Importance of studying the contributions of early adverse experience to neurobiological findings in depression

Heim, Christine; Plotsky, Paul M; Nemeroff, Charles B

doi:10.1038/sj.npp.1300397

Cited by 514Stress Responses and CortisolChild Abuse and TraumaTreatment of Major Depression

Importance of studying the contributions of early adverse experience to neurobiological findings in depression

Heim, Christine, Plotsky, Paul M, Nemeroff, Charles B·2004·Neuropsychopharmacology

DOI 10.1038/sj.npp.1300397

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Abstract

Almost four decades of intensive research have sought to elucidate the neurobiological bases of depression. Epidemiological studies have revealed that both genetic and environmental factors contribute to the risk for depression. Adverse early-life experiences influence neurobiological systems within genetic limits, leading to the neurobiological and behavioral manifestations of depression. We summarize the burgeoning evidence concerning a pre-eminent role of early adverse experience in the pathogenesis of depression. The available data suggest that (1) early adverse experience contributes to the pathophysiology of depression, (2) there are neurobiologically different subtypes of depression depending on the presence or absence of early adverse experience, likely having confounded previous research on the neurobiology of depression, and (3) early adverse experience likely influences treatment response in depression. Classification of depression based on developmental and neurobiological features will likely considerably improve future research in the field of depression, and might lead to optimized treatment strategies that directly target different neurobiological pathways to depression.

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Some well-established neurobiological correlates of depression might result from unrecognized early physical or sexual abuse.
“As such, many of the established neurobiological findings in depression may be due to the undetected presence of early physical or sexual abuse (Heim et al., 2004).”
From The Differential Impacts of Early Physical and Sexual Abuse and Internalizing Problems on Daytime Cortisol Rhythm in School-Aged Children (2010) · cites this paper as Heim et al., 2004

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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
Psychosocial predictors of the short-term course and outcome of major depression: A longitudinal study of a nonclinical sample with recent-onset episodes.
Lara, M. E., Klein, D. N., & Kasch, K. L. (2000) · Journal of Abnormal Psychology · doi:10.1037//0021-843x.109.4.644 · Cited by 64 · see citing works
Biology of schizophrenia and affective disease
Alarcón, R. D. (1997) · Depression and Anxiety · doi:10.1002/(sici)1520-6394(1997)5:2 · Cited by 59 · see citing works
Neurobiology of Early-Life Stress
Heim, C. C., Meinlschmidt, G., & Nemeroff, C. B. (2003) · Psychiatric Annals · doi:10.3928/0048-5713-20030101-05 · Cited by 58 · see citing works
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Postnatal Experiences and Genetic Effects on Squirrel Monkey Social Affinities and Emotional Distress
Lyons, D. M., Martel, F. L., Levine, S. D., RISCH, N. J., & Schatzberg, A. F. (1999) · Hormones and Behavior · doi:10.1006/hbeh.1999.1547 · Cited by 50 · see citing works
Psychosocial predictors of the short-term course and outcome of major depression: A longitudinal study of a nonclinical sample with recent-onset episodes.
Lara, M. E., Klein, D. N., & Kasch, K. L. (2000) · Journal of Abnormal Psychology · doi:10.1037/0021-843x.109.4.644 · Cited by 48 · see citing works
Cerebrospinal Fluid Corticotropin-Releasing Factor (CRF) and Vasopressin Concentrations Predict Pituitary Response in the CRF Stimulation Test: A Multiple Regression Analysis
Newport, D. J., Heim, C. C., Owens, M. J., Ritchie, J., Ramsey, C. H., Bonsall, R. W., Miller, A. H., & Nemeroff, C. B. (2002) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300071 · Cited by 44 · see citing works
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Depression Sub-Typing: Unitary, Binary or Arbitrary?
