Cited by 1,021Neuroendocrine regulation and behaviorStress Responses and CortisolAnimal Behavior and Reproduction

The DOI matches its Crossref record; 55 of the 55 references it cites were found in a registry or an index.

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

Champagne, Frances A, Francis, Darlene D, Mar, Adam, Meaney, Michael J·2003·Physiology & Behavior

Open this paper in CoChat — free account

Abstract

Variations in maternal care have been widely considered as a critical influence in development. In the rat, variations in maternal behavior, particularly in licking/grooming, regulate the development of endocrine, emotional and cognitive responses to stress. These studies form the basis of a potentially useful model for the study of maternal effects in mammals. In this paper we provide a detailed methodological investigation into this model of maternal behavior, providing an analysis of the frequency, temporal dynamics, and transmission of maternal licking/grooming in several large cohorts. Frequency data indicate that licking/grooming is normally distributed across dams. The peak in licking/grooming occurs in the first few days postpartum and gradually declines. Dams designated as High or Low LG mothers differ in this behavior only during the first week postpartum. Observations over Days 2 to 5 postpartum are essential for the reliable assessments of individual differences in maternal behavior. Individual differences in licking/grooming behavior are stable across multiple litters, and are not associated with differences in litter size, weaning weight of pups, or gender ratio of the litter. We also observed no significant differences in the amount of licking/grooming received by individual pups within a litter, though variation does exist. Finally, maternal licking/grooming is transmitted to female offspring, though there is considerable within-litter variation in the expression of this behavior. Overall, these findings indicate considerable, normal variations in licking/grooming in the rat that are a stable, individual characteristic of rat dams.

Integrity signals

Registry

Crossref · 10.1016/s0031-9384(03)00149-5

Cites

55 of 55 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Claims the paper makes

This paper’s full text isn’t openly available, so its claims and self-check weren’t run. The registry and citation checks still apply.

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?

Type 2 (non-insulin-dependent) diabetes mellitus: the thrifty phenotype hypothesis
Hales, C. N., & Barker, D. J. P. (1992) · Diabetologia · doi:10.1007/bf00400248 · Cited by 3,294
Diabetes mellitus: a "thrifty" genotype rendered detrimental by "progress"?
Neel, J. V. (1962) · Europe PMC (PubMed Central) · Cited by 3,172
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
Self-citation
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
Self-citation
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
Self-citation
The Ecology and Evolution of Inducible Defenses
Harvell, C. D. (1990) · The Quarterly Review of Biology · doi:10.1086/416841 · Cited by 1,728
Maternal Effects As Adaptations
(1998) · doi:10.1093/oso/9780195111637.001.0001 · Cited by 1,653
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
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
Self-citation
The Ecology and Evolution of Inducible Defenses
Tollrian, R., & Harvell, C. D. (1999) · Princeton University Press eBooks · doi:10.1515/9780691228198 · Cited by 971

Show all 55 references

Research works printed but not linked: 2

Pedersen, 1995, Oxytocin control of maternal behavior. Regulation by sex steriods and offspring stimuli, Ann. N. Y. Acad. Sci., 126
Champagne, 2000, Gestational stress effects on maternal behavior, Abstr. Soc. Neurosci., 26, 2035

