Developmental Timing of the Effects of Maternal Care on Gene Expression and Epigenetic Regulation of Hormone Receptor Levels in Female Rats

Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2−ΔΔCT Method

Livak, K. J., & Schmittgen, T. D. (2001) · Methods · doi:10.1006/meth.2001.1262 · Cited by 180,860 · see citing works

Analyzing real-time PCR data by the comparative CT method

Schmittgen, T. D., & Livak, K. J. (2008) · Nature Protocols · doi:10.1038/nprot.2008.73 · Cited by 26,190 · 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

The oxytocin receptor system: structure, function, and regulation

Gimpl, G., & Fahrenholz, F. (2001) · Physiological Reviews · doi:10.1152/physrev.2001.81.2.629 · Cited by 3,089 · see citing works

Active Genes Are Tri-Methylated at K4 of Histone H3

Santos-Rosa, H., Schneider, R., Bannister, A. J., Sherriff, J., Bernstein, B. E., Emre, N. C. T., Schreiber, S. L., Mellor, J., & Kouzarides, T. (2002) · Nature · doi:10.1038/nature01080 · Cited by 2,138 · see citing works

The diverse functions of histone lysine methylation

Martin, C., & Zhang, Y. (2005) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm1761 · Cited by 2,066 · 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

Comparing protein abundance and mRNA expression levels on a genomic scale

Greenbaum, D. (2003) · Genome biology · doi:10.1186/gb-2003-4-9-117 · Cited by 1,692 · see citing works

The neurobiology of pair bonding.

Young, L. J., & Wang, Z. (2004) · Nature Neuroscience · doi:10.1038/nn1327 · Cited by 1,523 · see citing works

Postpartum depression effects on early interactions, parenting, and safety practices: a review

Field, T. (2010) · Infant Behavior and Development · doi:10.1016/j.infbeh.2009.10.005 · Cited by 1,493 · see citing works

Maternal care, hippocampal synaptogenesis and cognitive development in rats

Liu, D., Diorio, J., Day, J. C., Francis, D. D., & Meaney, M. J. (2000) · Nature Neuroscience · doi:10.1038/77702 · Cited by 1,195 · see citing works

Variations in maternal care in the rat as a mediating influence for the effects of environment on development

Champagne, F. A., Francis, D. D., Mar, A., & Meaney, M. J. (2003) · Physiology & Behavior · doi:10.1016/s0031-9384(03)00149-5 · Cited by 1,021 · see citing works

Discordant Protein and mRNA Expression in Lung Adenocarcinomas

Chen, G., Gharib, T. G., Huang, C.-C., Taylor, J. M. G., Misek, D. E., Kardia, S. L. R., Giordano, T. J., Iannettoni, M. D., Orringer, M. B., Hanash, S., et al. (2002) · Molecular & Cellular Proteomics · doi:10.1074/mcp.m200008-mcp200 · Cited by 946 · 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

Central role of Drosophila SU(VAR)3–9 in histone H3‐K9 methylation and heterochromatic gene silencing

Schotta, G., Ebert, A., Krauss, V., Fischer, A., Hoffmann, J., Rea, S., Jenuwein, T., Dorn, R., & Reuter, G. (2002) · The EMBO Journal · doi:10.1093/emboj/21.5.1121 · Cited by 714 · see citing works

Naturally occurring variations in maternal behavior in the rat are associated with differences in estrogen-inducible central oxytocin receptors

Champagne, F., Diorio, J., Sharma, S., & Meaney, M. J. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.221224598 · Cited by 707 · see citing works

The Neurobiology of Parental Behavior

(2003) · Hormones, Brain, and Behavior · doi:10.1007/b97533 · Cited by 684 · see citing works

Maternal Care Associated with Methylation of the Estrogen Receptor-α1b Promoter and Estrogen Receptor-α Expression in the Medial Preoptic Area of Female Offspring

Champagne, F. A., Weaver, I. C. G., Diorio, J., Dymov, S., Szyf, M., & Meaney, M. J. (2006) · Endocrinology · doi:10.1210/en.2005-1119 · Cited by 675 · see citing works

Interventions to prevent child maltreatment and associated impairment

MacMillan, H. L., Wathen, C. N., Barlow, J., Fergusson, D. M., Leventhal, J. M., & Taussig, H. N. (2009) · The Lancet · doi:10.1016/s0140-6736(08)61708-0 · Cited by 654 · see citing works

Developmental catch-up, and deficit, following adoption after severe global early privation. English and Romanian Adoptees (ERA) Study Team.

Rutter, M. L. (1998) · PubMed · Cited by 653 · see citing works

Developmental catch-up, and deficit, following adoption after severe global early privation

Rutter, M. (1998) · Journal of Child Psychology and Psychiatry · doi:10.1017/s0021963098002236 · Cited by 640 · see citing works

Sex-specific epigenetic disruption and behavioral changes following low-dose in utero bisphenol A exposure

Kundakovic, M., Gudsnuk, K., Franks, B., Madrid, J., Miller, R. L., Perera, F. P., & Champagne, F. A. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1214056110 · Cited by 490 · see citing works

Roles of Estrogen Receptor-α Gene Expression in Reproduction-Related Behaviors in Female Mice**This work was supported by the Harry Frank Guggenheim Foundation (to S.O.), the University of Missouri-Columbia molecular biology program (to D.B.L.), and NIH Grant HD-05751 (to D.W.P.).