Parker, G. B., Hall, W., Boyce, P. M., Hadži-Pavlović, D., Mitchell, P. B., Wilhelm, K. A., Brodaty, H., Hickie, I. B., & Eyers, K. (1991) · Australian & New Zealand Journal of Psychiatry · doi:10.3109/00048679109077720 · Cited by 21 · see citing works

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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
The link between childhood trauma and depression: insights from HPA axis studies in humans
Heim, C., Newport, D. J., Mletzko, T., Miller, A. H., & Nemeroff, C. B. (2008) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2008.03.008 · Cited by 1,704 · see citing works
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Reconsidering anhedonia in depression: Lessons from translational neuroscience
Treadway, M. T., & Zald, D. H. (2011) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2010.06.006 · Cited by 1,579 · see citing works
Gene–environment interactions in psychiatry: joining forces with neuroscience
Caspi, A., & Moffitt, T. E. (2006) · Nature Reviews Neuroscience · doi:10.1038/nrn1925 · Cited by 1,300 · see citing works
Current research trends in early life stress and depression: Review of human studies on sensitive periods, gene–environment interactions, and epigenetics
Heim, C., & Binder, E. B. (2012) · Experimental Neurology · doi:10.1016/j.expneurol.2011.10.032 · Cited by 986 · see citing works
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A Heuristic for Developing Transdiagnostic Models of Psychopathology: Explaining Multifinality and Divergent Trajectories
Nolen-Hoeksema, S., & Watkins, E. R. (2011) · Perspectives on Psychological Science · doi:10.1177/1745691611419672 · Cited by 863 · see citing works
Behavioural and neurochemical effects of post-weaning social isolation in rodents—Relevance to developmental neuropsychiatric disorders
Fone, K. C. F., & Porkess, M. V. (2008) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2008.03.003 · Cited by 864 · see citing works
Child maltreatment and the developing HPA axis
Tarullo, A. R., & Gunnar, M. R. (2006) · Hormones and Behavior · doi:10.1016/j.yhbeh.2006.06.010 · Cited by 737 · see citing works
The brain and the stress axis: the neural correlates of cortisol regulation in response to stress
Dedovic, K., Duchesne, A., Andrews, J., Engert, V., & Pruessner, J. C. (2009) · NeuroImage · doi:10.1016/j.neuroimage.2009.05.074 · Cited by 699 · see citing works
The role of early life stress as a predictor for alcohol and drug dependence
Enoch, M.-A. (2011) · Psychopharmacology · doi:10.1007/s00213-010-1916-6 · Cited by 668 · see citing works
Posttraumatic stress disorder: a state-of-the-science review
Nemeroff, C. B., Bremner, J. D., Foa, E. B., Mayberg, H. S., North, C. S., & Stein, M. B. (2006) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2005.07.005 · Cited by 675 · see citing works
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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
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A Novel Mouse Model for Acute and Long-Lasting Consequences of Early Life Stress
Rice, C. J., Sandman, C. A., Lenjavi, M. R., & Baram, T. Z. (2008) · Endocrinology · doi:10.1210/en.2008-0633 · Cited by 521 · see citing works
Long term consequences of neonatal rearing on central corticotropin-releasing factor systems in adult male rat offspring
Plotsky, P. M., Thrivikraman, K. V., Nemeroff, C. B., Caldji, C., Sharma, S., & Meaney, M. J. (2005) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300769 · Cited by 522 · see citing works
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Lower CSF oxytocin concentrations in women with a history of childhood abuse
Heim, C., Young, L. J., Newport, D. J., Mletzko, T., Miller, A. H., & Nemeroff, C. B. (2009) · Molecular Psychiatry · doi:10.1038/mp.2008.112 · Cited by 518 · see citing works
