Epigenetic mechanisms and the transgenerational effects of maternal care

Champagne, Frances A.

doi:10.1016/j.yfrne.2008.03.003

Cited by 812Neuroendocrine regulation and behaviorEpigenetics and DNA MethylationGenetic Syndromes and Imprinting

Epigenetic mechanisms and the transgenerational effects of maternal care

Open access

Champagne, Frances A.·2008·Frontiers in Neuroendocrinology

DOI 10.1016/j.yfrne.2008.03.003PMC PMC2682215

Open this paper in CoChat — free account

Abstract

The transmission of traits across generations has typically been attributed to the inheritance by offspring of genomic information from parental generations. However, recent evidence suggests that epigenetic mechanisms are capable of mediating this type of transmission. In the case of maternal care, there is evidence for the behavioral transmission of postpartum behavior from mothers to female offspring. The neuroendocrine and molecular mediators of this transmission have been explored in rats and implicate estrogen-oxytocin interactions and the differential methylation of hypothalamic estrogen receptors. These maternal effects can influence multiple aspects of neurobiology and behavior of offspring and this particular mode of inheritance is dynamic in response to environmental variation. In this review, evidence for the generational transmission of maternal care and the mechanisms underlying this transmission will be discussed as will the implications of this inheritance system for offspring development and for the transmission of environmental information from parents to offspring.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

Integrity signals

Registry

Crossref · 10.1016/j.yfrne.2008.03.003

Cites

149 of 149 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Maternal licking and grooming of rat pups during the postpartum period has been associated with greater OT receptor binding or increased activity in brain areas critical for the development of parenting in mammals, including the medial preoptic area, lateral septum, the paraventricular nucleus of the hypothalamus, and the nucleus accumbens.
“For instance, maternal licking and grooming of rat pups during the postpartum period has been associated with greater OT receptor binding or increased activity in brain areas critical for the development of parenting in mammals, including the medial preoptic area, lateral septum, the paraventricular nucleus of the hypothalamus, and the nucleus accumbens (13–16).”
From Oxytocin and the development of parenting in humans (2010) · cites this paper as [14]
The links between maternal OT and maternal affectionate contact are consistent with studies in animal models that pointed to the involvement of central OT in regulating the degree of "licking-and-grooming" maternal behaviors in female rats.
“The links between maternal OT and maternal affectionate contact are consistent with studies in animal models (13,14,47) that pointed to the involvement of central OT in regulating the degree of “licking-and-grooming” maternal behaviors in female rats.”
From Oxytocin and the development of parenting in humans (2010) · cites this paper as [14]
Research in rodents and other mammals has highlighted the importance of OT (on a background of changing levels of estrogen and progesterone during pregnancy and labor) to facilitate the onset and maintenance of maternal behavior.
“Research in rodents and other mammals has highlighted the importance of OT (on a background of changing levels of estrogen and progesterone during pregnancy and labor) to facilitate the onset and maintenance of maternal behavior (Champagne et al., 2001; Champagne, 2008; Champagne et al., 2003; Insel and Young, 2001; Rosenblatt and Ceus, 1998).”
From Approaching the biology of human parental attachment: Brain imaging, oxytocin and coordinated assessments of mothers and fathers (2014) · cites this paper as Champagne, 2008