Sorted by citations

Items 101–200 of 997

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
Self-citation
Sex-Specific and Strain-Dependent Effects of Early Life Adversity on Behavioral and Epigenetic Outcomes
Kundaković, M., Lim, S. C., Gudsnuk, K. M., & Champagne, F. A. (2013) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2013.00078 · Cited by 179
Maternal separation decreases adult hippocampal cell proliferation and impairs cognitive performance but has little effect on stress sensitivity and anxiety in adult Wistar rats
Hulshof, H. J., Novati, A., Sgoifo, A., Luiten, P. G. M., den Boer, J. A., & Meerlo, P. (2011) · Behavioural Brain Research · doi:10.1016/j.bbr.2010.08.038 · Cited by 169
Epigenetic Programming of Phenotypic Variations in Reproductive Strategies in the Rat Through Maternal Care
Cameron, N. M., Shahrokh, D. K., Corpo, A. D., Dhir, S. K., Szyf, M., Champagne, F. A., & Meaney, M. J. (2008) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2008.01725.x · Cited by 171
Nature, nurture or nutrition? Impact of maternal nutrition on maternal care, offspring development and reproductive function
Connor, K. L., Vickers, M. H., Beltrand, J., Meaney, M. J., & Sloboda, D. M. (2012) · The Journal of Physiology · doi:10.1113/jphysiol.2011.223305 · Cited by 165
Epigenetics, brain evolution and behaviour
Keverne, E. B., & Curley, J. P. (2008) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2008.03.001 · Cited by 168
Parenting begets parenting: A neurobiological perspective on early adversity and the transmission of parenting styles across generations
Lomanowska, A. M., Boivin, M., Hertzman, C., & Fleming, A. S. (2017) · Neuroscience · doi:10.1016/j.neuroscience.2015.09.029 · Cited by 224
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
Natural variations in postpartum maternal care in inbred and outbred mice
Champagne, F. A., Curley, J. P., Keverne, E. B., & Bateson, P. P. G. (2007) · Physiology & Behavior · doi:10.1016/j.physbeh.2007.03.014 · Cited by 160
Epigenetics for behavioral ecologists
Ledón‐Rettig, C. C., Richards, C. L., & Martin, L. B. (2012) · Behavioral Ecology · doi:10.1093/beheco/ars145 · Cited by 160
Social allostasis: anticipatory regulation of the internal milieu
Schulkin, J. (2011) · Frontiers in Evolutionary Neuroscience · doi:10.3389/fnevo.2010.00111 · Cited by 157
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 159
Social enrichment during postnatal development induces transgenerational effects on emotional and reproductive behavior in mice
Curley, J. P. (2009) · Frontiers in Behavioral Neuroscience · doi:10.3389/neuro.08.025.2009 · Cited by 184
Maternal care, isolation-induced infant ultrasonic calling, and their relations to adult anxiety-related behavior in the rat.
Wöhr, M., & Schwarting, R. K. W. (2008) · Behavioral Neuroscience · doi:10.1037/0735-7044.122.2.310 · Cited by 161
Ancient origins of human developmental plasticity
Crespi, E. J., & Denver, R. J. (2004) · American Journal of Human Biology · doi:10.1002/ajhb.20098 · Cited by 153
Endocrine-disrupting chemicals: Effects on neuroendocrine systems and the neurobiology of social behavior
Gore, A. C., Krishnan, K., & Reilly, M. P. (2018) · Hormones and Behavior · doi:10.1016/j.yhbeh.2018.11.006 · Cited by 160
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
Self-citation
Epigenetics and parental effects
Kappeler, L., & Meaney, M. J. (2010) · BioEssays · doi:10.1002/bies.201000015 · Cited by 159
Epigenetic effects of stress and corticosteroids in the brain
Hunter, R. G. (2012) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2012.00018 · Cited by 150
Adaptive modulation of behavioural profiles by social stress during early phases of life and adolescence