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Depression, Neuroimaging and Connectomics: A Selective Overview
Gong, Q., & Yong He, A. (2014) · Biological Psychiatry · doi:10.1016/j.biopsych.2014.08.009 · Cited by 496 · 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
Mechanisms of late-onset cognitive decline after early-life stress
Brunson, K. L., Kramár, E., Lin, B., Chen, Y., Colgin, L. L., Yanagihara, T. K., Lynch, G., & Baram, T. Z. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.2281-05.2005 · Cited by 479 · see citing works
Neurobiological mechanisms in major depressive disorder
Rot, M. A. H., Mathew, S. J., & Charney, D. S. (2009) · Canadian Medical Association Journal · doi:10.1503/cmaj.080697 · Cited by 473 · see citing works
Life course pathways of adverse childhood experiences toward adult psychological well-being: A stress process analysis
Nurius, P. S., Green, S., Logan-Greene, P., & Borja, S. (2015) · Child Abuse & Neglect · doi:10.1016/j.chiabu.2015.03.008 · Cited by 457 · see citing works
Annual Research Review: All mothers are not created equal: neural and psychobiological perspectives on mothering and the importance of individual differences
Barrett, J., & Fleming, A. S. (2011) · Journal of Child Psychology and Psychiatry · doi:10.1111/j.1469-7610.2010.02306.x · Cited by 433 · see citing works
Antenatal maternal anxiety is related to HPA-axis dysregulation and self-reported depressive symptoms in adolescence: a prospective study on the fetal origins of depressed mood
Van den Bergh, B. R. H., Van Calster, B., Smits, T., Van Huffel, S., & Lagae, L. (2008) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301450 · Cited by 434 · see citing works
Impact of Maternal Stress, Depression and Anxiety on Fetal Neurobehavioral Development
KINSELLA, M. T., & MONK, C. (2009) · Clinical Obstetrics & Gynecology · doi:10.1097/grf.0b013e3181b52df1 · Cited by 422 · see citing works
Dysfunctional nurturing behavior in rat dams with limited access to nesting material: A clinically relevant model for early-life stress
Ivy, A. S., Brunson, K. L., Sandman, C., & Baram, T. Z. (2008) · Neuroscience · doi:10.1016/j.neuroscience.2008.04.019 · Cited by 407 · see citing works
Neurobiology of depression: an integrated view of key findings
Maletic, V., Robinson, M., Oakes, T. M. M., Iyengar, S., Ball, S. G., & Russell, J. D. (2007) · International Journal of Clinical Practice · doi:10.1111/j.1742-1241.2007.01602.x · Cited by 387 · see citing works
Serotonergic vulnerability and depression: assumptions, experimental evidence and implications
Jans, L. A. W., Riedel, W. J., Markus, C. R., & Blokland, A. (2006) · Molecular Psychiatry · doi:10.1038/sj.mp.4001920 · Cited by 372 · see citing works
Diminished cortisol responses to psychosocial stress associated with lifetime adverse events
Elzinga, B. M., Roelofs, K., Tollenaar, M. S., Bakvis, P., van Pelt, J., & Spinhoven, P. (2008) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2007.11.004 · Cited by 364 · see citing works
Moderate versus severe early life stress: Associations with stress reactivity and regulation in 10–12-year-old children
Gunnar, 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
Brain development under stress: Hypotheses of glucocorticoid actions revisited
Oitzl, M. S., Champagne, D. L., van der Veen, R., & de Kloet, E. R. (2009) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2009.07.006 · Cited by 358 · see citing works
The dexamethasone/corticotropin-releasing factor test in men with major depression: role of childhood trauma
Heim, C., Mletzko, T., Purselle, D., Musselman, D. L., & Nemeroff, C. B. (2008) · Biological Psychiatry · doi:10.1016/j.biopsych.2007.07.002 · Cited by 353 · see citing works
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A review of neighborhood effects and early child development: How, where, and for whom, do neighborhoods matter?