Ogawa, S., Eng, V., Taylor, J. A., Lubahn, D. B., Korach, K. S., & Pfaff, D. W. (1998) · Endocrinology · doi:10.1210/endo.139.12.6357 · Cited by 487 · see citing works

Transgenerational effects of social environment on variations in maternal care and behavioral response to novelty

Champagne, F. A., & Meaney, M. J. (2007) · Behavioral Neuroscience · doi:10.1037/0735-7044.121.6.1353 · Cited by 381 · see citing works

Epigenetic Effects of Prenatal Stress on 11β-Hydroxysteroid Dehydrogenase-2 in the Placenta and Fetal Brain

Peña, C. J., Monk, C. E., & Champagne, F. A. (2012) · PLoS ONE · doi:10.1371/journal.pone.0039791 · Cited by 377 · see citing works

Relationship between Histone H3 Lysine 9 Methylation, Transcription Repression, and Heterochromatin Protein 1 Recruitment

Stewart, M. D., Li, J., & Wong, J. (2005) · Molecular and Cellular Biology · doi:10.1128/mcb.25.7.2525-2538.2005 · Cited by 352 · see citing works

Natural Variations in Maternal Care Are Associated with Estrogen Receptor α Expression and Estrogen Sensitivity in the Medial Preoptic Area

Champagne, F. A., Weaver, I. C. G., Diorio, J. C., Sharma, S., & Meaney, M. J. (2003) · Endocrinology · doi:10.1210/en.2003-0564 · Cited by 295 · see citing works

Maternal behavior in the virgin and lactating rat.

Fleming, A. S., & Rosenblatt, J. S. (1974) · Journal of Comparative and Physiological Psychology · doi:10.1037/h0036414 · Cited by 278 · see citing works

Minireview: Genomic Organization of the Human ERα Gene Promoter Region

Koš, M., Reid, G., Denger, S., & Gannon, F. (2001) · Molecular Endocrinology · doi:10.1210/mend.15.12.0731 · Cited by 267 · see citing works

Hypothalamic Neural Circuits Regulating Maternal Responsiveness Toward Infants

Numan, M. (2006) · Behavioral and Cognitive Neuroscience Reviews · doi:10.1177/1534582306288790 · Cited by 247 · see citing works

The effects of early postnatal handling on hippocampal glucocorticoid receptor concentrations: temporal parameters

Meaney, M. J., & Aitken, D. H. (1985) · Developmental Brain Research · doi:10.1016/0165-3806(85)90183-x · Cited by 234 · see citing works

RNAi-mediated silencing of estrogen receptor α in the ventromedial nucleus of hypothalamus abolishes female sexual behaviors

Musatov, S. A., Chen, W. W., Pfaff, D. W., Kaplitt, M. G., & Ogawa, S. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0603045103 · Cited by 223 · see citing works

Effect of Maternal Depression on Child Behavior: A Sensitive Period?

Bagner, D. M., Pettit, J. W., Lewinsohn, P. M., & Seeley, J. R. (2010) · Journal of the American Academy of Child & Adolescent Psychiatry · doi:10.1016/j.jaac.2010.03.012 · Cited by 215 · see citing works

Hormonal regulation of brain circuits mediating male sexual behavior in birds.

Ball, G., & Balthazart, J. (2004) · Physiology and Behavior · doi:10.1016/j.physbeh.2004.08.020 · Cited by 203 · see citing works

Estrogen receptor α is essential for induction of oxytocin receptor by estrogen

Young, L. J., Wang, Z., Donaldson, R., & Rissman, E. F. (1998) · Neuroreport · doi:10.1097/00001756-199803300-00031 · Cited by 198 · see citing works

Developmental and hormone-induced epigenetic changes to estrogen and progesterone receptor genes in brain are dynamic across the life span

Schwarz, J. M., Nugent, B. M., & McCarthy, M. M. (2010) · Endocrinology · doi:10.1210/en.2010-0142 · Cited by 198 · see citing works

Functional Magnetic Resonance Imaging Shows Oxytocin Activates Brain Regions Associated with Mother–Pup Bonding during Suckling

Febo, M., Numan, M., & Ferris, C. F. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.3604-05.2005 · Cited by 197 · see citing works

Oxytocin induction of short-latency maternal behavior in nulliparous, estrogen-primed female rats

FAHRBACH, S. (1984) · Hormones and Behavior · doi:10.1016/0018-506x(84)90016-3 · Cited by 187 · see citing works

Hippocampal epigenetic modification at the brain‐derived neurotrophic factor gene induced by an enriched environment

Kuzumaki, N., Ikegami, D., Tamura, R., Hareyama, N., Imai, S., Narita, M., Torigoe, K., Niikura, K., Takeshima, H., Ando, T., et al. (2010) · Hippocampus · doi:10.1002/hipo.20775 · Cited by 185 · see citing works

Sex Differences in Epigenetic Regulation of the Estrogen Receptor-α Promoter within the Developing Preoptic Area

Kurian, J. R., Olesen, K. M., & Auger, A. P. (2010) · Endocrinology · doi:10.1210/en.2009-0649 · Cited by 185 · see citing works

Prolactin (PRL) Regulation of Maternal Behavior in Rats: Bromocriptine Treatment Delays and PRL Promotes the Rapid Onset of Behavior*

Bridges, R. S., & Ronsheim, P. M. (1990) · Endocrinology · doi:10.1210/endo-126-2-837 · Cited by 180 · see citing works

Maternal Programming of Sexual Behavior and Hypothalamic-Pituitary-Gonadal Function in the Female Rat

Cameron, N. M., Corpo, A. D., Diorio, J. C., McAllister, K., Sharma, S., & Meaney, M. J. (2008) · PLoS ONE · doi:10.1371/journal.pone.0002210 · Cited by 155 · see citing works

Termination of the hormone-sensitive period for differentiation of the sexually dimorphic nucleus of the preoptic area in male and female rats

Rhees, R. W., Shryne, J. E., & Gorski, R. A. (1990) · Developmental Brain Research · doi:10.1016/0165-3806(90)90217-m · Cited by 144 · see citing works

Onset of the hormone‐sensitive perinatal period for sexual differentiation of the sexually dimorphic nucleus of the preoptic area in female rats

Rhees, R. W., Shryne, J. E., & Gorski, R. A. (1990) · Journal of Neurobiology · doi:10.1002/neu.480210511 · Cited by 127 · see citing works