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals
Jaenisch, R., & Bird, A. (2003) · Nature Genetics · doi:10.1038/ng1089 · Cited by 6,325 · see citing works
Epigenetic programming by maternal behavior
Weaver, I. C. G., Cervoni, N., Champagne, F. A., D'Alessio, A. C., Sharma, S., Seckl, J. R., Dymov, S., Szyf, M., & Meaney, M. J. (2004) · Nature Neuroscience · doi:10.1038/nn1276 · Cited by 6,177 · see citing works
Self-citation
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
Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations
Meaney, M. J. (2001) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.24.1.1161 · Cited by 2,708 · see citing works
Epigenetic Transgenerational Actions of Endocrine Disruptors and Male Fertility
Anway, M. D., Cupp, A. S., Uzumcu, M., & Skinner, M. K. (2005) · Science · doi:10.1126/science.1108190 · Cited by 2,563 · see citing works
Adult attachment representations, parental responsiveness, and infant attachment: a meta-analysis on the predictive validity of the adult attachment interview
van IJzendoorn, M. H. (1995) · Psychological Bulletin · doi:10.1037/0033-2909.117.3.387 · Cited by 2,243 · see citing works
Patterns of attachment
Ainsworth, M. D. S. (1985) · PsycEXTRA Dataset · doi:10.1037/e550432011-004 · Cited by 2,140 · see citing works
Procedures for Identifying Infants as Disorganized/Disoriented During the Ainsworth Strange Situation
Main, M., & Solomon, J. (2026) · Routledge eBooks · doi:10.4324/9781003569978-2 · Cited by 1,978 · 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
High sensitivity mapping of methylated cytosines
Susan, J. C., Harrison, J., Paul, C. L., & Frommer, M. (1994) · Nucleic Acids Research · doi:10.1093/nar/22.15.2990 · Cited by 1,862 · see citing works
Cellular differentiation, cytidine analogs and DNA methylation
Jones, P. A., & Taylor, S. M. (1980) · Cell · doi:10.1016/0092-8674(80)90237-8 · Cited by 1,831 · see citing works
Enriched environments, experience-dependent plasticity and disorders of the nervous system
Nithianantharajah, J., & Hannan, A. J. (2006) · Nature Reviews Neuroscience · doi:10.1038/nrn1970 · Cited by 1,771 · see citing works
Attachment and development: A prospective, longitudinal study from birth to adulthood
Sroufe, L. A. (2005) · Attachment & Human Development · doi:10.1080/14616730500365928 · Cited by 1,685 · see citing works
Disorganized attachment in early childhood: Meta-analysis of precursors, concomitants, and sequelae
VAN IJZENDOORN, M. H., SCHUENGEL, C., & BAKERMANS–KRANENBURG, M. J. (1999) · Development and Psychopathology · doi:10.1017/s0954579499002035 · Cited by 1,625 · see citing works
Maternal care during infancy regulates the development of neural systems mediating the expression of fearfulness in the rat
Caldji, C., Tannenbaum, B., Sharma, S., Francis, D., Plotsky, P. M., & Meaney, M. J. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.9.5335 · Cited by 1,437 · see citing works
Parents' unresolved traumatic experiences are related to infant disorganized attachment status: Is frightened and/or frightening parental behavior the linking mechanism?
Main, M., & Hesse, E. (1990) · Cited by 1,203 · 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
Covalent Modification of DNA Regulates Memory Formation
Miller, C. A., & Sweatt, J. D. (2007) · Neuron · doi:10.1016/j.neuron.2007.02.022 · Cited by 1,180 · see citing works
Epigenetic mechanisms of gene regulation
Russo, V. E. A., Martienssen, R. A., & Riggs, A. D. (1996) · Medical Entomology and Zoology · Cited by 1,088 · see citing works
Untitled work
(1990) · doi:10.1097/00004583-199109000-00043 · Cited by 1,085 · see citing works
The Development of the person: the Minnesota study of risk and adaptation from birth to adulthood
(2005) · Choice Reviews Online · doi:10.5860/choice.43-2509 · Cited by 1,080 · see citing works
Determinants of Infant Behavior
&NA; (1964) · The Journal of Nervous and Mental Disease · doi:10.1097/00005053-196409000-00015 · Cited by 1,028 · 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
Estrogen Actions Throughout the Brain
McEwen, B. (2002) · Recent Progress in Hormone Research · doi:10.1210/rp.57.1.357 · Cited by 915 · see citing works
Reversal of maternal programming of stress responses in adult offspring through methyl supplementation: altering epigenetic marking later in life
Weaver, I. C. G., Champagne, F. A., Brown, S. E., Dymov, S., Sharma, S., Meaney, M. J., & Szyf, M. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.3652-05.2005 · Cited by 905 · see citing works
Self-citation
A Prospective Longitudinal Study of Attachment Disorganization/Disorientation
Carlson, E. A. (1998) · Child Development · doi:10.1111/j.1467-8624.1998.tb06163.x · Cited by 820 · see citing works
CpG methylation, chromatin structure and gene silencing—a three‐way connection
Razin, A. (1998) · The EMBO Journal · doi:10.1093/emboj/17.17.4905 · Cited by 791 · see citing works
Maternal care effects on the hippocampal transcriptome and anxiety-mediated behaviors in the offspring that are reversible in adulthood
Weaver, I. C. G., Meaney, M. J., & Szyf, M. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0507526103 · Cited by 771 · see citing works
Dopamine Release in Response to a Psychological Stress in Humans and Its Relationship to Early Life Maternal Care: A Positron Emission Tomography Study Using [ 11 C]Raclopride
Pruessner, J. C., Champagne, F., Meaney, M. J., & Dagher, A. (2004) · The Journal of Neuroscience · doi:10.1523/jneurosci.3422-03.2004 · Cited by 709 · see citing works
Self-citation
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
Self-citation
The potential influence of maternal stress hormones on development and mental health of the offspring
Weinstock, M. (2005) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2004.09.006 · Cited by 706 · 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
Self-citation
Environmental Enrichment Reverses the Effects of Maternal Separation on Stress Reactivity
Francis, D. D., Diorio, J., Plotsky, P. M., & Meaney, M. J. (2002) · The Journal of Neuroscience · doi:10.1523/jneurosci.22-18-07840.2002 · Cited by 663 · see citing works
Maternal Glucocorticoid Secretion Mediates Long-Term Effects of Prenatal Stress
Barbazanges, A., Piazza, P., le Moal, M., & Maccari, S. (1996) · Journal of Neuroscience · doi:10.1523/jneurosci.16-12-03943.1996 · Cited by 655 · see citing works
The Effects of Early Rearing Environment on the Development of GABAA and Central Benzodiazepine Receptor Levels and Novelty-Induced Fearfulness in the Rat
Caldji, C. (2000) · Neuropsychopharmacology · doi:10.1016/s0893-133x(99)00110-4 · Cited by 606 · see citing works
Chapter IV. Maternal Frightened, Frightening, or Atypical Behavior and Disorganized Infant Attachment Patterns
Lyons-Ruth, K., Bronfman, E., & Parsons, E. (2003) · Monographs of the Society for Research in Child Development · doi:10.1111/1540-5834.00034 · Cited by 581 · see citing works
Stability and Transmission of Attachment across Three Generations
Benoit, D., & Parker, K. C. H. (1994) · Child Development · doi:10.1111/j.1467-8624.1994.tb00828.x · Cited by 571 · see citing works
Tactile/Kinesthetic Stimulation Effects on Preterm Neonates
Field, T. M., Schanberg, S. M., SCAFIDI, F. A., Bauer, C. R., Vega‐Lahr, N., Garcia, R., Nystrom, J., & Kuhn, C. M. (1986) · PEDIATRICS · doi:10.1542/peds.77.5.654 · Cited by 553 · see citing works
Determinants of infant behavior
Dobbs, J. M. (1964) · The Journal of Pediatrics · doi:10.1016/s0022-3476(64)80303-6 · Cited by 519 · see citing works
Effect of social isolation on stress-related behavioural and neuroendocrine state in the rat
Weiss, I. C., Pryce, C. R., Jongen-Rêlo, A. L., Nanz-Bahr, N. I., & Feldon, J. (2004) · Behavioural Brain Research · doi:10.1016/j.bbr.2003.10.015 · Cited by 512 · see citing works
Stress During Gestation Alters Postpartum Maternal Care and the Development of the Offspring in a Rodent Model
Champagne, F. A., & Meaney, M. J. (2006) · Biological Psychiatry · doi:10.1016/j.biopsych.2005.10.016 · Cited by 510 · see citing works