Minh, A., Muhajarine, N., Janus, M., Brownell, M. D., & Guhn, M. (2017) · Health & Place · doi:10.1016/j.healthplace.2017.04.012 · Cited by 357 · see citing works
Corticotropin Releasing Factor (CRF) Receptor Signaling in the Central Nervous System: New Molecular Targets
Hauger, R., Risbrough, V. B., Brauns, O., & Dautzenberg, F. M. (2006) · CNS & Neurological Disorders - Drug Targets · doi:10.2174/187152706777950684 · Cited by 341 · see citing works
The Differential Impacts of Early Physical and Sexual Abuse and Internalizing Problems on Daytime Cortisol Rhythm in School-Aged Children
Cicchetti, D., Rogosch, F. A., Gunnar, M. R., & Toth, S. L. (2010) · Child Development · doi:10.1111/j.1467-8624.2009.01393.x · Cited by 337 · see citing works
Bringing basic research on early experience and stress neurobiology to bear on preventive interventions for neglected and maltreated children
Gunnar, M. R., Fisher, P. A., & THE EARLY EXPERIENCE, S. (2006) · Development and Psychopathology · doi:10.1017/s0954579406060330 · Cited by 329 · see citing works
Prenatal Alcohol Exposure: Foetal Programming, the Hypothalamic‐Pituitary‐Adrenal Axis and Sex Differences in Outcome
Weinberg, J., Sliwowska, J. H., Lan, N., & Hellemans, K. G. C. (2008) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2008.01669.x · Cited by 329 · see citing works
Meta-review of depressive subtyping models
Harald, B., & Gordon, P. (2012) · Journal of Affective Disorders · doi:10.1016/j.jad.2011.07.015 · Cited by 328 · see citing works
The journal of developmental processes
Disorders, L., & Milton (2006) · Medical Entomology and Zoology · Cited by 325 · see citing works
Effects of Therapeutic Interventions for Foster Children on Behavioral Problems, Caregiver Attachment, and Stress Regulatory Neural Systems
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
Neuronal plasticity: A link between stress and mood disorders
Calabrese, F., Molteni, R., Racagni, G., & Riva, M. A. (2009) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2009.05.014 · Cited by 299 · see citing works
Protective Effect of CRHR1 Gene Variants on the Development of Adult Depression Following Childhood Maltreatment: Replication and Extension
Polanczyk, G., Caspi, A., Williams, B., Price, T. S., Danese, A., Sugden, K., Uher, R., Poulton, R., & Moffitt, T. E. (2009) · Archives of General Psychiatry · doi:10.1001/archgenpsychiatry.2009.114 · Cited by 285 · see citing works
Interaction of FKBP5, a Stress-Related Gene, with Childhood Trauma Increases the Risk for Attempting Suicide
Roy, A., Gorodetsky, E., Yuan, Q., Goldman, D., & Enoch, M.-A. (2010) · Neuropsychopharmacology · doi:10.1038/npp.2009.236 · Cited by 282 · see citing works
Invited review: Effects of group housing of dairy calves on behavior, cognition, performance, and health
Costa, J. H. C., von Keyserlingk, M. A. G., & Weary, D. M. (2016) · Journal of Dairy Science · doi:10.3168/jds.2015-10144 · Cited by 283 · see citing works
The Development of Persistent Pain and Psychological Morbidity After Motor Vehicle Collision: Integrating the Potential Role of Stress Response Systems Into a Biopsychosocial Model
McLean, S. A., Clauw, D. J., Abelson, J. L., & Liberzon, I. (2005) · Psychosomatic Medicine · doi:10.1097/01.psy.0000181276.49204.bb · Cited by 273 · see citing works
A transdisciplinary perspective of chronic stress in relation to psychopathology throughout life span development
Juster, R.-P., Bizik, G., Picard, M., Arsenault-Lapierre, G., Sindi, S., Trepanier, L., Marin, M.-F., Wan, N., Sekerovic, Z., Lord, C., et al. (2011) · Development and Psychopathology · doi:10.1017/s0954579411000289 · Cited by 268 · see citing works
Interaction of childhood maltreatment with the corticotropin-releasing hormone receptor gene: effects on hypothalamic-pituitary-adrenal axis reactivity