Sachser, N., Hennessy, M. B., & Kaiser, S. (2010) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2010.09.002 · Cited by 152
Potential risk factors associated with feline behaviour problems
Amat, M., Ruiz-de-la-Torre, J. L., Fatjó, J., Mariotti, V. M., Wijk, S. V., & Manteca, X. (2009) · Applied Animal Behaviour Science · doi:10.1016/j.applanim.2009.09.012 · Cited by 145
Stress and Anxiety Across the Lifespan: Structural Plasticity and Epigenetic Regulation
Hunter, R. G., & McEwen, B. S. (2013) · Epigenomics · doi:10.2217/epi.13.8 · Cited by 142
The influence of unpredictable, fragmented parental signals on the developing brain
Glynn, L. M., & Baram, T. Z. (2019) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2019.01.002 · Cited by 146
The social brain: Neurobiological basis of affiliative behaviours and psychological well-being
Walker, S. C., & McGlone, F. P. (2013) · Neuropeptides · doi:10.1016/j.npep.2013.10.008 · Cited by 145
Social touch-like tactile stimulation activates a tachykinin 1-oxytocin pathway to promote social interactions
Yu, H., Miao, W., Ji, E., Huang, S., Jin, S., Zhu, X., Liu, M.-Z., Sun, Y.-G., Xu, F., & Yu, X. (2022) · Neuron · doi:10.1016/j.neuron.2021.12.022 · Cited by 144
Epigenetic Mechanisms and Gene Networks in the Nervous System
Colvis, C. M., Pollock, J. D., Goodman, R. H., Impey, S., Dunn, J. J., Mandel, G., Champagne, F. A., Mayford, M. R., Korzus, E., Kumar, A., et al. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.4119-05.2005 · Cited by 141
Early life experience drives structural variation of neural genomes in mice
Bedrosian, T. A., Quayle, C., Novaresi, N., & Gage, F. H. (2018) · Science · doi:10.1126/science.aah3378 · Cited by 131
A New Framework for Childhood Health Promotion: The Role of Policies and Programs in Building Capacity and Foundations of Early Childhood Health
Mistry, K. B., Minkovitz, C. S., Riley, A. W., Johnson, S. B., Grason, H. A., Dubay, L. C., & Guyer, B. (2012) · American Journal of Public Health · doi:10.2105/ajph.2012.300687 · Cited by 142
Of rats and women: Narratives of motherhood in environmental epigenetics
Kenney, M., & Müller, R. (2016) · BioSocieties · doi:10.1057/s41292-016-0002-7 · Cited by 142
The individuality of mice
Lathe, R. (2004) · Genes Brain & Behavior · doi:10.1111/j.1601-183x.2004.00083.x · Cited by 138
Prenatal air pollution exposure induces sexually dimorphic fetal programming of metabolic and neuroinflammatory outcomes in adult offspring
Bolton, J. L., Auten, R. L., & Bilbo, S. D. (2013) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2013.10.029 · Cited by 136
A neurobiological perspective on attachment problems in sexual offenders and the role of selective serotonin re-uptake inhibitors in the treatment of such problems
Beech, A. R., & Mitchell, I. (2004) · Clinical Psychology Review · doi:10.1016/j.cpr.2004.10.002 · Cited by 135
Stress Monitoring and Recent Advancements in Wearable Biosensors
Samson, C., & Koh, A. (2020) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2020.01037 · Cited by 129
Inter-individual vs line/strain differences in psychogenetically selected Roman High-(RHA) and Low-(RLA) Avoidance rats: neuroendocrine and behavioural aspects
Steimer, T. J., & Driscoll, P. (2004) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2004.07.002 · Cited by 133
Early motherhood in rats is associated with a modification of hippocampal function
Darnaudéry, M., Perez-Martin, M., Del Favero, F., Gomez-Roldan, C., Garcia-Segura, L. M., & Maccari, S. (2007) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2007.05.012 · Cited by 128
Programming social, cognitive, and neuroendocrine development by early exposure to novelty