Self-citation
Variations in maternal behaviour are associated with differences in oxytocin receptor levels in the rat
Francis, D. D., Champagne, F. C., & Meaney, M. J. (2000) · Journal of Neuroendocrinology · doi:10.1046/j.1365-2826.2000.00599.x · Cited by 496 · see citing works
Self-citation
Fetal undernutrition and disease in later life
Barker, D. (1997) · Reviews of Reproduction · doi:10.1530/ror.0.0020105 · Cited by 457 · see citing works
Influence of Neonatal Rearing Conditions on Stress‐Induced Adrenocorticotropin Responses and Norepinepherine Release in the Hypothalamic Paraventricular Nucleus
Liu, Caldji, Sharma, Plotsky, & Meaney (2000) · Journal of Neuroendocrinology · doi:10.1046/j.1365-2826.2000.00422.x · Cited by 451 · see citing works
Parental 'Affectionless Control' as an Antecedent to Adult Depression: A Risk Factor Delineated
Parker, G. (1983) · Archives of General Psychiatry · doi:10.1001/archpsyc.1983.01790080038005 · Cited by 408 · see citing works
Behavioral, neurochemical and endocrinological characterization of the early social isolation syndrome
Heidbreder, C. A., Weiss, I. C., Domeney, A. M., Pryce, C., Homberg, J., Hedou, G., Feldon, J., Moran, M. C., & Nelson, P. (2000) · Neuroscience · doi:10.1016/s0306-4522(00)00336-5 · Cited by 404 · see citing works
The Parental Bonding Instrument: psychometric properties reviewed.
Parker, G. B. (1989) · PubMed · Cited by 402 · see citing works
Variations in Nucleus Accumbens Dopamine Associated with Individual Differences in Maternal Behavior in the Rat
Champagne, F. A., Chretien, P., Stevenson, C. W., Zhang, T. Y., Gratton, A., & Meaney, M. J. (2004) · The Journal of Neuroscience · doi:10.1523/jneurosci.5322-03.2004 · Cited by 398 · see citing works
Self-citation
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
Self-citation
The role of corticotropin-releasing factor–norepinephrine systems in mediating the effects of early experience on the development of behavioral and endocrine responses to stress
Francis, D. D., Caldji, C., Champagne, F., Plotsky, P. M., & Meaney, M. J. (1999) · Biological Psychiatry · doi:10.1016/s0006-3223(99)00237-1 · Cited by 380 · see citing works
Self-citation
Motivational systems and the neural circuitry of maternal behavior in the rat
Numan, M. (2007) · Developmental Psychobiology · doi:10.1002/dev.20198 · Cited by 358 · see citing works
Stability and Transmission of Attachment across Three Generations
Benoit, D., & Parker, K. C. H. (1994) · Child Development · doi:10.2307/1131510 · Cited by 334 · see citing works
Parental reports of depressives
Parker, G. B. (1981) · Journal of Affective Disorders · doi:10.1016/0165-0327(81)90038-0 · Cited by 328 · see citing works
Assessing the Effects of High Methionine Intake on DNA Methylation
Waterland, R. A. (2006) · Journal of Nutrition · doi:10.1093/jn/136.6.1706s · Cited by 296 · 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
Self-citation
Child abuse and neglect : biosocial dimensions
Gelles, R. J., & Lancaster, J. B. (1987) · De Gruyter eBooks · Cited by 290 · see citing works
Trajectories of maternal depressive symptoms, maternal sensitivity, and children's functioning at school entry.
Campbell, S. B. G., Matestic, P., von Stauffenberg, C., Mohan, R., & Kirchner, T. (2007) · Developmental Psychology · doi:10.1037/0012-1649.43.5.1202 · Cited by 283 · see citing works
Effects of enriched and restricted early environments on the learning ability of bright and dull rats.
Cooper, R. M., & Zubek, J. P. (1958) · Canadian Journal of Psychology/Revue Canadienne de Psychologie · doi:10.1037/h0083747 · Cited by 280 · see citing works
Maternal attachment representations, maternal sensitivity, and the infant-mother attachment relationship.
Pederson, D. R., Gleason, K., Moran, G., & Bento, S. (1998) · Developmental Psychology · doi:10.1037//0012-1649.34.5.925 · Cited by 279 · see citing works
Weaning and Growth of Artificially Rreared Rats
HALL, W. G. (1975) · Science · doi:10.1126/science.1198116 · Cited by 253 · 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 Varying Environmental Demands on Maternal and Infant Behavior
Rosenblum, L. A., & Paully, G. S. (1984) · Child Development · doi:10.1111/j.1467-8624.1984.tb00293.x · Cited by 242 · see citing works
Variations in Maternal Care Alter GABAA Receptor Subunit Expression in Brain Regions Associated with Fear
Caldji, C., Diorio, J. C., & Meaney, M. J. (2003) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300237 · Cited by 241 · see citing works
Maternal behavior in rats: Evidence for the involvement of preoptic projections to the ventral tegmental area.
Numan, M., & Smith, H. G. (1984) · Behavioral Neuroscience · doi:10.1037//0735-7044.98.4.712 · Cited by 217 · see citing works
Early experience affects the intergenerational transmission of infant abuse in rhesus monkeys
Dario Maestripieri, A. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0504122102 · Cited by 213 · see citing works
Maternal care influences neuronal survival in the hippocampus of the rat
Bredy, T. W., Grant, R. J., Champagne, D. L., & Meaney, M. J. (2003) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2003.02965.x · Cited by 208 · see citing works
Environmental influences on the central nervous system and their implications for the aging rat
Mohammed, A. H. S., Henriksson, B. G., Söderström, S., Ebendal, T., Olsson, T., & Seckl, J. R. (1993) · Behavioural Brain Research · doi:10.1016/0166-4328(93)90134-c · Cited by 204 · see citing works
Mothering begets mothering
Fleming, A. S., Kraemer, G. W., Gonzalez, A., Lovic, V., Rees, S., & Melo, A. (2002) · Pharmacology Biochemistry and Behavior · doi:10.1016/s0091-3057(02)00793-1 · Cited by 203 · see citing works
Prenatal stress increases corticotropin-releasing factor (CRF) content and release in rat amygdala minces
Cratty, M. S., Ward, H. E., Johnson, E. A., Azzaro, A. J., & Birkle, D. L. (1995) · Brain Research · doi:10.1016/0006-8993(95)00087-7 · Cited by 201 · see citing works
Maternal Behavior One Year After Early and Extended Post‐partum Contact
Kennell, J. H., Jerauld, R., Wolfe, H., Chester, D., Kreger, N. C., McAlpine, W., Steffa, M., & Klaus, M. H. (1974) · Developmental Medicine & Child Neurology · doi:10.1111/j.1469-8749.1974.tb02738.x · Cited by 200 · 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
The Effects of Varying Environmental Demands on Maternal and Infant Behavior
Rosenblum, L. A., & Paully, G. S. (1984) · Child Development · doi:10.2307/1129854 · Cited by 198 · see citing works
Neuroanatomical Circuitry for Mammalian Maternal Behaviora
Numan, M., & Sheehan, T. P. (1997) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1997.tb51915.x · Cited by 194 · see citing works
Maternal behavior of socially deprived Rhesus monkeys.
Seay, B. M., ALEXANDER, B. K., & Harlow, H. F. (1964) · Journal of Abnormal & Social Psychology · doi:10.1037/h0040539 · Cited by 191 · see citing works
Maternal attachment representations, maternal sensitivity, and the infant–mother attachment relationship.
Pederson, D. R., Gleason, K. E., Moran, G., et al. (1998) · Developmental Psychology · doi:10.1037/0012-1649.34.5.925 · Cited by 191 · see citing works
Maternal behavior in rats: Evidence for the involvement of preoptic projections to the ventral tegmental area.
Numan, M., & Smith, H. G. (1984) · Behavioral Neuroscience · doi:10.1037/0735-7044.98.4.712 · Cited by 190 · see citing works
Influence of naturally occurring variations in maternal care on prepulse inhibition of acoustic startle and the medial prefrontal cortical dopamine response to stress in adult rats
Zhang, T. Y., Chrétien, P., Meaney, M. J., & Gratton, A. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.3293-04.2005 · Cited by 174 · see citing works
Prenatal stress effects on functional development of the offspring
Weinstock, M., Fride, E., & Hertzberg, R. (1988) · Progress in brain research · doi:10.1016/s0079-6123(08)60513-0 · Cited by 173 · see citing works