Tyrka, A. R., Price, L. H., Gelernter, J., Schepker, C., Anderson, G. M., & Carpenter, L. L. (2009) · Biological Psychiatry · doi:10.1016/j.biopsych.2009.05.012 · Cited by 264 · see citing works
Interaction of <i>FKBP5</i> Gene Variants and Adverse Life Events in Predicting Depression Onset: Results From a 10-Year Prospective Community Study
Zimmermann, P., Brückl, T., Nocon, A., Pfister, H., Binder, E. B., Uhr, M., Lieb, R., Moffitt, T. E., Caspi, A., Holsboer, F., et al. (2011) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2011.10111577 · Cited by 262 · see citing works
Zebrafish embryos and larvae: A new generation of disease models and drug screens
Ali, S., Champagne, D. L., Spaink, H. P., & Richardson, M. K. (2011) · Birth Defects Research Part C Embryo Today Reviews · doi:10.1002/bdrc.20206 · Cited by 260 · see citing works
Early care experiences and HPA axis regulation in children: a mechanism for later trauma vulnerability
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
Social isolation rearing‐induced impairment of the hippocampal neurogenesis is associated with deficits in spatial memory and emotion‐related behaviors in juvenile mice
Ibi, D., Takuma, K., Koike, H., Mizoguchi, H., Tsuritani, K., Kuwahara, Y., Kamei, H., Nagai, T., Yoneda, Y., Nabeshima, T., et al. (2007) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2007.05207.x · Cited by 242 · see citing works
The Molecular Neurobiology of Depression
Shelton, R. C. (2007) · Psychiatric Clinics of North America · doi:10.1016/j.psc.2006.12.005 · Cited by 242 · see citing works
Overlapping and segregated resting‐state functional connectivity in patients with major depressive disorder with and without childhood neglect
Wang, L., Dai, Z., Peng, H., Tan, L., Ding, Y., He, Z., Zhang, Y., Xia, M., Li, Z., Li, W., et al. (2014) · Human Brain Mapping · doi:10.1002/hbm.22241 · Cited by 236 · 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
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Differential functional connectivity within an emotion regulation neural network among individuals resilient and susceptible to the depressogenic effects of early life stress
Cisler, J. M., James, G. A., Tripathi, S., Mletzko, T., Heim, C., Hu, X. P., Mayberg, H. S., Nemeroff, C. B., & Kilts, C. D. (2013) · Psychological Medicine · doi:10.1017/s0033291712001390 · Cited by 236 · see citing works
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The Neurobiology of Social Distance
Bzdok, D., & Dunbar, R. (2020) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2020.05.016 · Cited by 234 · see citing works
Behavioral abnormality and pharmacologic response in social isolation-reared mice
Koike, H., Ibi, D., Mizoguchi, H., Nagai, T., Nitta, A., Takuma, K., Nabeshima, T., Yoneda, Y., & Yamada, K. (2009) · Behavioural Brain Research · doi:10.1016/j.bbr.2009.03.028 · Cited by 221 · 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
Of sound mind and body: depression, disease, and accelerated aging
Wolkowitz, O. M., Reus, V. I., & Mellon, S. H. (2011) · Dialogues in Clinical Neuroscience · doi:10.31887/dcns.2011.13.1/owolkowitz · Cited by 213 · see citing works
Postnatal stimulation of the pups counteracts prenatal stress-induced deficits in hippocampal neurogenesis
Lemaire, V., Lamarque, S., Le Moal, M., Piazza, P.-V., & Abrous, D. N. (2006) · Biological Psychiatry · doi:10.1016/j.biopsych.2005.11.009 · Cited by 211 · see citing works
Effects of Early and Recent Adverse Experiences on Adrenal Response to Psychosocial Stress in Depressed Adolescents
Rao, U., Hammen, C. L., Ortiz, L. R., Chen, L.-A., & Poland, R. E. (2008) · Biological Psychiatry · doi:10.1016/j.biopsych.2008.05.012 · Cited by 210 · see citing works
