioning and synaptic plasticity in the dentate gyrus
Saxe, M. D., Battaglia, F., Wang, J.-W., Malleret, G., David, D. J., Monckton, J. E., Garcia, A. D. R., Sofroniew, M. V., Kandel, E. R., Santarelli, L., et al. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0607207103 · Cited by 1,020 · see citing works
Social influences on neuroplasticity: stress and interventions to promote well-being
Davidson, R. J., & McEwen, B. S. (2012) · Nature Neuroscience · doi:10.1038/nn.3093 · Cited by 892 · see citing works
The medial prefrontal cortex in the rat: evidence for a dorso-ventral distinction based upon functional and anatomical characteristics
Heidbreder, C. A., & Groenewegen, H. J. (2003) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2003.09.003 · Cited by 882 · see citing works
Early Environmental Regulation of Forebrain Glucocorticoid Receptor Gene Expression: Implications for Adrenocortical Responses to Stress; pp. 49–60
Meaney, M. J., Diorio, J., Francis, D., Widdowson, J., LaPlante, P., Caldji, C., Sharma, S., Seckl, J. R., & Plotsky, P. M. (2010) · Developmental Neuroscience · doi:10.1159/000111395 · Cited by 878 · see citing works
Neurogenesis may relate to some but not all types of hippocampal‐dependent learning
Shors, T. J., Townsend, D. A., Zhao, M., Kozorovitskiy, Y., & Gould, E. (2002) · Hippocampus · doi:10.1002/hipo.10103 · Cited by 853 · see citing works
The structural and functional connectivity of the amygdala: from normal emotion to pathological anxiety
Kim, M. J., Loucks, R. A., Palmer, A. L., Brown, A. C., Solomon, K. M., Marchante, A. N., & Whalen, P. J. (2011) · Behavioural Brain Research · doi:10.1016/j.bbr.2011.04.025 · Cited by 838 · see citing works
Mineralocorticoid receptors are indispensable for nongenomic modulation of hippocampal glutamate transmission by corticosterone
Karst, H., Berger, S., Turiault, M., Tronche, F., Schütz, G., & Joëls, M. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0507572102 · Cited by 774 · see citing works
Regulation of adult neurogenesis by excitatory input and NMDA receptor activation in the dentate gyrus
Cameron, H. A., McEwen, B., & Gould, E. A. (1995) · Journal of Neuroscience · doi:10.1523/jneurosci.15-06-04687.1995 · Cited by 743 · see citing works
Infantile Experience and Resistance to Physiological Stress
Levine, S. (1957) · Science · doi:10.1126/science.126.3270.405 · Cited by 659 · see citing works
Adrenal hormones suppress cell division in the adult rat dentate gyrus
Gould, E., Cameron, H. A., Daniels, D., Woolley, C. S., & McEwen, B. (1992) · Journal of Neuroscience · doi:10.1523/jneurosci.12-09-03642.1992 · Cited by 652 · see citing works
Antidepressant effect of optogenetic stimulation of the medial prefrontal cortex
Covington, H. E., Lobo, M. K., Maze, I., Vialou, V., Hyman, J. M., Zaman, S., LaPlant, Q., Mouzon, E., Ghose, S., Tamminga, C. A., et al. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.1731-10.2010 · Cited by 621 · see citing works
Fear conditioning, synaptic plasticity and the amygdala: implications for posttraumatic stress disorder
Mahan, A. L., & Ressler, K. J. (2011) · Trends in Neurosciences · doi:10.1016/j.tins.2011.06.007 · Cited by 616 · see citing works
Dnmt3a regulates emotional behavior and spine plasticity in the nucleus accumbens
LaPlant, Q., Vialou, V., Covington, H. E., Dumitriu, D., Feng, J., Warren, B. L., Maze, I., Dietz, D. M., Watts, E. L., Iñiguez, S. D., et al. (2010) · Nature Neuroscience · doi:10.1038/nn.2619 · Cited by 612 · see citing works
The mood-improving actions of antidepressants do not depend on neurogenesis but are associated with neuronal remodeling
Bessa, J. M., Ferreira, D., Melo, I., Marques, F., Cerqueira, J. J., Palha, J. A., Almeida, O. F. X., & Sousa, N. (2009) · Molecular Psychiatry · doi:10.1038/mp.2008.119 · Cited by 598 · see citing works
Stress and anxiety: Structural plasticity and epigenetic regulation as a consequence of stress
McEwen, B. S., Eiland, L., Hunter, R. G., & Miller, M. M. (2012) · Neuropharmacology · doi:10.1016/j.neuropharm.2011.07.014 · Cited by 596 · see citing works
Limbic Regulation of Hypothalamo‐Pituitary‐Adrenocortical Function during Acute and Chronic Stress
Jankord, R., & Herman, J. P. (2008) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1410.012 · Cited by 578 · see citing works
5-HT1A receptor function in major depressive disorder
Savitz, J. B., Lucki, I., & Drevets, W. C. (2009) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2009.01.009 · Cited by 573 · see citing works
Sociodemographic and psychopathologic predictors of first incidence of DSM-IV substance use, mood and anxiety disorders: results from the Wave 2 National Epidemiologic Survey on Alcohol and Related Conditions
Grant, B. F., Goldstein, R. B., Chou, S. P., Huang, B., Stinson, F. S., Dawson, D. A., Saha, T. D., Smith, S. M., Pulay, A. J., Pickering, R. P., et al. (2008) · Molecular Psychiatry · doi:10.1038/mp.2008.41 · Cited by 568 · see citing works
Stress-Induced Anhedonia in Mice is Associated with Deficits in Forced Swimming and Exploration
Strekalova, T. V., Spanagel, R., Bartsch, D., Henn, F. A., & Gass, P. (2004) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300532 · Cited by 564 · see citing works