Effect of preoptic region implants of dilute estradiol on the maternal behavior of ovariectomized, nulliparous rats

Fahrbach, S. E., & Pfaff, D. W. (1986) · Hormones and Behavior · doi:10.1016/0018-506x(86)90043-7 · Cited by 124 · see citing works

Changes in licking behaviour of rat mother following handling of young

Lee, M. H. S., & Williams, D. I. (1974) · Animal Behaviour · doi:10.1016/s0003-3472(74)80016-3 · Cited by 121 · see citing works

Critical Period for Effects of Infantile Experience on Maturation of Stress Response

Levine, S., & Lewis, G. W. (1959) · Science · doi:10.1126/science.129.3340.42 · Cited by 119 · see citing works

Adoption and the effect on children’s development

Johnson, D. E. (2002) · Early Human Development · doi:10.1016/s0378-3782(02)00017-8 · Cited by 118 · see citing works

Cloning, Novel Promoter Sequence, and Estrogen Regulation of a Rat Oxytocin Receptor Gene

Bale, T. L., & Dorsa, D. M. (1997) · Endocrinology · doi:10.1210/endo.138.3.4998 · Cited by 118 · see citing works

siRNA silencing of estrogen receptor-α expression specifically in medial preoptic area neurons abolishes maternal care in female mice

Ribeiro, A. C. D. M., Musatov, S. A., Shteyler, A., Simanduyev, S., Arrieta‐Cruz, I., Ogawa, S., & Pfaff, D. W. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1214094109 · Cited by 107 · see citing works

Developmental profile of estrogen receptor mRNA in the preoptic area of male and female neonatal rats

DonCarlos, L. L., & Handa, R. J. (1994) · Developmental Brain Research · doi:10.1016/0165-3806(94)90133-3 · Cited by 102 · see citing works

Variation in maternal and anxiety-like behavior associated with discrete patterns of oxytocin and vasopressin 1a receptor density in the lateral septum

Curley, J. P., Jensen, C. L., Franks, B., & Champagne, F. A. (2012) · Hormones and Behavior · doi:10.1016/j.yhbeh.2012.01.013 · Cited by 90 · see citing works

Dopaminergic activation of estrogen receptors in neonatal brain alters progestin receptor expression and juvenile social play behavior.

Olesen, K. M., Jessen, H. M., Auger, C. J., & Auger, A. P. (2005) · Endocrinology · doi:10.1210/en.2005-0498 · Cited by 89 · see citing works

The medial preoptic area, necessary for adult maternal behavior in rats, is only partially established as a component of the neural circuit that supports maternal behavior in juvenile rats.

Kalinichev, M., Rosenblatt, J. S., & Morrell, J. I. (2000) · Behavioral Neuroscience · doi:10.1037//0735-7044.114.1.196 · Cited by 85 · see citing works

Cellular mechanisms of estradiol-mediated masculinization of the brain

Schwarz, J. M., & McCarthy, M. M. (2008) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/j.jsbmb.2008.03.012 · Cited by 85 · see citing works

The role of the estrogen receptor α in the medial preoptic area in sexual incentive motivation, proceptivity and receptivity, anxiety, and wheel running in female rats.

Spiteri, T., Ogawa, S., Musatov, S., Pfaff, D., & Ågmo, A. (2012) · Behavioural Brain Research · doi:10.1016/j.bbr.2012.01.048 · Cited by 83 · see citing works

The Adoption of Children from Public Care: A Prospective Study of Outcome in Adolescence

Rushton, A., & Dance, C. (2006) · Journal of the American Academy of Child & Adolescent Psychiatry · doi:10.1097/01.chi.0000220850.86768.e8 · Cited by 77 · see citing works

Minireview: Genomic Organization of the Human ER Gene Promoter Region

Koš, M. (2001) · Molecular Endocrinology · doi:10.1210/me.15.12.2057 · Cited by 75 · see citing works

Regional and cellular distribution of serotonin 5-hydroxytryptamine2a receptor mRNA in the nucleus accumbens, olfactory tubercle, and caudate putamen of the rat

Mijnster, M. J., Raimundo, A. G. V., Koskuba, K., Klop, H., Docter, G. J., Groenewegen, H. J., & Voorn, P. (1997) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19971208)389:1 · Cited by 59 · see citing works

The medial preoptic area, necessary for adult maternal behavior in rats, is only partially established as a component of the neural circuit that supports maternal behavior in juvenile rats.

Kalinichev, M., Rosenblatt, J. S., & Morrell, J. I. (2000) · Behavioral Neuroscience · doi:10.1037/0735-7044.114.1.196 · Cited by 59 · see citing works

Hormonal priming and triggering of maternal behavior in the rat with special reference to the relations between estrogen receptor binding and ER mRNA in specific brain regions

Rosenblatt, J. S., Wagner, C. K., & Morrell, J. I. (1994) · Psychoneuroendocrinology · doi:10.1016/0306-4530(94)90039-6 · Cited by 55 · see citing works

Implications of temporal variation in maternal care for the prediction of neurobiological and behavioral outcomes in offspring.