Tang, A. C., Akers, K. G., Reeb, B. C., Romeo, R. D., & McEwen, B. S. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0607374103 · Cited by 127
Maternal influences on the sexual behavior and reproductive success of the female rat
Cameron, N. M., Fish, E. W., & Meaney, M. J. (2008) · Hormones and Behavior · doi:10.1016/j.yhbeh.2008.02.013 · Cited by 122
The paradox of drug taking: The role of the aversive effects of drugs
Riley, A. L. (2010) · Physiology & Behavior · doi:10.1016/j.physbeh.2010.11.021 · Cited by 121
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
Development of individual differences in stress responsiveness: an overview of factors mediating the outcome of early life experiences
Claessens, S. E. F., Daskalakis, N. P., van der Veen, R., Oitzl, M. S., de Kloet, E. R., & Champagne, D. L. (2010) · Psychopharmacology · doi:10.1007/s00213-010-2118-y · Cited by 123
How Early Life Stress Impact Maternal Care: A Systematic Review of Rodent Studies
Orso, R., Creutzberg, K. C., Wearick‐Silva, L. E., Viola, T. W., Tractenberg, S. G., Benetti, F., & Grassi‐Oliveira, R. (2019) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2019.00197 · Cited by 131
Oxytocin and postpartum depression: Delivering on what's known and what's not
Kim, S., Soeken, T. A., CROMER, S. J., Martinez, S. R., Hardy, L. R., & Strathearn, L. (2013) · Brain Research · doi:10.1016/j.brainres.2013.11.009 · Cited by 121
Deprivation of maternal care has long-lasting consequences for the hypothalamic–pituitary–adrenal axis of zebra finches
Banerjee, S. B., Arterbery, A. S., Fergus, D. J., & Adkins–Regan, E. (2011) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2011.1265 · Cited by 118
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
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
Variations in postnatal maternal care and the epigenetic regulation of metabotropic glutamate receptor 1 expression and hippocampal function in the rat
Bagot, R. C., Zhang, T.-Y., Wen, X., Nguyen, T. T. T., Nguyen, H.-B., Diorio, J., Wong, T. P., & Meaney, M. J. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1204599109 · Cited by 141
Neuroepigenetics of stress
Griffiths, B. B., & Hunter, R. G. (2014) · Neuroscience · doi:10.1016/j.neuroscience.2014.06.041 · Cited by 117
Separating maternal and litter-size effects on early postnatal growth in two species of altricial small mammals
Rödel, H. G., Prager, G., Stefanski, V., von Holst, D., & Hudson, R. (2007) · Physiology & Behavior · doi:10.1016/j.physbeh.2007.11.047 · Cited by 111
Adult hippocampal glucocorticoid receptor expression and dentate synaptic plasticity correlate with maternal care received by individuals early in life
van Hasselt, F. N., Cornelisse, S., Yuan Zhang, T., Meaney, M. J., Velzing, E. H., Krugers, H. J., & Joëls, M. (2012) · Hippocampus · doi:10.1002/hipo.20892 · Cited by 109
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
Self-citation
Intergenerational transmission of maternal behavior in rhesus macaques and its underlying mechanisms
Dario Maestripieri, A., Lindell, S. G., & Higley, J. D. (2007) · Developmental Psychobiology · doi:10.1002/dev.20200 · Cited by 110
Disruption of Adult Neurogenesis in the Olfactory Bulb Affects Social Interaction but not Maternal Behavior
Feierstein, C. E., Lazarini, F., Wagner, S., Gabellec, M., de Chaumont, F., Olivo‐Marín, J., Boussin, F. D., Lledo, P., & Gheusi, G. (2010) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2010.00176 · Cited by 112
Associations between parenting behavior and anxiety in a rodent model and a clinical sample: relationship to peripheral BDNF levels
Molle, R. D., Portella, A. K., Goldani, M. Z., Kapczinski, F. P., Leistner‐Segal, S., Salum, G. A., Manfro, G. G., & Silveira, P. P. (2012) · Translational Psychiatry · doi:10.1038/tp.2012.126 · Cited by 114