Depletion in serotonin decreases neurogenesis in the dentate gyrus and the subventricular zone of adult rats
Brezun, J. M., & Daszuta, A. (1999) · Neuroscience · doi:10.1016/s0306-4522(98)00693-9 · Cited by 549 · see citing works
Adult hippocampal neurogenesis is involved in anxiety-related behaviors
Revest, J.-M., Dupret, D., Koehl, M., Funk-Reiter, C., Grosjean, N., Piazza, P.-V., & Abrous, D. N. (2009) · Molecular Psychiatry · doi:10.1038/mp.2009.15 · Cited by 549 · see citing works
Childhood Adversity and Epigenetic Modulation of the Leukocyte Glucocorticoid Receptor: Preliminary Findings in Healthy Adults
Tyrka, A. R., Price, L. H., Marsit, C., Walters, O. C., & Carpenter, L. L. (2012) · PLoS ONE · doi:10.1371/journal.pone.0030148 · Cited by 486 · see citing works
Animal model of depression: Pharmacological sensitivity of a hedonic deficit
Katz, R. J. (1982) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(82)90053-3 · Cited by 480 · see citing works
ΔFosB in brain reward circuits mediates resilience to stress and antidepressant responses
Vialou, V., Robison, A. J., LaPlant, Q. C., Covington, H. E., Dietz, D. M., Ohnishi, Y. N., Mouzon, E., Rush, A. J., Watts, E. L., Wallace, D. L., et al. (2010) · Nature Neuroscience · doi:10.1038/nn.2551 · Cited by 479 · see citing works
The Human Capacity to Thrive in the Face of Potential Trauma
Bonanno, G. A., & Mancini, A. D. (2008) · PEDIATRICS · doi:10.1542/peds.2007-1648 · Cited by 477 · see citing works
Anxiolytic- and antidepressant-like effects of the non-peptide vasopressin V <sub>1b</sub> receptor antagonist, SSR149415, suggest an innovative approach for the treatment of stress-related disorders
Griebel, G., Simiand, J., Serradeil-Le Gal, C., Wagnon, J., Pascal, M., Scatton, B., Maffrand, J.-P., & Soubrié, P. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.092012099 · Cited by 471 · see citing works
Psychobiological allostasis: resistance, resilience and vulnerability
Karatsoreos, I. N., & McEwen, B. S. (2011) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2011.10.005 · Cited by 458 · see citing works
Regional Differentiation of the Medial Prefrontal Cortex in Regulating Adaptive Responses to Acute Emotional Stress
Radley, J. J., Arias, C. M., & Sawchenko, P. E. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.4297-06.2006 · Cited by 456 · see citing works
Knockdown of brain-derived neurotrophic factor in specific brain sites precipitates behaviors associated with depression and reduces neurogenesis
Taliaz, D., Stall, N., Dar, D. E., & Zangen, A. (2010) · Molecular Psychiatry · doi:10.1038/mp.2009.67 · Cited by 454 · see citing works
Broad Epigenetic Signature of Maternal Care in the Brain of Adult Rats
McGowan, P. O., Suderman, M., Sasaki, A., Huang, T. C. T., Hallett, M., Meaney, M. J., & Szyf, M. (2011) · PLoS ONE · doi:10.1371/journal.pone.0014739 · Cited by 452 · see citing works
5-HT1A autoreceptor levels determine vulnerability to stress and response to antidepressants
Richardson-Jones, J. W., Craige, C. P., Guiard, B. P., Stephen, A., Metzger, K. L., Kung, H. F., Gardier, A. M., Dranovsky, A., David, D. J., Beck, S. G., et al. (2010) · Neuron · doi:10.1016/j.neuron.2009.12.003 · Cited by 450 · see citing works
Resilience to social stress coincides with functional DNA methylation of the Crf gene in adult mice
Elliott, E., Ezra-Nevo, G., Regev, L., Neufeld-Cohen, A., & Chen, A. (2010) · Nature Neuroscience · doi:10.1038/nn.2642 · Cited by 436 · see citing works
Restraint stress in biobehavioral research: Recent developments
Buynitsky, T., & Mostofsky, D. I. (2009) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2009.05.004 · Cited by 426 · see citing works
Stress, stress hormones, and adult neurogenesis
Schoenfeld, T. J., & Gould, E. (2011) · Experimental Neurology · doi:10.1016/j.expneurol.2011.01.008 · Cited by 425 · see citing works
Mesolimbic dopamine neurons in the brain reward circuit mediate susceptibility to social defeat and antidepressant action
Cao, J.-L., Covington, H. E., Friedman, A. K., Wilkinson, M. B., Walsh, J. J., Cooper, D. C., Nestler, E. J., & Han, M.-H. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.3177-10.2010 · Cited by 402 · see citing works
Sex differences in corticotropin-releasing factor receptor signaling and trafficking: potential role in female vulnerability to stress-related psychopathology
Bangasser, D. A., Curtis, A., Reyes, B. A. S., Bethea, T. T., Parastatidis, I., Ischiropoulos, H., Van Bockstaele, E. J., & Valentino, R. J. (2010) · Molecular Psychiatry · doi:10.1038/mp.2010.66 · Cited by 401 · see citing works
Epigenetic Status of Gdnf in the Ventral Striatum Determines Susceptibility and Adaptation to Daily Stressful Events
Uchida, S., Hara, K., Kobayashi, A., Otsuki, K., Yamagata, H., Hobara, T., Suzuki, T., Miyata, N., & Watanabe, Y. (2011) · Neuron · doi:10.1016/j.neuron.2010.12.023 · Cited by 398 · see citing works
Emerging role of glutamate in the pathophysiology of major depressive disorder
Hashimoto, K. (2009) · Brain Research Reviews · doi:10.1016/j.brainresrev.2009.05.005 · Cited by 381 · see citing works