11β-Hydroxysteroid dehydrogenases: Key enzymes in determining tissue-specific glucocorticoid effects
Edwards, C. R. W., Benediktsson, R., Lindsay, R. S., & Seckl, J. R. (1996) · Steroids · doi:10.1016/0039-128x(96)00033-5 · Cited by 171 · see citing works
Expression of Fos-like immunoreactivity in the preoptic area of maternally behaving virgin and postpartum rats.
Numan, M., & Numan, M. J. (1994) · Behavioral Neuroscience · doi:10.1037//0735-7044.108.2.379 · Cited by 160 · see citing works
The development of the glucocorticoid receptor system in the rat limbic brain. III. Negative-feedback regulation
Sapolsky, R. M., Meaney, M. J., & McEwen, B. S. (1985) · Developmental Brain Research · doi:10.1016/0165-3806(85)90261-5 · Cited by 158 · see citing works
Induced depression in monkeys
Harlow, H. F., & Suomi, S. J. (1974) · Behavioral Biology · doi:10.1016/s0091-6773(74)91475-8 · Cited by 152 · see citing works
Maternally separated rats show deficits in maternal care in adulthood
Lovic, V., González, A., & Fleming, A. S. (2001) · Developmental Psychobiology · doi:10.1002/dev.1024 · Cited by 149 · see citing works
Expression of Fos-like immunoreactivity in the preoptic area of maternally behaving virgin and postpartum rats.
Numan, M., & Numan, M. J. (1994) · Behavioral Neuroscience · doi:10.1037/0735-7044.108.2.379 · Cited by 143 · see citing works
Prenatal stress affects mother–infant interaction in norway rats
Moore, C., & Power, K. L. (1986) · Developmental Psychobiology · doi:10.1002/dev.420190309 · Cited by 141 · see citing works
Early experience and cross‐generational continuity of mother‐infant contact in vervet monkeys
Fairbanks, L. A. (1989) · Developmental Psychobiology · doi:10.1002/dev.420220703 · Cited by 136 · see citing works
Atypical Attachment in Infancy and Early Childhood Among Children at Developmental Risk
Vondra, J. I., Barnett, D., & Pipp‐Siegel, S. (2000) · Cited by 130 · see citing works
Variable foraging demand rearing: sustained elevations in cisternal cerebrospinal fluid corticotropin-releasing factor concentrations in adult primates
Coplan, J. D., Smith, E. L. P., Altemus, M., Scharf, B. A., Owens, M. J., Nemeroff, C. B., Gorman, J. M., & Rosenblum, L. A. (2001) · Biological Psychiatry · doi:10.1016/s0006-3223(01)01175-1 · Cited by 129 · see citing works
Early maternal rejection affects the development of monoaminergic systems and adult abusive parenting in rhesus macaques (Macaca mulatta).
Dario Maestripieri, A., Higley, J. D., Lindell, S. G., Newman, T. K., McCormack, K. M., & Sánchez, M. M. (2006) · Behavioral Neuroscience · doi:10.1037/0735-7044.120.5.1017 · Cited by 123 · 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
Parenting styles of abusive mothers in group-living rhesus macaques
Maestripieri, D. (1998) · Animal Behaviour · doi:10.1006/anbe.1997.0578 · Cited by 116 · see citing works
Prolactin regulation of estrogen receptor expression
Frasor, J. M., & Gibori, G. (2003) · Trends in Endocrinology and Metabolism · doi:10.1016/s1043-2760(03)00030-4 · Cited by 114 · see citing works
Effects of social deprivation on maternal behavior of rhesus monkeys.
Arling, G. L., & Harlow, H. F. (1967) · Journal of Comparative and Physiological Psychology · doi:10.1037/h0025221 · Cited by 112 · see citing works
Tactile-kinesthetic stimulation effects on sympathetic and adrenocortical function in preterm infants
Kuhn, C. M., Schanberg, S. M., Field, T. M., Symanski, R., Zimmerman, E. A., SCAFIDI, F. A., & Roberts, J. (1991) · The Journal of Pediatrics · doi:10.1016/s0022-3476(05)82059-1 · Cited by 110 · see citing works
Maternal Licking of Young: Resource Exchange and Proximate Controls
Gubernick, D. J., & Alberts, J. R. (1983) · Physiology & Behavior · doi:10.1016/s0031-9384(24)00190-2 · Cited by 108 · see citing works
Commentary: Is maternal stimulation the mediator of the handling effect in infancy?
Denenberg, V. H. (1999) · Developmental Psychobiology · doi:10.1002/(sici)1098-2302(199901)34:1 · Cited by 107 · see citing works
The measurement of pathogenic parental style and its relevance to psychiatric disorder
Parker, G. B. (1984) · Social Psychiatry and Psychiatric Epidemiology · doi:10.1007/bf00583818 · Cited by 103 · see citing works
Effects of prenatal stress on anxiety and social interactions in adult rats
Patin, V., Lordi, B., Vincent, A., & Caston, J. (2005) · Developmental Brain Research · doi:10.1016/j.devbrainres.2005.09.010 · Cited by 101 · see citing works
Aberrant DNA methylation in cancer: potential clinical interventions
Strathdee, G. R., & Brown, R. E. (2002) · Expert Reviews in Molecular Medicine · doi:10.1017/s1462399402004222 · Cited by 101 · see citing works
Maternal nutrition during pregnancy and health of the offspring
Martin‐Gronert, M. S., & Ozanne, S. E. (2006) · Biochemical Society Transactions · doi:10.1042/bst0340779 · Cited by 99 · see citing works
Child abuse and neglect: Usefulness of the animal data.
Maestripieri, D., & Carroll, K. A. (1998) · Psychological Bulletin · doi:10.1037/0033-2909.123.3.211 · Cited by 98 · see citing works
Adult antisocial personality traits are associated with experiences of low parental care and maternal overprotection
Reti, I. M., SAMUELS, J. F., Eaton, W. W., Bienvenu, O. J., Costa, P. T., & Nestadt, G. (2002) · Acta Psychiatrica Scandinavica · doi:10.1034/j.1600-0447.2002.02305.x · Cited by 98 · see citing works
Early weaning deprives mouse pups of maternal care and decreases their maternal behavior in adulthood
Kikusui, T., Isaka, Y., & Mori, Y. (2005) · Behavioural Brain Research · doi:10.1016/j.bbr.2005.03.013 · Cited by 97 · see citing works
Site-Specific Analysis of Histone Methylation and Acetylation
Umlauf, D., Goto, Y., & Feil, R. (2004) · Humana Press eBooks · doi:10.1385/1-59259-828-5:099 · Cited by 95 · see citing works
Positive effects of tactile versus kinesthetic or vestibular stimulation on neuroendocrine and ODC activity in maternally-deprived rat pups
Pauk, J. S., Kuhn, C. M., Field, T. M., & Schanberg, S. M. (1986) · Life Sciences · doi:10.1016/0024-3205(86)90359-0 · Cited by 94 · see citing works
Parental representations of neurotic and endogenous depressives
Parker, G. B. (1987) · Journal of Affective Disorders · doi:10.1016/0165-0327(87)90076-0 · Cited by 94 · see citing works
Chromatin and Gene Regulation
(2001) · Wiley eBooks · doi:10.1002/9780470750629 · Cited by 94 · see citing works
Differential Effects of Prenatal Stress in Two Inbred Strains of Rats
Stöhr, T., Wermeling, D. S., Szuran, T. F., et al. (1998) · Pharmacology Biochemistry and Behavior · doi:10.1016/s0091-3057(97)00541-8 · Cited by 87 · see citing works
Intergenerational Transmission of Parental Bonding Among Women
Miller, L., KRAMER, R. A., Warner, V., WICKRAMARATNE, P. J., & Weissman, M. M. (1997) · Journal of the American Academy of Child & Adolescent Psychiatry · doi:10.1097/00004583-199708000-00022 · Cited by 81 · see citing works
Infant abuse runs in families of group-living pigtail macaques
Maestripieri, D., Wallen, K., & Carroll, K. A. (1997) · Child Abuse & Neglect · doi:10.1016/s0145-2134(97)00006-9 · Cited by 75 · see citing works
Neurobiological characteristics of rhesus macaque abusive mothers and their relation to social and maternal behavior
Dario Maestripieri, A., Lindell, S. G., Ayala, A. R., Gold, P. W., & Higley, J. D. (2004) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2004.05.004 · Cited by 75 · see citing works
Maternal behavior regulates long‐term hippocampal expression of BAX and apoptosis in the offspring
Weaver, I. C. G., Grant, R. J., & Meaney, M. J. (2002) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.2002.01054.x · Cited by 73 · see citing works
The Development of Affiliative and Agonistic Social Patterns in Differentially Reared Monkeys
Andrews, M. W., & Rosenblum, L. A. (1994) · Child Development · doi:10.1111/j.1467-8624.1994.tb00824.x · Cited by 72 · see citing works
Postnatal environmental or experiential amelioration of neurobehavioral effects of perinatal alcohol exposure in rats