Jensen Peña, C., & Champagne, F. A. (2013) · Behavioral Neuroscience · doi:10.1037/a0031219 · Cited by 54 · see citing works

The 5′ flank of the rat estrogen receptor gene: structural characterization and evidence for tissue- and species-specific promoter utilization

Freyschuss, B., & Grandien, K. (1996) · Journal of Molecular Endocrinology · doi:10.1677/jme.0.0170197 · Cited by 31 · see citing works

Neonatal isolation decreases cued fear conditioning and frontal cortical histone 3 lysine 9 methylation in adult female rats

Kao, G.-S., Cheng, L.-Y., Chen, L.-H., Tzeng, W.-Y., Cherng, C. G., Su, C.-C., Wang, C.-Y., & Yu, L. (2012) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2012.09.040 · Cited by 28 · see citing works

The role of the androgen receptor in anabolic androgenic steroid-induced aggressive behavior in C57BL/6J and Tfm mice

Robinson, S., Penatti, C. A. A., & Clark, A. S. (2011) · Hormones and Behavior · doi:10.1016/j.yhbeh.2011.10.004 · Cited by 25 · see citing works

Dopaminergic activation of estrogen receptors induces fos expression within restricted regions of the neonatal female rat brain

Olesen, K. M., & Auger, A. P. (2008) · PLoS ONE · doi:10.1371/journal.pone.0002177 · Cited by 18 · see citing works

Pubertal Development of Estrogen Receptors in the Rat Brain

Brown, T. J., Hochberg, R. B., Naftolin, F. N., & MacLusky, N. J. (1994) · Molecular and Cellular Neuroscience · doi:10.1006/mcne.1994.1058 · Cited by 16 · see citing works

Measuring Variations in Maternal Behavior: Relevance for Studies of Mood and Anxiety

Franks, B., Curley, J. P., & Champagne, F. A. (2011) · Neuromethods · doi:10.1007/978-1-61779-313-4_13 · Cited by 15 · see citing works

Early life stress confers lifelong stress susceptibility in mice via ventral tegmental area OTX2

Peña, C. J., Kronman, H. G., Walker, D. M., Cates, H. M., Bagot, R. C., Purushothaman, I., Issler, O., Loh, Y.-H. E., Leong, T., Kiraly, D. D., et al. (2017) · Science · doi:10.1126/science.aan4491 · Cited by 394 · see citing works

Growing a social brain

Atzil, S., Gao, W., Fradkin, I., & Barrett, L. F. (2018) · Nature Human Behaviour · doi:10.1038/s41562-018-0384-6 · Cited by 415 · see citing works

The recent progress in animal models of depression

Wang, Q., Timberlake, M. A., Prall, K., & Dwivedi, Y. (2017) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2017.04.008 · Cited by 370 · 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

Epigenetic basis of mental illness

Nestler, E. J., Peña, C. J., Kundakovic, M., Mitchell, A., & Akbarian, S. (2016) · The Neuroscientist · doi:10.1177/1073858415608147 · Cited by 342 · see citing works

Neuroendocrine regulation of maternal behavior

Bridges, R. S. (2015) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2014.11.007 · Cited by 346 · see citing works

Sensitive periods for the effect of childhood adversity on DNA methylation: results from a prospective, longitudinal study

Dunn, E. C., Soare, T. W., Zhu, Y., Simpkin, A. J., Suderman, M. J., Klengel, T., Smith, A. D. A. C., Ressler, K. J., & Relton, C. L. (2019) · Biological Psychiatry · doi:10.1016/j.biopsych.2018.12.023 · Cited by 315 · see citing works

Early-life experience, epigenetics, and the developing brain

Kundakovic, M., & Champagne, F. A. (2015) · Neuropsychopharmacology · doi:10.1038/npp.2014.140 · Cited by 304 · see citing works

Epigenetics and depression

Penner-Goeke, S., & Binder, E. B. (2019) · Dialogues in Clinical Neuroscience · doi:10.31887/dcns.2019.21.4/ebinder · Cited by 254 · see citing works

Influence of maternal care on the developing brain: Mechanisms, temporal dynamics and sensitive periods

Curley, J. P., & Champagne, F. A. (2015) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2015.11.001 · Cited by 257 · see citing works

Early life stress alters transcriptomic patterning across reward circuitry in male and female mice

Peña, C. J., Smith, M., Ramakrishnan, A., Cates, H. M., Bagot, R. C., Kronman, H. G., Patel, B., Chang, A. B., Purushothaman, I., Dudley, J., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-13085-6 · Cited by 219 · see citing works

Developmental Perspectives on Oxytocin and Vasopressin

Hammock, E. A. D. (2014) · Neuropsychopharmacology · doi:10.1038/npp.2014.120 · Cited by 177 · see citing works

Epigenetic signaling in psychiatric disorders: stress and depression

Bagot, R. C., Labonté, B., Peña, C. J., & Nestler, E. J. (2014) · Dialogues in Clinical Neuroscience · doi:10.31887/dcns.2014.16.3/rbagot · Cited by 171 · see citing works

Effects of maternal care on the development of midbrain dopamine pathways and reward-directed behavior in female offspring

Peña, C. J., Neugut, Y. D., Calarco, C. A., & Champagne, F. A. (2014) · European Journal of Neuroscience · doi:10.1111/ejn.12479 · Cited by 120 · see citing works

Risk of Depression in the Adolescent and Adult Offspring of Mothers With Perinatal Depression

Tirumalaraju, V., Suchting, R., Evans, J., Goetzl, L. M., Refuerzo, J., Neumann, A., Anand, D., Ravikumar, R., Green, C. E., Cowen, P. J., et al. (2020) · JAMA Network Open · doi:10.1001/jamanetworkopen.2020.8783 · Cited by 120 · see citing works

Mothers, Fathers, and Others: Neural Substrates of Parental Care

Rogers, F. D., & Bales, K. L. (2019) · Trends in Neurosciences · doi:10.1016/j.tins.2019.05.008 · Cited by 116 · see citing works

Hormonal and non-hormonal bases of maternal behavior: The role of experience and epigenetic mechanisms

Stolzenberg, D. S., & Champagne, F. A. (2015) · Hormones and Behavior · doi:10.1016/j.yhbeh.2015.07.005 · Cited by 115 · see citing works

Unraveling the epigenetic landscape of depression: focus on early life stress

Torres‐Berrío, A., Issler, O., Parise, E. M., & Nestler, E. J. (2019) · Dialogues in Clinical Neuroscience · doi:10.31887/dcns.2019.21.4/enestler · Cited by 102 · see citing works