Chronic stress: Implications for neuronal morphology, function and neurogenesis
Joëls, M., Karst, H., Krugers, H. J., & Lucassen, P. J. (2007) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2007.04.001 · Cited by 381 · 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
Involvement of AMPA receptor in both the rapid and sustained antidepressant-like effects of ketamine in animal models of depression
Koike, H., Iijima, M., & Chaki, S. (2011) · Behavioural Brain Research · doi:10.1016/j.bbr.2011.05.035 · Cited by 346 · see citing works
Paternal Transmission of Stress-Induced Pathologies
Dietz, D. M., LaPlant, Q., Watts, E. L., Hodes, G. E., Russo, S. J., Feng, J., Oosting, R. S., Vialou, V., & Nestler, E. J. (2011) · Biological Psychiatry · doi:10.1016/j.biopsych.2011.05.005 · Cited by 346 · see citing works
Functional anatomy of ventromedial prefrontal cortex: implications for mood and anxiety disorders
Myers-Schulz, B., & Koenigs, M. (2012) · Molecular Psychiatry · doi:10.1038/mp.2011.88 · Cited by 333 · see citing works
Corticotropin-releasing hormone receptor subtypes and emotion
Steckler, T., & Holsboer, F. (1999) · Biological Psychiatry · doi:10.1016/s0006-3223(99)00170-5 · Cited by 323 · see citing works
Serotonergic modulation of the limbic system
Hensler, J. G. (2006) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2005.06.007 · Cited by 319 · see citing works
Environmental enrichment requires adult neurogenesis to facilitate the recovery from psychosocial stress
Schloesser, R. J., Lehmann, M., Martinowich, K., Manji, H. K., & Herkenham, M. (2010) · Molecular Psychiatry · doi:10.1038/mp.2010.34 · Cited by 319 · 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
Interaction between a selective 5‐HT1Areceptor antagonist and an SSRI in vivo: effects on 5‐HT cell firing and extracellular 5‐HT
Gartside, S. E., Umbers, V., Hajós, M., & Sharp, T. (1995) · British Journal of Pharmacology · doi:10.1111/j.1476-5381.1995.tb15919.x · Cited by 311 · see citing works
Early life stress enhances behavioral vulnerability to stress through the activation of REST4-mediated gene transcription in the medial prefrontal cortex of rodents
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
Early disruption of the mother–infant relationship: effects on brain plasticity and implications for psychopathology
Cirulli, F., Berry, A., & Alleva, E. (2003) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(03)00010-1 · Cited by 303 · see citing works
A Role for Repressive Histone Methylation in Cocaine-Induced Vulnerability to Stress
Covington, H. E., Maze, I., Sun, H., Bomze, H. M., DeMaio, K. D., Wu, E. Y., Dietz, D. M., Lobo, M. K., Ghose, S., Mouzon, E., et al. (2011) · Neuron · doi:10.1016/j.neuron.2011.06.007 · 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
Comparison of the effects of early handling and early deprivation on maternal care in the rat
Pryce, C. R., Rüedi‐Bettschen, D., & Feldon, J. (2001) · Developmental Psychobiology · doi:10.1002/dev.1018 · Cited by 270 · see citing works
Imipramine Treatment and Resiliency Exhibit Similar Chromatin Regulation in the Mouse Nucleus Accumbens in Depression Models
Wilkinson, M. B., Xiao, G., Kumar, A., LaPlant, Q., Renthal, W., Sikder, D., Kodadek, T. J., & Nestler, E. J. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.0932-09.2009 · Cited by 262 · see citing works
BDNF and glucocorticoids regulate corticotrophin-releasing hormone (CRH) homeostasis in the hypothalamus
Jeanneteau, F. D., Lambert, W. M., Ismaili, N., Bath, K. G., Lee, F. S., Garabedian, M. J., & Chao, M. V. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1114122109 · Cited by 252 · see citing works
Individual Differences in Reactivity to Social Stress Predict Susceptibility and Resilience to a Depressive Phenotype: Role of Corticotropin-Releasing Factor
Wood, S. K., Walker, H. E., Valentino, R. J., & Bhatnagar, S. (2010) · Endocrinology · doi:10.1210/en.2009-1026 · Cited by 251 · see citing works
Differential patterns of whole-genome DNA methylation in institutionalized children and children raised by their biological parents
Naumova, O. Y., Lee, M., Koposov, R. A., Moshe Szyf, A., Dozier, M., & Grigorenko, E. L. (2011) · Development and Psychopathology · doi:10.1017/s0954579411000605 · Cited by 251 · see citing works
Previous Experience with Behavioral Control over Stress Blocks the Behavioral and Dorsal Raphe Nucleus Activating Effects of Later Uncontrollable Stress: Role of the Ventral Medial Prefrontal Cortex
Amat, J., Paul, E., Zarza, C., Watkins, L. R., & Maier, S. F. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.3630-06.2006 · Cited by 249 · see citing works
The neurogenesis hypothesis of affective and anxiety disorders: Are we mistaking the scaffolding for the building?
Petrik, D., Lagace, D. C., & Eisch, A. J. (2012) · Neuropharmacology · doi:10.1016/j.neuropharm.2011.09.003 · Cited by 241 · cited 1× · see citing works
“However, it can also sometimes increase anxiety after stress but have no effect on depression or even have no effect at all (Petrik et al., 2012; Revest et al., 2009; Saxe et al., 2006; Shors et al., 2002).”