Hannigan, J. H., O’Leary‐Moore, S. K., & Berman, R. F. (2006) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2006.06.019 · Cited by 71 · see citing works
The estrogen receptor gene: Promoter organization and expression
Grandien, K., Berkenstam, A. L., & Gustafsson, J.-Å. (1997) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/s1357-2725(97)89967-0 · Cited by 71 · see citing works
The effect of tactile stimulation on serum growth hormone and tissue ornithine decarboxylase activity during maternal deprivation in rat pups.
Evoniuk, G. E., Kuhn, C. M., & Schanberg, S. M. (1979) · PubMed · Cited by 68 · see citing works
Gonadal steroid regulation of oxytocin and oxytocin receptor gene expression.
Zingg, H., Rozen, F., Breton, C., Larcher, A., Neculcea, J., Chu, K., Russo, C., & Arslan, A. (1995) · PubMed · Cited by 67 · see citing works
Immature siblings and mother-infant relationships among free-ranging rhesus monkeys on Cayo Santiago
Berman, C. M. (1992) · Animal Behaviour · doi:10.1016/0003-3472(92)90031-4 · Cited by 62 · see citing works
THE NATURE AND QUALITIES OF PARENTING PROVIDED BY WOMEN RAISED IN INSTITUTIONS
Dowdney, L., Skuse, D., Rutter, M. L., et al. (1985) · Journal of Child Psychology and Psychiatry · doi:10.1111/j.1469-7610.1985.tb01644.x · Cited by 62 · see citing works
The Development of Affiliative and Agonistic Social Patterns in Differentially Reared Monkeys
Andrews, M. W., & Rosenblum, L. A. (1994) · Child Development · doi:10.2307/1131506 · Cited by 60 · see citing works
The effects of early rearing environment on the hormonal induction of maternal behavior in virgin rats
Novakov, M., & FLEMING, A. (2005) · Hormones and Behavior · doi:10.1016/j.yhbeh.2005.04.011 · Cited by 57 · see citing works
Artificial rearing causes changes in maternal behavior and c-fos expression in juvenile female rats.
González, A., & Fleming, A. S. (2002) · Behavioral Neuroscience · doi:10.1037//0735-7044.116.6.999 · Cited by 57 · see citing works
Parental representations in drug-dependent patients and their parents
Torresani, S., Favaretto, E., & Zimmermann, C. (2000) · Comprehensive Psychiatry · doi:10.1016/s0010-440x(00)90145-7 · Cited by 56 · see citing works
Dysfunctional parenting as a risk factor to lifetime depression in a sample of employed Japanese adults: evidence for the ‘affectionless control’ hypothesis
Sato, T., Sakado, K., Uehara, T., Narita, T., Hirano, S., Nishioka, K., & Kasahara, Y. (1998) · Psychological Medicine · doi:10.1017/s0033291797006430 · Cited by 56 · see citing works
Evidence for non‐genomic transmission of ecological information via maternal behavior in female rats
McLeod, J., Sinal, C. J., & Perrot-Sinal, T. S. (2006) · Genes Brain & Behavior · doi:10.1111/j.1601-183x.2006.00214.x · Cited by 55 · see citing works
Tactile stimulation and behavioral development among low-birthweight infants
Solkoff, N., & Matuszak, D. L. (1975) · Child Psychiatry & Human Development · doi:10.1007/bf01434430 · Cited by 55 · see citing works
Facilitative effects of maternal environmental enrichment on maze learning in rat offspring
Kiyono, S., Seo, M. L., Shibagaki, M., & Inouye, M. (1985) · Physiology & Behavior · doi:10.1016/0031-9384(85)90207-0 · Cited by 54 · see citing works
Function of nuclear sex hormone receptors in gene regulation
Kato, S., Sato, T., Watanabe, T., Takemasa, S., Masuhiro, Y., Ohtake, F., & Μatsumoto, T. (2005) · Cancer Chemotherapy and Pharmacology · doi:10.1007/s00280-005-0102-8 · Cited by 50 · see citing works
Effects of variation in postnatal maternal environment on maternal behaviour and fear and stress responses in rats
Macrı̀, S., & Würbel, H. (2006) · Animal Behaviour · doi:10.1016/j.anbehav.2006.03.029 · Cited by 47 · see citing works
Artificial rearing causes changes in maternal behavior and c-fos expression in juvenile female rats.
González, A., & Fleming, A. S. (2002) · Behavioral Neuroscience · doi:10.1037/0735-7044.116.6.999 · Cited by 46 · see citing works
Tail-pinch facilitates onset of maternal behavior in rats
Szechtman, H., Siegel, H. I., Rosenblatt, J. S., & Komisaruk, B. R. (1977) · Physiology & Behavior · doi:10.1016/0031-9384(77)90319-5 · Cited by 45 · see citing works
CSF Corticotropin-Releasing Factor in Personality Disorder: Relationship with Self-Reported Parental Care
Lee, R. J., Gollan, J., Kasckow, J., Geracioti, T., & Coccaro, E. F. (2006) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301104 · Cited by 44 · see citing works
Glucocorticoids and fetal programming
Seckl, J. R., Nyirenda, M., Walker, B., & Chapman, K. E. (1999) · Biochemical Society Transactions · doi:10.1042/bst0270074 · Cited by 44 · see citing works
Perceived parenting behavior in the childhood of cocaine users: Relationship with genotype and personality traits
Gerra, G., Zaimovic, A., Garofano, L., Ciusa, F., Moi, G., Avanzini, P., Talarico, E., Gardini, F., Brambilla, F., Manfredini, M., et al. (2006) · American Journal of Medical Genetics Part B Neuropsychiatric Genetics · doi:10.1002/ajmg.b.30388 · Cited by 43 · see citing works
The Impact of Maternal Intergenerational Risk Factors on Adverse Developmental Outcomes
Chapman, D. A., & Scott, K. G. (2001) · Developmental Review · doi:10.1006/drev.2000.0523 · Cited by 42 · see citing works
Transfer of effects from environmentally enriched and impoverished female rats to future offspring
Dell, P. A., & Rose, F. D. (1987) · Physiology & Behavior · doi:10.1016/0031-9384(87)90008-4 · Cited by 39 · see citing works
Influence of Maternal Grooming, Sex and Age on Fos Immunoreactivity in the Preoptic Area of Neonatal Rats: Implications for Sexual Differentiation
McCarthy, M. M., Besmer, H. R., Jacobs, S. C., Keidan, G. M. O., & Gibbs, R. B. (1997) · Developmental Neuroscience · doi:10.1159/000111246 · Cited by 37 · see citing works
Handbook of Stress and the Brain - Part 1: The Neurobiology of Stress
(2005) · Techniques in the behavioral and neural sciences · doi:10.1016/s0921-0709(05)x8001-4 · Cited by 35 · see citing works
Growth hormone response to clonidine in adversely reared young adult primates: relationship to serial cerebrospinal fluid corticotropin-releasing factor concentrations
Coplan, J. D., Smith, E. L., Trost, R. C., Scharf, B., Altemus, M. M., Bjornson, L., Owens, M. J., Gorman, J. M., Nemeroff, C. B., & Rosenblum, L. A. (2000) · Psychiatry Research · doi:10.1016/s0165-1781(00)00173-6 · Cited by 34 · see citing works
Maternal licking by virgin and lactating rats: Water transfer from pups
Gubernick, D. J., & Alberts, J. R. (1985) · Physiology & Behavior · doi:10.1016/0031-9384(85)90040-x · Cited by 33 · 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
Physical stimulation reduces the body temperature of infant rats
Sullivan, R. M., Shokrai, N., & Leon, M. (1988) · Developmental Psychobiology · doi:10.1002/dev.420210304 · Cited by 30 · see citing works
Analysis of taste mixtures by adults and children
Oram, N., Laing, D. G., Freeman, M., & Hutchinson, I. (2000) · Developmental Psychobiology · doi:10.1002/1098-2302(2001)38:1 · Cited by 30 · see citing works
Group and matriline differences in the behaviour of rhesus monkey infants
Simpson, M. J. A., & Howe, S. (1986) · Animal Behaviour · doi:10.1016/s0003-3472(86)80114-2 · Cited by 24 · see citing works
Effect of Tactile Stimulation on Serum Lactate in the Newborn Rat
Alasmi, M., Pickens, W. L., & Hoath, S. B. (1997) · Pediatric Research · doi:10.1203/00006450-199706000-00010 · Cited by 21 · see citing works
Physical stimulation reduces the brain temperature of infant rats
Sullivan, R. M., Wilson, D. A., & Leon, M. (1988) · Developmental Psychobiology · doi:10.1002/dev.420210305 · Cited by 16 · see citing works
Chromatin and Gene Regulation
Zlatanova, J. S. (2002) · Heredity · doi:10.1038/sj.hdy.6800149 · Cited by 13 · see citing works
Transcriptional Regulation of the Oxytocin Receptor Gene
Bale, T. L., & Dorsa, D. M. (1998) · Advances in experimental medicine and biology · doi:10.1007/978-1-4615-4871-3_38 · Cited by 7 · see citing works
Untitled work
(1999) · doi:10.1002/(sici)1096-8644(199909)110:1