Genetic approaches to hypothalamic-pituitary-adrenal axis regulation
Arnett, M. G., Muglia, L. M., Laryea, G., & Muglia, L. J. (2016) · Neuropsychopharmacology · doi:10.1038/npp.2015.215 · Cited by 105
Effects of gestational stress: 1. Evaluation of maternal and juvenile offspring behavior
Baker, S., Chebli, M., Rees, S., Marec, N. L., Godbout, R., & Bielajew, C. H. (2008) · Brain Research · doi:10.1016/j.brainres.2008.03.035 · Cited by 114
Maternal separation and maternal care act independently on the development of HPA responses in male rats
Macrı̀, S., Chiarotti, F., & Würbel, H. (2008) · Behavioural Brain Research · doi:10.1016/j.bbr.2008.03.031 · Cited by 118
Behavioral phenotyping of mouse models of neurodevelopmental disorders: Relevant social behavior patterns across the life span
Ricceri, L., Moles, A., & Crawley, J. N. (2006) · Behavioural Brain Research · doi:10.1016/j.bbr.2006.08.024 · Cited by 113
Corticotropin-releasing factor receptor 1 mediates acute and delayed stress-induced visceral hyperalgesia in maternally separated Long-Evans rats
Schwetz, I., McRoberts, J. A., Coutinho, S. V., Bradesi, S., Gale, G. D., Fanselow, M. S., Million, M., Ohning, G., Taché, Y., Plotsky, P. M., et al. (2005) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00498.2004 · Cited by 109
Early life influences on emotional reactivity: Evidence that social enrichment has greater effects than handling on anxiety-like behaviors, neuroendocrine responses to stress and central BDNF levels
Cirulli, F., Berry, A., Bonsignore, L. T., Capone, F., D’Andrea, I., Aloe, L., Branchi, I., & Alleva, E. (2010) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2010.02.008 · Cited by 105
Maternal Programming of Individual Differences in Defensive Responses in the Rat
ZHANG, T., Parent, C. I., Weaver, I. C. G., & Meaney, M. J. (2004) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1314.007 · Cited by 103
A review of fundamental principles for animal models of DOHaD research: an Australian perspective
Dickinson, H., Moss, T. J. M., Gatford, K. L., Moritz, K. M., Akison, L. K., Fullston, T., Hryciw, D. H., Maloney, C., Morris, M. J., Wooldridge, A. L., et al. (2016) · Journal of Developmental Origins of Health and Disease · doi:10.1017/s2040174416000477 · Cited by 109
Determinants of Parenting
Bornstein, M. H. (2016) · Wiley eBooks · doi:10.1002/9781119125556.devpsy405 · Cited by 111
Maternal oxytocin response predicts mother-to-infant gaze
Kim, S., Fonagy, P., Koos, O., Dorsett, K., & Strathearn, L. (2014) · Brain Research · doi:10.1016/j.brainres.2013.10.050 · Cited by 102
Paternal influence on female behavior: The role of Peg3 in exploration, olfaction, and neuroendocrine regulation of maternal behavior of female mice.
Champagne, F. A., Curley, J. P., Swaney, W. T., Hasen, N. S., & Keverne, E. B. (2009) · Behavioral Neuroscience · doi:10.1037/a0015060 · Cited by 104
Exposure of neonatal rats to alcohol has differential effects on neuroinflammation and neuronal survival in the cerebellum and hippocampus
Topper, L. A., Baculis, B. C., & Valenzuela, C. F. (2015) · Journal of Neuroinflammation · doi:10.1186/s12974-015-0382-9 · Cited by 107
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 100
Early Experience Modifies the Postnatal Assembly of Autonomic Emotional Motor Circuits in Rats
Card, J. P., Levitt, P. R., Gluhovsky, M. Y., & Rinaman, L. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.2345-05.2005 · Cited by 97
Levels of maternal care in dogs affect adult offspring temperament
Foyer, P., Wilsson, E., & Jensen, P. (2016) · Scientific Reports · doi:10.1038/srep19253 · Cited by 105