Adult hippocampal neurogenesis and related neurotrophic factors
Lee, E., & Son, H. (2009) · BMB Reports · doi:10.5483/bmbrep.2009.42.5.239 · Cited by 240 · see citing works
Intracellular and extracellular electrophysiology of nigral dopaminergic neurons—2. Action potential generating mechanisms and morphological correlates
Grace, A. A., & Bunney, B. S. (1983) · Neuroscience · doi:10.1016/0306-4522(83)90136-7 · Cited by 235 · see citing works
Sex, trauma, stress hormones and depression
Young, E., & Korszun, A. (2010) · Molecular Psychiatry · doi:10.1038/mp.2009.94 · Cited by 235 · see citing works
Environmental Enrichment Confers Stress Resiliency to Social Defeat through an Infralimbic Cortex-Dependent Neuroanatomical Pathway
Lehmann, M. L., & Herkenham, M. (2011) · The Journal of Neuroscience · doi:10.1523/jneurosci.0577-11.2011 · Cited by 234 · see citing works
Strain Differences in Stress Responsivity Are Associated with Divergent Amygdala Gene Expression and Glutamate-Mediated Neuronal Excitability
Mozhui, K., Karlsson, R.-M., Kash, T. L., Ihne, J., Norcross, M., Patel, S., Farrell, M. R., Hill, E. E., Graybeal, C., Martin, K. P., et al. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.5017-09.2010 · Cited by 226 · see citing works
Predictable chronic mild stress improves mood, hippocampal neurogenesis and memory
Parihar, V. K., Hattiangady, B., Kuruba, R., Shuai, B., & Shetty, A. K. (2009) · Molecular Psychiatry · doi:10.1038/mp.2009.130 · Cited by 225 · see citing works
Recovery of the Hypothalamic-Pituitary-Adrenal Response to Stress
García, A., Martı́, O., Vallès, A., Dal-Zotto, S., & Armario, A. (2000) · Neuroendocrinology · doi:10.1159/000054578 · Cited by 212 · see citing works
Age‐dependent expression of glucocorticoid‐ and mineralocorticoid receptors on neural precursor cell populations in the adult murine hippocampus
Garcia, A. D. R., Steiner, B., Kronenberg, G., Bick‐Sander, A., & Kempermann, G. (2004) · Aging Cell · doi:10.1111/j.1474-9728.2004.00130.x · Cited by 209 · see citing works
Influence of Early Stress on Social Abilities and Serotonergic Functions across Generations in Mice
Franklin, T. B., Linder, N., Russig, H., Thöny, B., & Mansuy, I. M. (2011) · PLoS ONE · doi:10.1371/journal.pone.0021842 · Cited by 207 · see citing works
Self-citation
Prenatal programing: At the intersection of maternal stress and immune activation
Howerton, C. L., & Bale, T. L. (2012) · Hormones and Behavior · doi:10.1016/j.yhbeh.2012.03.007 · Cited by 205 · see citing works
Glucocorticoid receptor interaction with TrkB promotes BDNF-triggered PLC-γ signaling for glutamate release via a glutamate transporter
Numakawa, T., Kumamaru, E., Adachi, N., Yagasaki, Y., Izumi, A., & Kunugi, H. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0800888106 · Cited by 200 · see citing works
NCS-1 in the Dentate Gyrus Promotes Exploration, Synaptic Plasticity, and Rapid Acquisition of Spatial Memory
Saab, B. J., Georgiou, J., Nath, A., Lee, F. J. S., Wang, M., Michalon, A., Liu, F., Mansuy, I. M., & Roder, J. (2009) · Neuron · doi:10.1016/j.neuron.2009.08.014 · Cited by 198 · see citing works
Self-citation
Stress sensitivity and resilience in the chronic mild stress rat model of depression; an in situ hybridization study
Bergström, A., Jayatissa, M. N., Mørk, A., & Wiborg, O. (2007) · Brain Research · doi:10.1016/j.brainres.2007.12.025 · Cited by 195 · see citing works
Stress inoculation‐induced indications of resilience in monkeys
Lyons, D. M., & Parker, K. J. (2007) · Journal of Traumatic Stress · doi:10.1002/jts.20265 · Cited by 193 · see citing works
Serotonin-1A Autoreceptors Are Necessary and Sufficient for the Normal Formation of Circuits Underlying Innate Anxiety
Richardson-Jones, J. W., Craige, C. P., Nguyen, T. H., Kung, H. F., Gardier, A. M., Dranovsky, A., David, D. J., Guiard, B. P., Beck, S. G., Hen, R., et al. (2011) · The Journal of Neuroscience · doi:10.1523/jneurosci.5836-10.2011 · Cited by 192 · see citing works
The Development and Neurobiology of Infant Attachment and Fear
Landers, M. S., & Sullivan, R. M. (2012) · Developmental Neuroscience · doi:10.1159/000336732 · Cited by 180 · see citing works
Reduced expression of glutamate transporters vGluT1, EAAT2 and EAAT4 in learned helpless rats, an animal model of depression
Zink, M., Vollmayr, B., Gebicke-Haerter, P. J., & Henn, F. A. (2010) · Neuropharmacology · doi:10.1016/j.neuropharm.2009.09.005 · Cited by 177 · see citing works
Epigenetic Inheritance of Disease and Disease Risk
Bohacek, J., & Mansuy, I. M. (2012) · Neuropsychopharmacology · doi:10.1038/npp.2012.110 · Cited by 176 · see citing works
Self-citation
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
Hippocampus, amygdala, and stress: interacting systems that affect susceptibility to addiction
Belujon, P., & Grace, A. A. (2011) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2010.05896.x · Cited by 171 · see citing works
Long-Term Potentiation at CA3–CA1 Hippocampal Synapses with Special Emphasis on Aging, Disease, and Stress