Flagged first, then by citations

Research works printed but not linked: 2

[23]Berman C. Intergenerational transmission of maternal rejection rates among free-ranging rheus monkeys on Cayo Santiago. Animal Behavior. 1990;44:247–258. [Google Scholar]
[76]Maestripieri D, Tomaszycki M, Carroll KA. Consistency and change in the behavior of rhesus macaque abusive mothers with successive infants. Dev Psychobiol. 1999;34:29–35. [PubMed] [Google Scholar]

Sorted by citations

Socioeconomic status and the brain: mechanistic insights from human and animal research
Hackman, D. A., Farah, M. J., & Meaney, M. J. (2010) · Nature Reviews Neuroscience · doi:10.1038/nrn2897 · Cited by 1,409 · see citing works
Lasting epigenetic influence of early-life adversity on the BDNF gene
Roth, T. L., Lubin, F. D., Funk, A. J., & Sweatt, J. D. (2009) · Biological Psychiatry · doi:10.1016/j.biopsych.2008.11.028 · Cited by 1,273 · see citing works
Epigenetics and the biological definition of gene×environment interactions
Meaney, M. J. (2010) · Child Development · doi:10.1111/j.1467-8624.2009.01381.x · Cited by 1,239 · see citing works
Beyond DNA: integrating inclusive inheritance into an extended theory of evolution
Danchin, É., Charmantier, A., Champagne, F. A., Mesoudi, A., Pujol, B., & Blanchet, S. (2011) · Nature Reviews Genetics · doi:10.1038/nrg3028 · Cited by 860 · see citing works
Self-citation
The Neurobiology of Human Attachments
Feldman, R. (2017) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2016.11.007 · Cited by 839 · see citing works
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
Oxytocin and social affiliation in humans
Feldman, R. (2012) · Hormones and Behavior · doi:10.1016/j.yhbeh.2012.01.008 · Cited by 767 · see citing works
Maternal Depression and Anxiety Across the Postpartum Year and Infant Social Engagement, Fear Regulation, and Stress Reactivity
Feldman, R., Granat, A., Pariente, C., Kanety, H., Kuint, J., & Gilboa-Schechtman, E. (2009) · Journal of the American Academy of Child & Adolescent Psychiatry · doi:10.1097/chi.0b013e3181b21651 · Cited by 747 · see citing works
Early-life programming of later-life brain and behavior: a critical role for the immune system
Bilbo, S. D. (2009) · Frontiers in Behavioral Neuroscience · doi:10.3389/neuro.08.014.2009 · Cited by 652 · see citing works
Natural variations in maternal and paternal care are associated with systematic changes in oxytocin following parent–infant contact
Feldman, R., Gordon, I., Schneiderman, I., Weisman, O., & Zagoory-Sharon, O. (2010) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2010.01.013 · Cited by 638 · see citing works
Epigenetics and the environmental regulation of the genome and its function
Zhang, T.-Y., & Meaney, M. J. (2010) · Annual Review of Psychology · doi:10.1146/annurev.psych.60.110707.163625 · Cited by 565 · see citing works
Mother and infant coordinate heart rhythms through episodes of interaction synchrony
Feldman, R., Magori-Cohen, R., Galili, G., Singer, M., & Louzoun, Y. (2011) · Infant Behavior and Development · doi:10.1016/j.infbeh.2011.06.008 · Cited by 505 · see citing works
Maternal and paternal plasma, salivary, and urinary oxytocin and parent–infant synchrony: considering stress and affiliation components of human bonding
Feldman, R., Gordon, I., & Zagoory‐Sharon, O. (2011) · Developmental Science · doi:10.1111/j.1467-7687.2010.01021.x · Cited by 486 · see citing works
Oxytocin and the development of parenting in humans
Gordon, I., Zagoory-Sharon, O., Leckman, J. F., & Feldman, R. (2010) · Biological Psychiatry · doi:10.1016/j.biopsych.2010.02.005 · Cited by 469 · see citing works
Touch attenuates infants' physiological reactivity to stress
Feldman, R., Singer, M., & Zagoory, O. (2010) · Developmental Science · doi:10.1111/j.1467-7687.2009.00890.x · Cited by 436 · see citing works
Specifying the Neurobiological Basis of Human Attachment: Brain, Hormones, and Behavior in Synchronous and Intrusive Mothers
Atzil, S., Hendler, T., & Feldman, R. (2011) · Neuropsychopharmacology · doi:10.1038/npp.2011.172 · Cited by 399 · see citing works
Sensitive Parenting Is Associated with Plasma Oxytocin and Polymorphisms in the OXTR and CD38 Genes
Feldman, R., Zagoory-Sharon, O., Weisman, O., Schneiderman, I., Gordon, I., Maoz, R., Shalev, I., & Ebstein, R. P. (2012) · Biological Psychiatry · doi:10.1016/j.biopsych.2011.12.025 · Cited by 393 · 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
Epigenetic influences on brain development and plasticity
Fagiolini, M., Jensen, C. L., & Champagne, F. A. (2009) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2009.05.009 · Cited by 362 · see citing works
Self-citation
Global methylation profiling of lymphoblastoid cell lines reveals epigenetic contributions to autism spectrum disorders and a novel autism candidate gene, RORA , whose protein product is reduced in autistic brain
Nguyen, A., Rauch, T. A., Pfeifer, G. P., & Hu, V. W. (2010) · The FASEB Journal · doi:10.1096/fj.10-154484 · Cited by 350 · see citing works
Transgenerational Inheritance of an Acquired Small RNA-Based Antiviral Response in C. elegans
Rechavi, O., Minevich, G., & Hobert, O. (2011) · Cell · doi:10.1016/j.cell.2011.10.042 · Cited by 351 · see citing works
The role of DNA methylation in stress-related psychiatric disorders
Klengel, T., Pape, J., Binder, E. B., & Mehta, D. (2014) · Neuropharmacology · doi:10.1016/j.neuropharm.2014.01.013 · Cited by 309 · 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
Self-citation
Beyond allostatic load: Rethinking the role of stress in regulating human development
Ellis, B. J., & Del Giudice, M. (2014) · Development and Psychopathology · doi:10.1017/s0954579413000849 · Cited by 290 · see citing works
Approaching the biology of human parental attachment: Brain imaging, oxytocin and coordinated assessments of mothers and fathers
Swain, J. E., Kim, P., Spicer, J., Ho, S. S., Dayton, C. J., Elmadih, A., & Abel, K. M. (2014) · Brain Research · doi:10.1016/j.brainres.2014.03.007 · Cited by 290 · see citing works
Epigenetic Mechanisms of Depression and Antidepressant Action
Vialou, V., Feng, J., Robison, A. J., & Nestler, E. J. (2013) · Annual Review of Pharmacology and Toxicology · doi:10.1146/annurev-pharmtox-010611-134540 · Cited by 277 · see citing works
Epigenetic influence of social experiences across the lifespan
Champagne, F. A. (2010) · Developmental Psychobiology · doi:10.1002/dev.20436 · Cited by 273 · see citing works
Self-citation
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
The Role of Oxytocin in Mother-Infant Relations: A Systematic Review of Human Studies
Galbally, M., Lewis, A. J., van IJzendoorn, M., & Permezel, M. (2011) · Harvard Review of Psychiatry · doi:10.3109/10673229.2011.549771 · Cited by 260 · see citing works
The cross-generation transmission of oxytocin in humans
Feldman, R., Gordon, I., & Zagoory-Sharon, O. (2010) · Hormones and Behavior · doi:10.1016/j.yhbeh.2010.06.005 · Cited by 256 · see citing works
Transcriptional modulation of the developing immune system by early life social adversity
Cole, S. W., Conti, G., Arevalo, J. M. G., Ruggiero, A. M., Heckman, J. J., & Suomi, S. J. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1218253109 · Cited by 207 · 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
Epigenetics and the Biological Basis of Gene × Environment Interactions
Bagot, R. C., & Meaney, M. J. (2010) · Journal of the American Academy of Child & Adolescent Psychiatry · doi:10.1016/j.jaac.2010.06.001 · Cited by 177 · see citing works
Oxytocin, cortisol, and triadic family interactions
Gordon, I., Zagoory-Sharon, O., Leckman, J. F., & Feldman, R. (2010) · Physiology & Behavior · doi:10.1016/j.physbeh.2010.08.008 · Cited by 158 · see citing works
The applied implications of epigenetics in anxiety, affective and stress-related disorders - A review and synthesis on psychosocial stress, psychotherapy and prevention
Schiele, M. A., Gottschalk, M. G., & Domschke, K. (2020) · Clinical Psychology Review · doi:10.1016/j.cpr.2020.101830 · Cited by 156 · see citing works
Oxytocin and the maternal brain
LENG, G., MEDDLE, S., & DOUGLAS, A. (2008) · Current Opinion in Pharmacology · doi:10.1016/j.coph.2008.07.001 · Cited by 158 · see citing works
Developmental Timing of the Effects of Maternal Care on Gene Expression and Epigenetic Regulation of Hormone Receptor Levels in Female Rats