Relationships among estrogen receptor, oxytocin and vasopressin gene expression and social interaction in male mice
Murakami, G., Hunter, R. G., Fontaine, C., Ribeiro, A., & Pfaff, D. (2011) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2011.07761.x · Cited by 99
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 97
Epigenetic correlates of neonatal contact in humans
Moore, S. R., McEwen, L. M., Quirt, J., Morin, A. M., Mah, S. M., Barr, R. G., Boyce, W. T., & Kobor, M. S. (2017) · Development and Psychopathology · doi:10.1017/s0954579417001213 · Cited by 95
Limited Bedding and Nesting Induces Maternal Behavior Resembling Both Hypervigilance and Abuse
Gallo, M. E., Shleifer, D. G., Godoy, L. D., Ofray, D., Olaniyan, A., Campbell, T., & Bath, K. G. (2019) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2019.00167 · Cited by 93
The impact of emotional stress early in life on adult voluntary ethanol intake-results of maternal separation in rats
Roman, E., & Nylander, I. (2005) · Stress · doi:10.1080/10253890500188666 · Cited by 94
Maternal Programming of Defensive Responses Through Sustained Effects on Gene Expression
Meaney, M. J. (2007) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780195306255.003.0007 · Cited by 92
Effects of maternal care on the development, emotionality, and reproductive functions in male and female rats
Uriarte, N., Breigeiron, M. K., Benetti, F., Rosa, X. F., & Lucion, A. B. (2007) · Developmental Psychobiology · doi:10.1002/dev.20241 · Cited by 93
Maternal isolation alters the expression of neural proteins during development: ‘Stroking’ stimulation reverses these effects
Chatterjee, D., Chatterjee‐Chakraborty, M., Rees, S., Cauchi, J., de Medeiros, C. B., & Fleming, A. S. (2007) · Brain Research · doi:10.1016/j.brainres.2007.04.069 · Cited by 92
Within-litter variation in maternal care received by individual pups correlates with adolescent social play behavior in male rats.
van Hasselt, F. N., Tieskens, J. M., Trezza, V., Krugers, H. J., Vanderschuren, L. J. M. J., & Joëls, M. (2012) · Physiology & Behavior · doi:10.1016/j.physbeh.2011.12.007 · Cited by 91
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
The Developmental Approach to Child and Adult Health
Conti, G., & Heckman, J. J. (2013) · PEDIATRICS · doi:10.1542/peds.2013-0252d · Cited by 87
Lactational programming? mother's milk energy predicts infant behavior and temperament in rhesus macaques (Macaca mulatta)
Hinde, K., & Capitanio, J. P. (2010) · American Journal of Primatology · doi:10.1002/ajp.20806 · Cited by 89
The importance of early life experiences for the development of behavioural disorders in domestic dogs
Dietz, L., Arnold, A. K., Goerlich, V. C., & Vinke, C. M. (2018) · Behaviour · doi:10.1163/1568539x-00003486 · Cited by 108
Effects of early maternal separation on ethanol intake, GABA receptors and metabolizing enzymes in adult rats
Jaworski, J. N., Francis, D. D., Brommer, C. L., Morgan, E. T., & Kuhar, M. J. (2005) · Psychopharmacology · doi:10.1007/s00213-005-2232-4 · Cited by 88
Why and how the early-life environment affects development of coping behaviours
Langenhof, M. R., & Komdeur, J. (2018) · Behavioral Ecology and Sociobiology · doi:10.1007/s00265-018-2452-3 · Cited by 100
Behaviour and experiences of dogs during the first year of life predict the outcome in a later temperament test
Foyer, P., Bjällerhag, N., Wilsson, E., & Jensen, P. (2014) · Applied Animal Behaviour Science · doi:10.1016/j.applanim.2014.03.006 · Cited by 97
Impact of Prenatal Stress on Neuroendocrine Programming
Viltart, O., & Vanbesien-Mailliot, C. (2007) · The Scientific World JOURNAL · doi:10.1100/tsw.2007.204 · Cited by 91
The absence of maternal pineal melatonin rhythm during pregnancy and lactation impairs offspring physical growth, neurodevelopment, and behavior