Kumar, A. (2011) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2011.00007 · Cited by 169 · see citing works
Regulation of Neurogenesis and Gliogenesis by Stress and Antidepressant Treatment
Banasr, M., & Duman, R. (2007) · CNS & Neurological Disorders - Drug Targets · doi:10.2174/187152707783220929 · Cited by 169 · see citing works
Inheritable Effect of Unpredictable Maternal Separation on Behavioral Responses in Mice
Weiss, I. C., Franklin, T. B., Vizi, S., & Mansuy, I. M. (2011) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2011.00003 · Cited by 169 · see citing works
Self-citation
Early-Life Experience Reduces Excitation to Stress-Responsive Hypothalamic Neurons and Reprograms the Expression of Corticotropin-Releasing Hormone
Kőrösi, A., Shanabrough, M., McClelland, S., Liu, Z.-W., Borók, E., Gao, X., Horváth, T. L., & Baram, T. Z. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.4214-09.2010 · Cited by 168 · see citing works
Identification of Combinatorial Patterns of Post-Translational Modifications on Individual Histones in the Mouse Brain
Tweedie‐Cullen, R. Y., Brunner, A. M., Grossmann, J., Mohanna, S., Sichau, D., Nanni, P., Panse, C., & Mansuy, I. M. (2012) · PLoS ONE · doi:10.1371/journal.pone.0036980 · Cited by 162 · see citing works
Self-citation
Animal models of early life stress: Implications for understanding resilience
Lyons, D. M., Parker, K. J., & Schatzberg, A. F. (2010) · Developmental Psychobiology · doi:10.1002/dev.20429 · Cited by 157 · see citing works
Epigenetic understanding of gene-environment interactions in psychiatric disorders: a new concept of clinical genetics
Kubota, T., Miyake, K., & Hirasawa, T. (2012) · Clinical Epigenetics · doi:10.1186/1868-7083-4-1 · Cited by 157 · see citing works
Role of vascular endothelial growth factor in adult hippocampal neurogenesis: Implications for the pathophysiology and treatment of depression
Fournier, N. M., & Duman, R. S. (2011) · Behavioural Brain Research · doi:10.1016/j.bbr.2011.04.022 · Cited by 155 · see citing works
AMPA receptor subunit 1 (GluR‐A) knockout mice model the glutamate hypothesis of depression
Chourbaji, S., Vogt, M. A., Fumagalli, F., Sohr, R., Frasca, A., Brandwein, C., Hörtnagl, H., Riva, M. A., Sprengel, R., & Gass, P. (2008) · The FASEB Journal · doi:10.1096/fj.08-106450 · Cited by 144 · see citing works
Sex Differences in Response to Stress and Expression of Depressive-Like Behaviours in the Rat
Dalla, C., Pitychoutis, P. M., Kokras, N., & Papadopoulou‐Daifoti, Z. (2010) · Current topics in behavioral neurosciences · doi:10.1007/7854_2010_94 · Cited by 134 · see citing works
Opioid systems in the dentate gyrus
Drake, C. T., Chavkin, C., & Milner, T. A. (2007) · Progress in brain research · doi:10.1016/s0079-6123(07)63015-5 · Cited by 130 · see citing works
KAP1-Mediated Epigenetic Repression in the Forebrain Modulates Behavioral Vulnerability to Stress
Jakobsson, J., Cordero, M. I., Bisaz, R., Groner, A. C., Busskamp, V., Bensadoun, J., Cammas, F. M., Losson, R., Mansuy, I. M., Sandi, C., et al. (2008) · Neuron · doi:10.1016/j.neuron.2008.09.036 · Cited by 130 · see citing works
Self-citation
Neurobiology of Serotonin in Depression and Suicidea
Stockmeier, C. A. (1997) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1997.tb52362.x · Cited by 130 · see citing works
Chronic mild stress generates clear depressive but ambiguous anxiety-like behaviour in rats
Kompagne, H., Bárdos, G., Szénási, G., Gacsályi, I., Hársing, L. G., & Lévay, G. I. (2008) · Behavioural Brain Research · doi:10.1016/j.bbr.2008.06.008 · Cited by 129 · see citing works
Development of individual differences in stress responsiveness: an overview of factors mediating the outcome of early life experiences
Claessens, S. E. F., Daskalakis, N. P., van der Veen, R., Oitzl, M. S., de Kloet, E. R., & Champagne, D. L. (2010) · Psychopharmacology · doi:10.1007/s00213-010-2118-y · Cited by 119 · see citing works
Anxiety-like behaviour and associated neurochemical and endocrinological alterations in male pups exposed to prenatal stress
Laloux, C., Mairesse, J., Camp, G. V., Giovine, A., Branchi, I., Bouret, S. G., Morley‐Fletcher, S., Bergonzelli, G. E., Malagodi, M., Gradini, R., et al. (2012) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2012.02.010 · Cited by 117 · see citing works
Behavioral profiles and stress-induced corticosteroid secretion in male Wistar rats subjected to short and prolonged periods of maternal separation
Roman, E., Gustafsson, L., Berg, M., & Nylander, I. (2006) · Hormones and Behavior · doi:10.1016/j.yhbeh.2006.06.016 · Cited by 113 · see citing works
Balancing histone methylation activities in psychiatric disorders
Peter, C. J., & Akbarian, S. (2011) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2011.02.003 · Cited by 110 · see citing works
Stress coping stimulates hippocampal neurogenesis in adult monkeys
Lyons, D. M., Buckmaster, P. S., Lee, A. G., Wu, C., Mitra, R., Duffey, L. M., Buckmaster, C. L., Her, S., Patel, P. D., & Schatzberg, A. F. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0914568107 · Cited by 109 · see citing works