Peña, C. J., Neugut, Y. D., & Champagne, F. A. (2013) · Endocrinology · doi:10.1210/en.2013-1595 · Cited by 150 · see citing works
Self-citation
Oxytocin׳s role in anxiety: A critical appraisal
MacDonald, K., & Feifel, D. (2014) · Brain Research · doi:10.1016/j.brainres.2014.01.025 · Cited by 139 · see citing works
Dynamical systems modeling of physiological coregulation in dyadic interactions
Ferrer, E., & Helm, J. L. (2013) · International Journal of Psychophysiology · doi:10.1016/j.ijpsycho.2012.10.013 · Cited by 132 · see citing works
Oxytocin, vasopressin, and the motivational forces that drive social behaviors
Caldwell, H. K., & Albers, H. E. (2015) · Current Topics in Behavioral Neurosciences · doi:10.1007/7854_2015_390 · Cited by 129 · see citing works
At the frontier of epigenetics of brain sex differences
McCarthy, M. M., & Nugent, B. M. (2015) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2015.00221 · Cited by 123 · see citing works
Bio-behavioral synchrony promotes the development of conceptualized emotions
Atzil, S., & Gendron, M. (2017) · Current Opinion in Psychology · doi:10.1016/j.copsyc.2017.07.009 · Cited by 120 · see citing works
Sex, Receptors, and Attachment: A Review of Individual Factors Influencing Response to Oxytocin
MacDonald, K. S. (2013) · Frontiers in Neuroscience · doi:10.3389/fnins.2012.00194 · Cited by 119 · see citing works
Oxytocin and vasopressin support distinct configurations of social synchrony
Apter-Levi, Y., Zagoory-Sharon, O., & Feldman, R. (2014) · Brain Research · doi:10.1016/j.brainres.2013.10.052 · Cited by 116 · see citing works
Natural variation in early parental care correlates with social behaviors in adolescent prairie voles (Microtus ochrogaster)
Perkeybile, A. M., Griffin, L. L., & Bales, K. L. (2013) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2013.00021 · Cited by 114 · see citing works
Early Adversity and Developmental Outcomes: Interaction Between Genetics, Epigenetics, and Social Experiences Across the Life Span
Champagne, F. A. (2010) · Perspectives on Psychological Science · doi:10.1177/1745691610383494 · Cited by 110 · see citing works
Self-citation
Epigenetic mechanisms in stress and adaptation
Mifsud, K. R., Gutièrrez-Mecinas, M., Trollope, A. F., Collins, A., Saunderson, E. A., & Reul, J. M. H. M. (2011) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2011.06.005 · Cited by 100 · see citing works
Methylation matters in child development: toward developmental behavioral epigenetics
van IJzendoorn, M. H., Bakermans-Kranenburg, M. J., & Ebstein, R. P. (2011) · Child Development Perspectives · doi:10.1111/j.1750-8606.2011.00202.x · Cited by 97 · see citing works
Mechanisms of transgenerational inheritance of addictive-like behaviors
Vassoler, F. M., & Sadri-Vakili, G. (2014) · Neuroscience · doi:10.1016/j.neuroscience.2013.07.064 · Cited by 96 · see citing works
Prereproductive stress to female rats alters corticotropin releasing factor type 1 expression in ova and behavior and brain corticotropin releasing factor type 1 expression in offspring
Zaidan, H., Leshem, M., & Gaisler-Salomon, I. (2013) · Biological Psychiatry · doi:10.1016/j.biopsych.2013.04.014 · Cited by 94 · see citing works
Repeated intranasal oxytocin administration in early life dysregulates the HPA axis and alters social behavior
Rault, J.-L., Carter, C. S., Garner, J. P., Marchant, J. N., Richert, B. T., & Lay, D. C. (2013) · Physiology & Behavior · doi:10.1016/j.physbeh.2013.02.007 · Cited by 94 · see citing works
Germ Cell Origins of Posttraumatic Stress Disorder Risk: The Transgenerational Impact of Parental Stress Experience
Rodgers, A. B., & Bale, T. L. (2015) · Biological Psychiatry · doi:10.1016/j.biopsych.2015.03.018 · Cited by 91 · see citing works
The meaning of weaning: Influence of the weaning period on behavioral development in mice
Curley, J. P., Jordan, E. R., Swaney, W. T., Izraelit, A., Kammel, S., & Champagne, F. A. (2009) · Developmental Neuroscience · doi:10.1159/000216543 · Cited by 92 · see citing works
Early secure attachment as a protective factor against later cognitive decline and dementia
Walsh, E., Blake, Y., Donati, A., Stoop, R., & von Gunten, A. (2019) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2019.00161 · Cited by 84 · see citing works
Environmental regulation of the neural epigenome
Caldji, C., Hellstrom, I. C., Zhang, T.-Y., Diorio, J., & Meaney, M. J. (2011) · FEBS Letters · doi:10.1016/j.febslet.2011.03.032 · Cited by 82 · see citing works
Maternal imprints and the origins of variation
Champagne, F. A. (2011) · Hormones and Behavior · doi:10.1016/j.yhbeh.2011.02.016 · Cited by 74 · see citing works
Self-citation
A review of infants’ and children’s facial cues’ influence on adults’ perceptions and behaviors.
Franklin, P., & Volk, A. A. (2018) · Evolutionary Behavioral Sciences · doi:10.1037/ebs0000108 · Cited by 66 · see citing works
Evolutionary systems theory: a unifying meta-theory of psychological science
Badcock, P. B. (2012) · Review of General Psychology · doi:10.1037/a0026381 · Cited by 61 · see citing works
Early adversity and serotonin transporter genotype interact with hippocampal glucocorticoid receptor mRNA expression, corticosterone, and behavior in adult male rats
Belay, H., Burton, C. L., Lovic, V., Meaney, M. J., Sokolowski, M., & Fleming, A. S. (2011) · Behavioral Neuroscience · doi:10.1037/a0022891 · Cited by 61 · see citing works
Maternal Behavior: Neural Circuits, Stimulus Valence, and Motivational Processes
Numan, M. (2012) · Parenting · doi:10.1080/15295192.2012.680406 · Cited by 62 · see citing works
Incorporating epigenetic mechanisms to advance fetal programming theories
Conradt, E., Adkins, D. E., Crowell, S. E., Raby, K. L., Diamond, L. M., & Ellis, B. (2018) · Development and Psychopathology · doi:10.1017/s0954579418000469 · Cited by 60 · see citing works
The elusive engram: what can infantile amnesia tell us about memory?
Callaghan, B. L., Li, S., & Richardson, R. (2014) · Trends in Neurosciences · doi:10.1016/j.tins.2013.10.007 · Cited by 51 · see citing works
Frank A. Beach Award: Programming of neuroendocrine function by early-life experience: A critical role for the immune system
Bilbo, S. D. (2013) · Hormones and Behavior · doi:10.1016/j.yhbeh.2013.02.017 · Cited by 46 · see citing works
Oxytocin and Cortisol in the Hypnotic Interaction 1
Varga, K., & Kekecs, Z. (2014) · International Journal of Clinical and Experimental Hypnosis · doi:10.1080/00207144.2013.841494 · Cited by 43 · see citing works
Prenatal lipopolysaccharide disrupts maternal behavior, reduces nest odor preference in pups, and induces anxiety: studies of F1 and F2 generations
Penteado, S. H. W., Teodorov, E., Kirsten, T. B., Eluf, B. P., Reis-Silva, T. M., Acenjo, M. K., de Melo, R. C., Suffredini, I. B., & Bernardi, M. M. (2014) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2014.05.058 · Cited by 33 · see citing works
Effects of pre-reproductive maternal enrichment on maternal care, offspring’s play behavior and oxytocinergic neurons
Cutuli, D., Berretta, E., Caporali, P., Sampedro-Piquero, P., De Bartolo, P., Laricchiuta, D., Gelfo, F., Pesoli, M., Foti, F., Farioli Vecchioli, S., et al. (2019) · Neuropharmacology · doi:10.1016/j.neuropharm.2018.02.015 · Cited by 30 · see citing works
Changes in oxytocin and cortisol in active-alert hypnosis: hormonal changes benefiting low hypnotizable participants
Kasos, E., Kasos, K., Pusztai, F., Polyák, Á., Kovács, K. J., & Varga, K. (2018) · International Journal of Clinical and Experimental Hypnosis · doi:10.1080/00207144.2018.1495009 · Cited by 20 · see citing works
Alteration in oxytocin levels induced by early social environment affects maternal behavior and estrogen receptor alpha in mandarin voles (Microtus mandarinus)
Feng, T., An, S., Kinden, R., Zhang, X., Jia, R., & Tai, F. (2019) · Behavioural Brain Research · doi:10.1016/j.bbr.2019.02.038 · Cited by 18 · see citing works
Challenges and prospects for pharmacotherapy in functional gastrointestinal disorders
Sanger, G. J., Chang, L., Bountra, C., & Houghton, L. A. (2010) · Therapeutic Advances in Gastroenterology · doi:10.1177/1756283x10369922 · Cited by 17 · see citing works
The organizational effects of oxytocin and vasopressin: Behavioral implications
Cushing, B. S. (2013) · Oxytocin, Vasopressin and Related Peptides in the Regulation of Behavior · doi:10.1017/cbo9781139017855.006 · Cited by 9 · see citing works