Plasticity of the epigenome during early-life stress

Barnett-Burns, S., Szyszkowicz, J. K., Luheshi, G. N., Lutz, P.-É., & Turecki, G. (2017) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2017.09.033 · Cited by 91 · see citing works

Multi- and Transgenerational Outcomes of an Exposure to a Mixture of Endocrine-Disrupting Chemicals (EDCs) on Puberty and Maternal Behavior in the Female Rat

Rodríguez, D. L., Aylwin, C. F., Delli, V., Sevrin, E., Campanile, M., Martin, M. J., Franssen, D., Gérard, A., Blacher, S., Tirelli, E., et al. (2021) · Environmental Health Perspectives · doi:10.1289/ehp8795 · Cited by 90 · see citing works

Epigenetic legacy of parental experiences: Dynamic and interactive pathways to inheritance

Champagne, F. A. (2016) · Development and Psychopathology · doi:10.1017/s0954579416000808 · Cited by 80 · see citing works

Oxytocin receptor dynamics in the brain across development and species

Vaidyanathan, R., & Hammock, E. A. D. (2016) · Developmental Neurobiology · doi:10.1002/dneu.22403 · Cited by 82 · see citing works

The early care environment and DNA methylome variation in childhood

Garg, E., Chen, L., Nguyen, T. T. T., Pokhvisneva, I., Chen, L. M., Unternaehrer, E., MacIsaac, J. L., McEwen, L. M., Mah, S. M., Gaudreau, H., et al. (2018) · Development and Psychopathology · doi:10.1017/s0954579418000627 · Cited by 82 · see citing works

Cross-generational influences on childhood anxiety disorders: pathways and mechanisms

Lebowitz, E. R., Leckman, J., Silverman, W., & Feldman, R. (2016) · Journal of neural transmission · doi:10.1007/s00702-016-1565-y · Cited by 65 · see citing works

Conquering Racial Disparities in Perinatal Outcomes

Willis, E., McManus, P., Magallanes, N., Johnson, S., & Majnik, A. V. (2014) · Clinics in Perinatology · doi:10.1016/j.clp.2014.08.008 · Cited by 77 · see citing works

Within- and between-litter maternal care alter behavior and gene regulation in female offspring.

Pan, P., Fleming, A. S., Lawson, D. O., Jenkins, J. M., & McGowan, P. O. (2014) · Behavioral Neuroscience · doi:10.1037/bne0000014 · Cited by 72 · see citing works

How stress can influence brain adaptations to motherhood

Kim, P. (2020) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2020.100875 · Cited by 73 · see citing works

The Parental Brain

Numan, M. (2020) · doi:10.1093/oso/9780190848675.001.0001 · Cited by 101 · see citing works

Neuroanatomical and neurochemical basis of parenting: Dynamic coordination of motivational, affective and cognitive processes

Pereira, M., & Ferreira, A. (2015) · Hormones and Behavior · doi:10.1016/j.yhbeh.2015.08.005 · Cited by 68 · see citing works

Cross-fostering: Elucidating the effects of gene×environment interactions on phenotypic development

McCarty, R. C. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.12.025 · Cited by 61 · see citing works

Age-dependent changes in behavioural plasticity: insights from Bayesian models of development

Stamps, J. A., & Krishnan, V. V. (2017) · Animal Behaviour · doi:10.1016/j.anbehav.2017.01.013 · Cited by 63 · see citing works

Early life social stress induced changes in depression and anxiety associated neural pathways which are correlated with impaired maternal care

Murgatroyd, C., Peña, C. J., Podda, G., Nestler, E. J., & Nephew, B. C. (2015) · Neuropeptides · doi:10.1016/j.npep.2015.05.002 · Cited by 61 · see citing works

New opportunities in vasopressin and oxytocin research: a perspective from the amygdala.

Stoop, R., Hegoburu, C., & van den Burg, E. (2015) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-071714-033904 · Cited by 56 · see citing works

Elevation of 11β-hydroxysteroid dehydrogenase type 2 activity in Holocaust survivor offspring: Evidence for an intergenerational effect of maternal trauma exposure

Bierer, L. M., Bader, H. N., Daskalakis, N. P., Lehrner, A. L., Makotkine, I., Seckl, J. R., & Yehuda, R. (2014) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2014.06.001 · Cited by 57 · see citing works

Role of epigenetic factors in the development of mental illness throughout life

Guintivano, J., & Kaminsky, Z. A. (2014) · Neuroscience Research · doi:10.1016/j.neures.2014.08.003 · Cited by 54 · see citing works

Effects of Diesel Engine Exhaust Origin Secondary Organic Aerosols on Novel Object Recognition Ability and Maternal Behavior in BALB/C Mice

Win‐Shwe, T., Fujitani, Y., Kyi‐Tha‐Thu, C., Furuyama, A., Michikawa, T., Tsukahara, S., Nitta, H., & Hirano, S. (2014) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph111111286 · Cited by 51 · see citing works

Early life stress dampens stress responsiveness in adolescence: Evaluation of neuroendocrine reactivity and coping behavior

Hsiao, Y.-M., Tsai, T.-C., Lin, Y.-T., Chen, C., Huang, C., & Hsu, K. (2016) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2016.02.004 · Cited by 42 · see citing works

Effect of Early Life Stress on the Epigenetic Profiles in Depression

Li, M., Fu, X., Xie, W., Guo, W., Li, B., Cui, R., & Yang, W. (2020) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.00867 · Cited by 41 · see citing works

Histone Deacetylase Inhibition Induces Long-Lasting Changes in Maternal Behavior and Gene Expression in Female Mice

Stolzenberg, D. S., Stevens, J. S., & Rissman, E. F. (2014) · Endocrinology · doi:10.1210/en.2013-1946 · Cited by 40 · see citing works

Impact of maternal immune activation on maternal care behavior, offspring emotionality and intergenerational transmission in C3H/He mice