Animal models of early life stress: Implications for understanding resilience
Lyons, D. M., Parker, K. J., & Schatzberg, A. F. (2010) · Developmental Psychobiology · doi:10.1002/dev.20500 · Cited by 109 · see citing works
Uncontrollable, But Not Controllable, Stress Desensitizes 5-HT<sub>1A</sub>Receptors in the Dorsal Raphe Nucleus
Rozeske, R. R., Evans, A. K., Frank, M. G., Watkins, L. R., Lowry, C. A., & Maier, S. F. (2011) · The Journal of Neuroscience · doi:10.1523/jneurosci.3095-11.2011 · Cited by 100 · see citing works
DNA methylation as a risk factor in the effects of early life stress
Kinnally, E. L., Feinberg, C., Kim, D. S., Ferguson, K., Leibel, R. L., Coplan, J. D., & Mann, J. J. (2011) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2011.05.001 · Cited by 99 · see citing works
Individual Stress Vulnerability Is Predicted by Short-Term Memory and AMPA Receptor Subunit Ratio in the Hippocampus
Schmidt, M. V., Trümbach, D., Weber, P., Wagner, K., Scharf, S. H., Liebl, C., Datson, N., Namendorf, C., Gerlach, T., Kühne, C., et al. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.4668-10.2010 · Cited by 91 · see citing works
Serum Response Factor Promotes Resilience to Chronic Social Stress through the Induction of ΔFosB
Vialou, V., Maze, I., Renthal, W., LaPlant, Q. C., Watts, E. L., Mouzon, E., Ghose, S., Tamminga, C. A., & Nestler, E. J. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.2496-10.2010 · Cited by 91 · see citing works
Current status and future prospects for epigenetic psychopharmacology
Boks, M. P., de Jong, N. M., Kas, M. J. H., Vinkers, C. H., Fernandes, C., Kahn, R. S., Mill, J., & Ophoff, R. A. (2012) · Epigenetics · doi:10.4161/epi.7.1.18688 · Cited by 89 · see citing works
Depletion of the neural precursor cell pool by glucocorticoids
Yu, S., Patchev, A. V., Wu, Y., Lu, J., Holsboer, F., Zhang, J., Sousa, N., & Almeida, O. F. X. (2009) · Annals of Neurology · doi:10.1002/ana.21812 · Cited by 87 · see citing works
A genomic point-of-view on environmental factors influencing the human brain methylome
LaSalle, J. M. (2011) · Epigenetics · doi:10.4161/epi.6.7.16353 · Cited by 86 · see citing works
Regulation of corticosteroid receptors in the rat brain: the role of serotonin and stress
Robertson, D. A. F., Beattie, J., Reid, I., & Balfour, D. J. K. (2005) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2005.03990.x · Cited by 84 · see citing works
Sex differences in corticotropin-releasing factor signaling and trafficking
Bangasser, D. A., Curtis, A. L., Reyes, B. A. S., Bethea, T. T., Parastatidis, I., Ischiropoulos, H., Bockstaele, E. J. V., & Valentino, R. J. (2010) · Molecular Psychiatry · doi:10.1038/mp.2010.89 · Cited by 83 · see citing works
Testing the cumulative stress and mismatch hypotheses of psychopathology in a rat model of early-life adversity
Daskalakis, N. P., Oitzl, M. S., Schächinger, H., Champagne, D. L., & de Kloet, E. R. (2012) · Physiology & Behavior · doi:10.1016/j.physbeh.2012.01.015 · Cited by 76 · see citing works
Repeated Restraint Stress Alters Hippocampal Glutamate Uptake and Release in the Rat
Fontella, F. U., Vendite, D., Tabajara, Â. S., Porciúncula, L. O., Torres, I. L. D. S., Jardim, F. M. A., Martini, L., Souza, D. O., Netto, C. A., & Dalmaz, C. (2004) · Neurochemical Research · doi:10.1023/b:nere.0000035805.46592.6c · Cited by 74 · see citing works
Maternal discrimination of pup sex in rats
Richmond, G., & Sachs, B. D. (1984) · Developmental Psychobiology · doi:10.1002/dev.420170108 · Cited by 72 · see citing works
Pituitary glucocorticoid receptor deletion reduces vulnerability to chronic stress
Wagner, K. V., Wang, X., Liebl, C., Scharf, S. H., Müller, M. B., & Schmidt, M. V. (2010) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2010.09.007 · Cited by 69 · see citing works
Sensitive, stimulating caregiving predicts cognitive and behavioral resilience in neurodevelopmentally at-risk infants
Jaffee, S. R. (2007) · Development and Psychopathology · doi:10.1017/s0954579407000326 · Cited by 66 · see citing works
Early Environmental Regulation of Glucocorticoid Feedback Sensitivity in Young Adult Monkeys
Lyons, D. M., Yang, C., Mobley, B. W., Nickerson, J., & Schatzberg, A. F. (2000) · Journal of Neuroendocrinology · doi:10.1046/j.1365-2826.2000.00505.x · Cited by 64 · see citing works
Early handling effects on neophobia and conditioned taste aversion
Weinberg, J., Smotherman, W. P., & Levine, S. (1978) · Physiology & Behavior · doi:10.1016/0031-9384(78)90251-2 · Cited by 64 · see citing works
CRH Signaling
Refojo, D., & Holsboer, F. (2009) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2009.04983.x · Cited by 64 · see citing works
Effects of chronic unpredictable stress and methamphetamine on hippocampal glutamate function
Raudensky, J., & Yamamoto, B. K. (2007) · Brain Research · doi:10.1016/j.brainres.2006.12.002 · Cited by 63 · see citing works
Molecular Tools and Approaches for Optogenetics