Clonal Transgenerational Effects Transmit for Multiple Generations in a Floating Plant
Zhang, X., Jin, Y., Xue, W., et al. (2023) · Phyton · doi:10.32604/phyton.2023.027113 · Cited by 4 · see citing works
Maternal effects influence temperature-dependent offspring survival in Drosophila melanogasterPreprint
Mohan, S., Groothuis, T. G. G., Vinke, C., et al. (2018) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/372870 · Cited by 2 · see citing works
Maternal age and maternal environment affect egg composition, yolk testosterone, offspring growth and behaviour in laying hens
Widowski, T. M., Cooley, L., Hendriksen, S., & Peixoto, M. R. L. V. (2022) · Scientific Reports · doi:10.1038/s41598-022-05491-6 · Cited by 22 · see citing works
Flight-induced transgenerational maternal effects influence butterfly offspring performance during times of drought
Gibbs, M., Dyck, H. V., & Breuker, C. J. (2017) · Oecologia · doi:10.1007/s00442-017-4030-1 · Cited by 9 · see citing works
The Maternal Environment Affects Offspring Viability via an Indirect Effect of Yolk Investment on Offspring Size
Warner, D. A., & Lovern, M. B. (2014) · Physiological and Biochemical Zoology · doi:10.1086/674454 · Cited by 80 · see citing works

Authors: Champagne, F. A.
Affiliations: Columbia University (US)
Corresponding author: Champagne, Frances A.
ORCID: Champagne, Frances A.
Venue: Frontiers in Neuroendocrinology
Publisher: Elsevier BV
Published: 2008-06
Volume: 29
Issue: 3
Pages: 386-397
ISSN: 0091-3022 (ISSN-L)
DOI: 10.1016/j.yfrne.2008.03.003
PMC: PMC2682215
OpenAlex: W2137189178
Cited by: 812
References: 149
Citations by year: 2026: 31 · 2025: 24 · 2024: 20 · 2023: 51 · 2022: 29 · 2021: 44 · 2020: 90 · 2019: 40 · 2018: 58 · 2017: 49 · 2016: 40 · 2015: 58 · 2014: 48 · 2013: 50 · 2012: 40
FWCI: 6.02
Type: journal article
Language: en
Open access: green
europepmc.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Frontiers in Neuroendocrinology (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Funders: National Institutes of Health (1dp2od001674-01)
Topics: Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic Syndromes and Imprinting
Keywords: epigenetic inheritance, transgenerational effects, maternal care, hypothalamus, postpartum behavior, offspring development, rats
MeSH terms: Animals, Environment, Gene Expression Regulation, Maternal Behavior, Neurosecretory Systems, Stress, Psychological, Touch, Epigenesis, Genetic

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

Epigenetic mechanisms and the transgenerational effects of maternal care

Abstract

Integrity signals

Claims the paper makes

Claims other papers make about this one

Self-check

Cites

Cited by

Related

Record

About these checks