Berger, S., Ronovsky, M., Horvath, O., Berger, A., & Pollak, D. D. (2018) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2018.02.008 · Cited by 40 · see citing works

The role of maternal care in shaping CNS function

Nephew, B. C., & Murgatroyd, C. (2013) · Neuropeptides · doi:10.1016/j.npep.2013.10.013 · Cited by 39 · see citing works

The Epigenetics of Early Life Adversity: Current Limitations and Possible Solutions

Barnett-Burns, S., Almeida, D. M., & Turecki, G. (2018) · Progress in molecular biology and translational science · doi:10.1016/bs.pmbts.2018.01.008 · Cited by 34 · see citing works

Beyond a means of exposure: a new view of the mother in toxicology research

Catanese, M. C., Suvorov, A., & Vandenberg, L. N. (2014) · Toxicology Research · doi:10.1039/c4tx00119b · Cited by 34 · see citing works

Plasticity of the Maternal Brain Across the Lifespan

Champagne, F. A., & Curley, J. P. (2016) · New Directions for Child and Adolescent Development · doi:10.1002/cad.20164 · Cited by 32 · see citing works

Perinatal exposure to low-dose bisphenol A disrupts learning/memory and DNA methylation of estrogen receptor alpha in the hippocampus

Chang, H., Wang, M., Xia, W., Chen, T., Huo, W., Mao, Z., Zhu, Y., Li, Y., & Xu, S. (2016) · Toxicology Research · doi:10.1039/c5tx00449g · Cited by 31 · see citing works

The Cambridge Handbook of Infant Development

Lockman, J. J., Hertz, D., Tamis-LeMonda, C. S., Brain, B. C., Context..........................................., Rey, J., Falck-Ytter, T., Jones, E., Maurer, D., Cirelli, L., et al. (2020) · Cambridge University Press eBooks · doi:10.1017/9781108351959 · Cited by 30 · see citing works

Epigenetics: Where Environment, Society and Genetics Meet

Majnik, A. V., & Lane, R. H. (2014) · Epigenomics · doi:10.2217/epi.13.83 · Cited by 28 · see citing works

Neonatal overexpression of estrogen receptor‐α alters midbrain dopamine neuron development and reverses the effects of low maternal care in female offspring

Peña, C. J., & Champagne, F. A. (2014) · Developmental Neurobiology · doi:10.1002/dneu.22206 · Cited by 26 · see citing works

Pharmacological manipulation of DNA methylation normalizes maternal behavior, DNA methylation, and gene expression in dams with a history of maltreatment

Keller, S. M., Doherty, T. S., & Roth, T. L. (2019) · Scientific Reports · doi:10.1038/s41598-019-46539-4 · Cited by 25 · see citing works

Revisiting paternal absence: Female alloparental replacement of fathers recovers partner preference formation in female, but not male prairie voles ( Microtus ochrogaster )

Rogers, F. D., & Bales, K. L. (2019) · Developmental Psychobiology · doi:10.1002/dev.21943 · Cited by 25 · see citing works

Hormone-epigenome interactions in behavioural regulation

Baumbach, J. L., & Zovkic, I. B. (2020) · Hormones and Behavior · doi:10.1016/j.yhbeh.2020.104680 · Cited by 24 · see citing works

The brain oxytocin and corticotropin-releasing factor systems in grieving mothers: What we know and what we need to learn

Demarchi, L., Pawluski, J. L., & Bosch, O. J. (2021) · Peptides · doi:10.1016/j.peptides.2021.170593 · Cited by 24 · see citing works

Epigenetic changes in the estrogen receptor α gene promoter: implications in sociosexual behaviors

Matsuda, K. (2014) · Frontiers in Neuroscience · doi:10.3389/fnins.2014.00344 · Cited by 25 · see citing works

Epigenetic mechanisms in alcohol- and adversity-induced developmental origins of neurobehavioral functioning

Boschen, K. E., Keller, S. M., Roth, T. L., & Klintsova, A. Y. (2018) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2017.12.009 · Cited by 24 · see citing works

The Development of Multisensory Attention Skills

Bahrick, L. E., Lickliter, R., & Todd, J. T. T. (2020) · Cambridge University Press eBooks · doi:10.1017/9781108351959.011 · Cited by 24 · see citing works

Postnatal maternal care predicts divergent weaning strategies and the development of social behavior

Franks, B., Champagne, F. A., & Curley, J. P. (2015) · Developmental Psychobiology · doi:10.1002/dev.21326 · Cited by 22 · see citing works

Intergenerational transmission of maternal care deficiency and offspring development delay induced by perinatal protein malnutrition

Gianatiempo, O., Sonzogni, S. V., Fesser, E. A., Belluscio, L. M., Smucler, E., Sued, M., & Cánepa, E. T. (2018) · Nutritional Neuroscience · doi:10.1080/1028415x.2018.1509178 · Cited by 18 · see citing works

Genome-wide methylation analysis reveals differentially methylated loci that are associated with an age-dependent increase in bovine fibroblast response to LPS

Korkmaz, F. T., & Kerr, D. E. (2017) · BMC Genomics · doi:10.1186/s12864-017-3796-1 · Cited by 17 · see citing works

Reproductive experiential regulation of cognitive and emotional resilience

Kinsley, C. H., Bales, K. L., Bardi, M., & Stolzenberg, D. S. (2015) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2015.05.015 · Cited by 17 · see citing works

Postnatal separation prevents the development of prenatal stress‐induced anxiety in association with changes in oestrogen receptor and oxytocin immunoreactivity in female mandarin vole (Microtus mandarinus) offspring

He, F., Wang, Z., & Guo, G. (2017) · European Journal of Neuroscience · doi:10.1111/ejn.13788 · Cited by 17 · see citing works

Early life adversity across different cell- types in the brain

Warhaftig, G., Almeida, D. M., & Turecki, G. (2023) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2023.105113 · Cited by 16 · see citing works