Yuan, M., & Zhang, F. (2012) · Biological Psychiatry · doi:10.1016/j.biopsych.2012.02.019 · Cited by 63 · see citing works
Personality, Coping Style, and Constitutional Neuroimmunology
Zozulya, A. A., Gabaeva, M. V., Sokolov, O. Y., Surkina, I. D., & Кост, Н. В. (2008) · Journal of Immunotoxicology · doi:10.1080/15476910802131444 · Cited by 63 · see citing works
Hypothalamic-Pituitary-Adrenal Axis Activity of Newborn Mice Rapidly Desensitizes to Repeated Maternal Absence but Becomes Highly Responsive to Novelty
Enthoven, L., Oitzl, M. S., Koning, N. R., van der Mark, M. H., & de Kloet, E. R. (2008) · Endocrinology · doi:10.1210/en.2008-0238 · Cited by 60 · see citing works
Biological pathways to adaptability – interactions between genome, epigenome, nervous system and environment for adaptive behavior
Wolf, C., & Linden, D. E. J. (2011) · Genes Brain & Behavior · doi:10.1111/j.1601-183x.2011.00752.x · Cited by 57 · see citing works
Regulation of adult neurogenesis in the hippocampus by stress, acetylcholine and dopamine
Srikumar, B. N., Veena, J., & Rao, B. S. (2011) · Journal of Natural Science Biology and Medicine · doi:10.4103/0976-9668.82312 · Cited by 55 · see citing works
Childhood Sexual Abuse, HPA Axis Regulation, and Mental Health
Hulme, P. A. (2010) · Western Journal of Nursing Research · doi:10.1177/0193945910388949 · Cited by 48 · see citing works
A comparison of activation patterns of cells in selected prefrontal cortical and amygdala areas of rats which are more or less anxious in response to predator exposure or submersion stress
Adamec, R., Toth, M., Haller, J., Halasz, J., & Blundell, J. (2012) · Physiology & Behavior · doi:10.1016/j.physbeh.2011.09.016 · Cited by 37 · see citing works
The Role of Cognitive Appraisal in Adaptation to Traumatic Stress in Adults With Serious Mental Illness: A Critical Review
Sherrer, M. V. (2011) · Trauma Violence & Abuse · doi:10.1177/1524838011404254 · Cited by 34 · see citing works
Activation of a ΔFOSB dependent gene expression pattern in the dorsolateral prefrontal cortex of patients with major depressive disorder
Teyssier, J., Ragot, S., Chauvet‐Gélinier, J., Trojak, B., & Bonin, B. (2011) · Journal of Affective Disorders · doi:10.1016/j.jad.2011.04.021 · Cited by 33 · see citing works
The involvement of epigenetic defects in mental retardation
Franklin, T. B., & Mansuy, I. M. (2011) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2011.04.001 · Cited by 20 · see citing works
Self-citation
Maternal modulation of novelty effects on physical development
Tang, A. C., Yang, Z., Reeb‐Sutherland, B. C., Romeo, R. D., & McEwen, B. S. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1121056109 · Cited by 18 · see citing works
Forebrain glucocorticoid receptor overexpression increases environmental reactivity and produces a stress-induced spatial discrimination deficit
Hebda‐Bauer, E. K., Pletsch, A., Darwish, H., Fentress, H. M., Simmons, T. A., Wei, Q., Watson, S. J., & Akil, H. (2010) · Neuroscience · doi:10.1016/j.neuroscience.2010.05.033 · Cited by 11 · see citing works

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Paternal Stress Exposure Alters Sperm MicroRNA Content and Reprograms Offspring HPA Stress Axis Regulation
Rodgers, A. B., Morgan, C. P., Bronson, S. L., Revello, S., & Bale, T. L. (2013) · The Journal of Neuroscience · doi:10.1523/jneurosci.0914-13.2013 · Cited by 814 · see citing works
The three-hit concept of vulnerability and resilience: toward understanding adaptation to early-life adversity outcome
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
Stress-induced perinatal and transgenerational epigenetic programming of brain development and mental health
Babenko, O., Kovalchuk, I., & Metz, G. A. S. (2015) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2014.11.013 · Cited by 513 · see citing works
The endocannabinoid system in guarding against fear, anxiety and stress
Lutz, B., Marsicano, G., Maldonado, R., & Hillard, C. J. (2015) · Nature reviews. Neuroscience · doi:10.1038/nrn4036 · Cited by 506 · see citing works
Vagal neurocircuitry and its influence on gastric motility
Travagli, R. A., & Anselmi, L. (2016) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/nrgastro.2016.76 · Cited by 323 · see citing works
When pain gets stuck: the evolution of pain chronification and treatment resistance
Borsook, D., Youssef, A. M., Simons, L., Elman, I., & Eccleston, C. (2018) · Pain · doi:10.1097/j.pain.0000000000001401 · Cited by 281 · see citing works
Distinct Ventral Pallidal Neural Populations Mediate Separate Symptoms of Depression
Knowland, D., Lilascharoen, V., Pacia, C. P., Shin, S., Wang, E. H.-J., & Lim, B. K. (2017) · Cell · doi:10.1016/j.cell.2017.06.015 · Cited by 273 · see citing works
An overview of maternal separation effects on behavioural outcomes in mice: evidence from a four-stage methodological systematic review
Tractenberg, S. G., Levandowski, M. L., de Azeredo, L. A., Orso, R., Roithmann, L. G., Hoffmann, E. S., Brenhouse, H., & Grassi-Oliveira, R. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.06.021 · Cited by 267 · see citing works