Sensitivity to Intranasal Oxytocin in Adult Men with Early Parental Separation
Meinlschmidt, G., & Heim, C. C. (2006) · Biological Psychiatry · doi:10.1016/j.biopsych.2006.09.007 · Cited by 210 · see citing works
Self-citation
Depression: An Evolutionarily Conserved Mechanism to Terminate Separation Distress? A Review of Aminergic, Peptidergic, and Neural Network Perspectives
Watt, D. F., & Panksepp, J. (2009) · Neuropsychoanalysis · doi:10.1080/15294145.2009.10773593 · Cited by 207 · see citing works
Biological Aspects of Social Bonding and the Roots of Human Violence
Pedersen, C. A. (2004) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1330.006 · Cited by 209 · see citing works
Expression and Regulation of the Fkbp5 Gene in the Adult Mouse Brain
Scharf, S. H., Liebl, C., Binder, E. B., Schmidt, M. V., & Müller, M. B. (2011) · PLoS ONE · doi:10.1371/journal.pone.0016883 · Cited by 202 · see citing works
The use of the zebrafish model in stress research
Steenbergen, P. J., Richardson, M. K., & Champagne, D. L. (2010) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2010.10.010 · Cited by 199 · see citing works
Age‐dependent effects of chronic stress on brain plasticity and depressive behavior
Tóth, E., Gersner, R., Wilf‐Yarkoni, A., Raizel, H., Dar, D. E., Richter‐Levin, G., Levit, O., & Zangen, A. (2008) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2008.05642.x · Cited by 195 · see citing works
Therapy Insight: is there an imbalanced response of mineralocorticoid and glucocorticoid receptors in depression?
de Kloet, E. R., DeRijk, R. H., & Meijer, O. C. (2007) · Nature Clinical Practice Endocrinology & Metabolism · doi:10.1038/ncpendmet0403 · Cited by 193 · see citing works
Identifying key features of early stressful experiences that produce stress vulnerability and resilience in primates
Parker, K. J., & Dario Maestripieri, A. (2010) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2010.09.003 · Cited by 192 · 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
Effects of positive and negative childhood experiences on adult family health
Daines, C., Hansen, D., Novilla, M. L. B., & Crandall, A. (2021) · BMC Public Health · doi:10.1186/s12889-021-10732-w · Cited by 189 · see citing works
Momentary relationship between cortisol secretion and symptoms in patients with fibromyalgia
McLean, S. A., Williams, D. A., Harris, R. E., Kop, W. J., Groner, K. H., Ambrose, K., Lyden, A. K., Gracely, R. H., Crofford, L. J., Geisser, M. E., et al. (2005) · Arthritis & Rheumatism · doi:10.1002/art.21372 · Cited by 187 · 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
Interpersonal Stress Regulation and the Development of Anxiety Disorders: An Attachment-Based Developmental Framework
Nolte, T., Guiney, J., Fonagy, P., Mayes, L., & Luyten, P. (2011) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2011.00055 · Cited by 241 · see citing works
Gene–environment interactions predict cortisol responses after acute stress: implications for the etiology of depression
Alexander, N., Kuepper, Y., Schmitz, A., Osinsky, R., Kozyra, E., & Hennig, J. (2009) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2009.03.017 · Cited by 171 · see citing works
Maternal prenatal stress and cortisol reactivity to stressors in human infants
Tollenaar, M. S., Beijers, R., Jansen, J., Riksen‐Walraven, J. M., & de Weerth, C. (2010) · Stress · doi:10.3109/10253890.2010.499485 · Cited by 171 · see citing works
Effects of early life stress on amygdala and striatal development
Fareri, D. S., & Tottenham, N. (2016) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2016.04.005 · Cited by 166 · see citing works
Gene-Environment Interactions in Depression Research
Monroe, S. M., & Reid, M. W. (2008) · Psychological Science · doi:10.1111/j.1467-9280.2008.02181.x · Cited by 167 · see citing works