Loss of ERα partially reverses the effects of maternal high-fat diet on energy homeostasis in female mice

Roepke, T. A., Yasrebi, A., Villalobos, A., Krumm, E. A., Yang, J., & Mamounis, K. J. (2017) · Scientific Reports · doi:10.1038/s41598-017-06560-x · Cited by 16 · see citing works

Associations among within-litter differences in early mothering received and later emotional behaviors, mothering, and cortical tryptophan hydroxylase-2 expression in female laboratory rats

Ragan, C. M., Harding, K. M., & Lonstein, J. S. (2015) · Hormones and Behavior · doi:10.1016/j.yhbeh.2015.07.017 · Cited by 16 · see citing works

Infant Emotion Development and Temperament

Aktar, E., & Pérez‐Edgar, K. E. (2020) · Cambridge University Press eBooks · doi:10.1017/9781108351959.026 · Cited by 14 · see citing works

Peritonitis, dialysate infusion and lung function in continuous ambulatory peritoneal dialysis (CAPD).

da Silva, A. M. T., Davis, W. B., Winchester, J. F., Coleman, D., & Weir, C. W. (1985) · PubMed · Cited by 15 · see citing works

Microglia depletion facilitates the display of maternal behavior and alters activation of the maternal brain network in nulliparous female rats

Dye, C. N., Franceschelli, D. V., Leuner, B., & Lenz, K. M. (2023) · Neuropsychopharmacology · doi:10.1038/s41386-023-01624-1 · Cited by 12 · see citing works

Cross-Cultural Perspectives on Parent–Infant Interactions

Bornstein, M. H., & Esposito, G. (2020) · Cambridge University Press eBooks · doi:10.1017/9781108351959.029 · Cited by 11 · see citing works

Social and Behavioral Epigenetics: Evolving Perspectives on Nature-Nurture Interplay, Plasticity, and Inheritance

Champagne, F. A. (2017) · Palgrave Macmillan UK eBooks · doi:10.1057/978-1-137-52879-7_10 · Cited by 11 · see citing works

Impact of a bisphenol A, F, and S mixture and maternal care on the brain transcriptome of rat dams and pups

Lapp, H. E., Margolis, A. E., & Champagne, F. A. (2022) · NeuroToxicology · doi:10.1016/j.neuro.2022.08.014 · Cited by 10 · see citing works

Brain Development in Infants

Richards, J. E., & Conte, S. (2020) · Cambridge University Press eBooks · doi:10.1017/9781108351959.004 · Cited by 9 · see citing works

Shaping the development of complex social behavior

Curley, J. P., & Champagne, F. A. (2023) · Annals of the New York Academy of Sciences · doi:10.1111/nyas.15076 · Cited by 7 · see citing works

Action in Development

Rachwani, J., Hoch, J. E., & Adolph, K. E. (2020) · Cambridge University Press eBooks · doi:10.1017/9781108351959.017 · Cited by 8 · see citing works

Infant Object Manipulation and Play

Tamis‐LeMonda, C. S., & Lockman, J. J. (2020) · Cambridge University Press eBooks · doi:10.1017/9781108351959.019 · Cited by 8 · see citing works

Effects of Prenatal Phthalate Exposure and Childhood Exercise on Maternal Behaviors in Female Rats at Postpartum: A Role of Oxtr Methylation in the Hypothalamus

Lee, Y.-J., Lin, H., Chaudhary, M. A., Lee, Y., & Wang, D. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22189847 · Cited by 8 · see citing works

Nurture outpaces nature: fostering with an attentive mother alters social dominance in a mouse model of stress sensitivity

Sur, D., Agranyoni, O., Kirby, M. L., Cohen, N., Bagaev, A., Karandasheva, K., Shmerkin, E., Gorobets, D., Savita, B. K., Avneri, R., et al. (2023) · Molecular Psychiatry · doi:10.1038/s41380-023-02273-y · Cited by 7 · see citing works

Conception and Development of the Warmth/Affection Coding System (WACS): A Novel Hybrid Behavioral Observational Tool for Assessing Parent-to-Child Warmth

Prasad, A. H., Keevers, Y., Kaouar, S., & Kimonis, E. R. (2023) · Research on Child and Adolescent Psychopathology · doi:10.1007/s10802-023-01055-y · Cited by 7 · see citing works

Inter‐individual maternal care received and genotype interactions affect dopaminergic phenotypes in female rat offspring

Lauby, S. C., Chatterjee, D., Pan, P., McGowan, P. O., & Fleming, A. S. (2019) · Journal of Neuroendocrinology · doi:10.1111/jne.12706 · Cited by 7 · see citing works

Infant Vocal Learning and Speech Production

Warlaumont, A. S. (2020) · Cambridge University Press eBooks · doi:10.1017/9781108351959.022 · Cited by 7 · see citing works

The Development of Infant Feeding

Mennella, J. A., Forestell, C. A., Ventura, A. K., & Fisher, J. O. (2020) · Cambridge University Press eBooks · doi:10.1017/9781108351959.010 · Cited by 7 · see citing works

Epigenetic transmission of maternal behavior: Impact on the neurobiological system of healthy mothers

Elmadih, A., & Abumadini, M. S. (2018) · Saudi Journal of Medicine and Medical Sciences · doi:10.4103/sjmms.sjmms_163_17 · Cited by 6 · see citing works

Infant Attachment (to Mother and Father) and Its Place in Human Development

Dagan, O., & Sagi‐Schwartz, A. (2020) · Cambridge University Press eBooks · doi:10.1017/9781108351959.025 · Cited by 6 · see citing works

Understanding and Evaluating the Moral World in Infancy

Hamlin, J. K., & Sitch, M. J. (2020) · Cambridge University Press eBooks · doi:10.1017/9781108351959.028 · Cited by 5 · see citing works

Neonatal Anoxia Impacts Rats’ Maternal Behavior and Offspring Development due to Ultrasonic Vocalization’s Impairment