Role of adult hippocampal neurogenesis in stress resilience
Levone, B. R., Cryan, J. F., & O'Leary, O. F. (2015) · Neurobiology of Stress · doi:10.1016/j.ynstr.2014.11.003 · Cited by 218 · see citing works
An Efficient Chronic Unpredictable Stress Protocol to Induce Stress-Related Responses in C57BL/6 Mice
Monteiro, S., Roque, S., de SÃ¡-CalÃ§ada, D., Sousa, N., Correia-Neves, M., & Cerqueira, J. J. (2015) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2015.00006 · Cited by 216 · see citing works
Epigenetic mechanisms of major depression: Targeting neuronal plasticity
Uchida, S., Yamagata, H., Seki, T., & Watanabe, Y. (2018) · Psychiatry and Clinical Neurosciences · doi:10.1111/pcn.12621 · Cited by 181 · see citing works
Potential of Environmental Enrichment to Prevent Transgenerational Effects of Paternal Trauma
Gapp, K., Bohacek, J., Grossmann, J., Brunner, A. M., Manuella, F., Nanni, P., & Mansuy, I. M. (2016) · Neuropsychopharmacology · doi:10.1038/npp.2016.87 · Cited by 172 · see citing works
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Gut Vagal Afferents Differentially Modulate Innate Anxiety and Learned Fear
Klarer, M., Arnold, M., Günther, L., Winter, C., Langhans, W., & Meyer, U. (2014) · The Journal of Neuroscience · doi:10.1523/jneurosci.0252-14.2014 · Cited by 159 · see citing works
Hippocampal MicroRNA-124 Enhances Chronic Stress Resilience in Mice
Higuchi, F., Uchida, S., Yamagata, H., Abe-Higuchi, N., Hobara, T., Hara, K., Kobayashi, A., Shintaku, T., Itoh, Y., Suzuki, T., et al. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.0319-16.2016 · Cited by 158 · see citing works
Dysfunctional astrocytic and synaptic regulation of hypothalamic glutamatergic transmission in a mouse model of early-life adversity: relevance to neurosteroids and programming of the stress response
Gunn, B. G., Cunningham, L., Cooper, M. A., Corteen, N. L., Seifi, M., Swinny, J. D., Lambert, J. J., & Belelli, D. (2013) · The Journal of Neuroscience · doi:10.1523/jneurosci.1337-13.2013 · Cited by 151 · see citing works
GABAA receptor-acting neurosteroids: a role in the development and regulation of the stress response
Gunn, B. G., Cunningham, L., Mitchell, S. G., Swinny, J. D., Lambert, J. J., & Belelli, D. (2015) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2014.06.001 · Cited by 149 · see citing works
The epigenetic impacts of social stress: how does social adversity become biologically embedded?
Cunliffe, V. T. (2016) · Epigenomics · doi:10.2217/epi-2016-0075 · Cited by 141 · see citing works
Glial Dysfunction in the Mouse Habenula Causes Depressive-Like Behaviors and Sleep Disturbance
Cui, W., Mizukami, H., Yanagisawa, M., Aida, T., Nomura, M., Isomura, Y., Takayanagi, R., Ozawa, K., Tanaka, K., & Aizawa, H. (2014) · The Journal of Neuroscience · doi:10.1523/jneurosci.1465-14.2014 · Cited by 139 · see citing works
Resilience: A psychobiological construct for psychiatric disorders
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Ni, X., Liao, Y., Li, L., Zhang, X., & Wu, Z. (2018) · Journal of Integrative Neuroscience · doi:10.3233/jin-170052 · Cited by 26 · see citing works
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Yang, M., Ding, Q., Zhang, M., Moon, C., & Wang, H. (2020) · Neurobiology of Stress · doi:10.1016/j.ynstr.2020.100237 · Cited by 12 · see citing works

Authors: Franklin, T. B., Saab, B. J., & Mansuy, I. M.
Affiliations: European Molecular Biology Laboratory (IT)
University of Zurich (CH)
Corresponding author: Mansuy, Isabelle M.
ORCID: Franklin, Tamara B.
Saab, Bechara J.
Mansuy, Isabelle M.
Venue: Neuron
Publisher: Elsevier BV
Published: 2012-09
Volume: 75
Issue: 5
Pages: 747-761
ISSN: 0896-6273 (ISSN-L)
DOI: 10.1016/j.neuron.2012.08.016
OpenAlex: W2086379739
Cited by: 500
References: 153
Citations by year: 2026: 19 · 2025: 33 · 2024: 41 · 2023: 37 · 2022: 44 · 2021: 46 · 2020: 34 · 2019: 43 · 2018: 39 · 2017: 39 · 2016: 38 · 2015: 34 · 2014: 32 · 2013: 20
FWCI: 1.79
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (vor, 370 d)
Locations: Neuron (publishedVersion)
PubMed (publishedVersion)
Zurich Open Repository and Archive (University of Zurich) (submittedVersion)
INFM-OAR (INFN Catania) (submittedVersion, other-oa)
Topics: Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
Social Sciences › Psychology › Clinical Psychology › Resilience and Mental Health
Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Keywords: stress resilience, stress vulnerability, neuroendocrine system, hippocampus, cortical circuits, reward systems, epigenetics, neurogenesis, stress-related disorders, individual differences in stress response, brain connectivity
MeSH terms: Adaptation, Psychological, Animals, Brain Diseases, Humans, Hypothalamo-Hypophyseal System, Neural Pathways, Stress, Psychological, Neurotransmitter Agents, Genetic Predisposition to Disease

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Neural Mechanisms of Stress Resilience and Vulnerability

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