Sex as a Biological Variable: Who, What, When, Why, and How
Bale, T. L., & Epperson, C. N. (2016) · Neuropsychopharmacology · doi:10.1038/npp.2016.215 · Cited by 165 · see citing works
Juvenile stress induces a predisposition to either anxiety or depressive-like symptoms following stress in adulthood
Tsoory, M., Cohen, H., & Richter‐Levin, G. (2006) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2006.06.007 · Cited by 165 · see citing works
Effects of Environmental Stress and Gender on Associations among Symptoms of Depression and the Serotonin Transporter Gene Linked Polymorphic Region (5-HTTLPR)
Brummett, B. H., Boyle, S. H., Siegler, I. C., Kuhn, C. M., Ashley-Koch, A., Jonassaint, C. R., Züchner, S., Collins, A., & Williams, R. B. (2008) · Behavior Genetics · doi:10.1007/s10519-007-9172-1 · Cited by 201 · see citing works
Parenting begets parenting: A neurobiological perspective on early adversity and the transmission of parenting styles across generations
Lomanowska, A. M., Boivin, M., Hertzman, C., & Fleming, A. S. (2017) · Neuroscience · doi:10.1016/j.neuroscience.2015.09.029 · Cited by 224 · see citing works
Models of Depression
Duman, C. H. (2010) · Vitamins and hormones · doi:10.1016/s0083-6729(10)82001-1 · Cited by 160 · see citing works
Decreased cortisol awakening response after early loss experience
Meinlschmidt, G., & Heim, C. C. (2005) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2005.01.006 · Cited by 160 · see citing works
Self-citation
Negative and positive life events are associated with small but lasting change in neuroticism
Jeronimus, B. F., Ormel, J., Aleman, A., Penninx, B. W. J. H., & Riese, H. (2013) · Psychological Medicine · doi:10.1017/s0033291713000159 · Cited by 161 · see citing works
Translating basic research knowledge on the biological embedding of early-life stress into novel approaches for the developmental programming of lifelong health
Heim, C. M., Entringer, S., & Buss, C. (2019) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2018.12.011 · Cited by 158 · see citing works
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Authors: Heim, C., Plotsky, P. M., & Nemeroff, C. B.
Affiliations: Emory University (US)
Corresponding author: Nemeroff, Charles B
ORCID: Heim, Christine
Nemeroff, Charles B
Venue: Neuropsychopharmacology
Publisher: Springer Science and Business Media LLC
Published: 2004-03-03
Volume: 29
Issue: 4
Pages: 641-648
ISSN: 0893-133X (ISSN-L)
1740-634X
DOI: 10.1038/sj.npp.1300397
OpenAlex: W2329414057
Cited by: 514
References: 88
Citations by year: 2026: 3 · 2025: 4 · 2024: 6 · 2023: 10 · 2022: 7 · 2021: 16 · 2020: 12 · 2019: 16 · 2018: 15 · 2017: 24 · 2016: 31 · 2015: 23 · 2014: 28 · 2013: 32 · 2012: 27
FWCI: 2.56
Type: journal article
Language: en
Open access: closed
Licence: www.springer.com/tdm (tdm)
Locations: Neuropsychopharmacology (publishedVersion)
PubMed (publishedVersion)
Funders: National Alliance for Research on Schizophrenia and Depression
National Institute of Mental Health (R01MH042088, P50MH058922, MH58922, MH42088)
Topics: Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
Social Sciences › Psychology › Clinical Psychology › Child Abuse and Trauma
Health Sciences › Medicine › Pharmacology › Treatment of Major Depression
Keywords: childhood adversity, depression, neurobiology of depression, depression pathogenesis, genetic and environmental risk factors, depression subtypes, treatment response, developmental origins of mental disorders, depression classification
MeSH terms: Animals, Depression, Environment, Humans, Hypothalamo-Hypophyseal System, Life Change Events, Neurobiology, Pituitary-Adrenal System, Stress, Physiological

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