Helou, A. Y., Cruz-Ochoa, N. A., Felício, L. F., & Nogueira, M. I. (2022) · Developmental Neuroscience · doi:10.1159/000526810 · Cited by 5 · see citing works

Delivering Clinically on Our Knowledge of Oxytocin and Sensory Stimulation: The Potential of Infant Carrying in Primary Prevention

Norholt, H. (2021) · Frontiers in Psychology · doi:10.3389/fpsyg.2020.590051 · Cited by 4 · see citing works

Ghosts of mother's past: Previous maternal stress leads to altered maternal behavior following a subsequent pregnancy in rats

Kan, J. M., & Richardson, R. (2018) · Developmental Psychobiology · doi:10.1002/dev.21609 · Cited by 4 · see citing works

Transgenerational Epigenetics

Curley, J. P., Rahia Mashoodh, A., & Champagne, F. A. (2017) · Elsevier eBooks · doi:10.1016/b978-0-12-805388-1.00024-9 · Cited by 4 · see citing works

Infant Emotional Development

Mitsven, S. G., Messinger, D. S., Moffitt, J., & Ahn, Y. A. (2020) · Cambridge University Press eBooks · doi:10.1017/9781108351959.027 · Cited by 6 · see citing works

Social Interactions and Indirect Genetic Effects on Complex Juvenile and Adult Traits

Ashbrook, D. G., & Hager, R. (2016) · Methods in molecular biology · doi:10.1007/978-1-4939-6427-7_24 · Cited by 4 · see citing works

Maternal care‐related differences in males and females rats’ sensitivity to ethanol and the associations between the GABAergic system and steroids in males

Popoola, D. O., & Cameron, N. M. (2018) · Developmental Psychobiology · doi:10.1002/dev.21607 · Cited by 4 · see citing works

Transgenerational Epigenetics

Curley, J. P., Rahia Mashoodh, A., & Champagne, F. A. (2022) · Elsevier eBooks · doi:10.1016/b978-0-323-91909-8.00023-2 · Cited by 4 · see citing works

Epigenetic Mechanisms Linking Prenatal Maternal Stress to Developmental Outcomes in Infants and Children

Champagne, F. A., Dosanjh, L. H., & Firestein, M. R. (2024) · Springer eBooks · doi:10.1007/978-3-031-48627-2_9 · Cited by 3 · see citing works

The Infant’s Visual World

Jayaraman, S., & Smith, L. B. (2020) · Cambridge University Press eBooks · doi:10.1017/9781108351959.020 · Cited by 2 · see citing works

Visual Development

Maurer, D. M. (2020) · Cambridge University Press eBooks · doi:10.1017/9781108351959.006 · Cited by 3 · see citing works

Epigenetic Advances in Behavioral and Brain Sciences Have Relevance for Public Policy

Roth, T. L. (2017) · Policy Insights from the Behavioral and Brain Sciences · doi:10.1177/2372732217719091 · Cited by 3 · see citing works

Infant Learning in the Digital Age

Rusnak, S. N., & Barr, R. (2020) · Cambridge University Press eBooks · doi:10.1017/9781108351959.016 · Cited by 3 · see citing works

Infant Memory

Hayne, H., & Herbert, J. S. (2020) · Cambridge University Press eBooks · doi:10.1017/9781108351959.012 · Cited by 2 · see citing works

An Analysis of Between-Cow Variation in Innate Immunity in Relation to Mastitis Severity

Korkmaz, F. T. (2018) · ScholarWorks -A service of University of Vermont Libraries (University of Vermont) · Cited by 2 · see citing works

Epigenetics in Health and Disease

Cabej, N. R. (2018) · Elsevier eBooks · doi:10.1016/b978-0-12-814067-3.00014-4 · Cited by 2 · see citing works

Mechanisms by which early-life experiences promote enduring stress resilience or vulnerability

Short, A. K., Bolton, J. L., & Baram, T. Z. (2019) · Elsevier eBooks · doi:10.1016/b978-0-12-813983-7.00012-4 · Cited by 2 · see citing works

Embodied Brain Model for Understanding Functional Neural Development of Fetuses and Infants

Yamada, Y., Kanazawa, H., & Kuniyoshi, Y. (2020) · Cambridge University Press eBooks · doi:10.1017/9781108351959.001 · Cited by 2 · see citing works

Variation in postpartum maternal care programs the development of neuroendocrine and mesolimbic dopamine pathways in female offspring

Peña, C. J. (2013) · doi:10.7916/d8fr03pv

Maternal Care Associated with Methylation of the Estrogen Receptor-α1b Promoter and Estrogen Receptor-α Expression in the Medial Preoptic Area of Female Offspring

Champagne, F. A., Weaver, I. C. G., Diorio, J., Dymov, S., Szyf, M., & Meaney, M. J. (2006) · Endocrinology · doi:10.1210/en.2005-1119 · Cited by 675 · see citing works

Maternal care associated with methylation of the estrogen receptor-alpha1b promoter and estrogen receptor-alpha expression in themedial preoptic area of female offspring

Champagne, F. A., Weaver, I. C. G., Diorio, J. C., Dymov, S., Moshe Szyf, A., & Meaney, M. J. (2006)

doi: 10.1210/en.2003-0564 Natural Variations in Maternal Care Are Associated with Estrogen Receptor � Expression and Estrogen Sensitivity in the Medial Preoptic Area

Champagne, F. A., Weaver, I. C. G., Diorio, J. C., Sharma, S., & Meaney, M. J. (2013)

Natural Variations in Maternal Care Are Associated with Estrogen Receptor α Expression and Estrogen Sensitivity in the Medial Preoptic Area

Champagne, F. A., Weaver, I. C. G., Diorio, J. C., Sharma, S., & Meaney, M. J. (2003) · Endocrinology · doi:10.1210/en.2003-0564 · Cited by 295 · see citing works