Motta‐Teixeira, L. C., Machado‐Nils, A. V., Battagello, D. S., Diniz, G. B., Andrade-Silva, J., Silva, S., de Matos, R. A., do Amaral, F. G., Xavier, G. F., Bittencourt, J. C., et al. (2018) · Hormones and Behavior · doi:10.1016/j.yhbeh.2018.08.006 · Cited by 86
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
Epigenetic dynamics in psychiatric disorders: Environmental programming of neurodevelopmental processes
Kofink, D., Boks, M. P. M., Timmers, H. T. M., & Kas, M. J. (2013) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2013.03.020 · Cited by 83
Natural variation in maternal care and cross-tissue patterns of oxytocin receptor gene methylation in rats
Beery, A. K., McEwen, L. M., MacIsaac, J. L., Francis, D. D., & Kobor, M. S. (2016) · Hormones and Behavior · doi:10.1016/j.yhbeh.2015.05.022 · Cited by 81
Maternal Contact Differentially Modulates Central and Peripheral Oxytocin in Rat Pups During a Brief Regime of Mother–Pup Interaction that Induces a Filial Huddling Preference
Kojima, S., Stewart, R., Demas, G. E., & Alberts, J. R. (2012) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2012.02280.x · Cited by 85
Maternal voluntary drinking in C57BL/6J mice: Advancing a model for fetal alcohol spectrum disorders
Kleiber, M. L., Wright, E., & Singh, S. M. (2011) · Behavioural Brain Research · doi:10.1016/j.bbr.2011.05.005 · Cited by 83
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
Language development after cochlear implantation: an epigenetic model
The CDaCI Investigative Team, Markman, T. M., Quittner, A. L., Eisenberg, L. S., Tobey, E. A., Thal, D. J., Niparko, J. K., & Wang, N. (2011) · Journal of Neurodevelopmental Disorders · doi:10.1007/s11689-011-9098-z · Cited by 89
Early weaning augments neuroendocrine stress responses in mice
Kikusui, T., Nakamura, K., Kakuma, Y., & Mori, Y. (2006) · Behavioural Brain Research · doi:10.1016/j.bbr.2006.08.007 · Cited by 85
Neonatal overfeeding alters adult anxiety and stress responsiveness
Spencer, S. J., & Tilbrook, A. J. (2009) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2009.02.013 · Cited by 82
A guide to designing germline-dependent epigenetic inheritance experiments in mammals
Bohacek, J., & Mansuy, I. M. (2017) · Nature Methods · doi:10.1038/nmeth.4181 · Cited by 80
Using a Developmental Ecology Framework to Align Fear Neurobiology Across Species
Callaghan, B. L., Meyer, H. C., Opendak, M. M., Tieghem, M. V., Harmon, C., Li, A., Lee, F. S., Sullivan, R. M., & Tottenham, N. (2019) · Annual Review of Clinical Psychology · doi:10.1146/annurev-clinpsy-050718-095727 · Cited by 81
Epigenetic programming of neurodegenerative diseases by an adverse environment
Babenko, O., Kovalchuk, I., & Metz, G. A. S. (2012) · Brain Research · doi:10.1016/j.brainres.2012.01.038 · Cited by 80
Effect of androgen treatment during foetal and/or neonatal life on ovarian function in prepubertal and adult rats
Tyndall, V., Broyde, M., Sharpe, R. M., Welsh, M., Drake, A. J., & McNeilly, A. S. (2011) · Reproduction · doi:10.1530/rep-11-0239 · Cited by 80
Transgenerational effects of early environmental insults on aging and disease incidence
Ambeskovic, M., Roseboom, T. J., & Metz, G. A. S. (2017) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2017.08.002 · Cited by 81

Authors: Champagne, F. A., Francis, D. D., Mar, A., & Meaney, M. J.
Affiliations: Douglas Mental Health University Institute (CA)
Corresponding author: Meaney, Michael J
ORCID: Champagne, Frances A
Mar, Adam
Meaney, Michael J
Venue: Physiology & Behavior
Publisher: Elsevier BV
Published: 2003-08
Volume: 79
Issue: 3
Pages: 359-371
ISSN: 0031-9384 (ISSN-L)
DOI: 10.1016/s0031-9384(03)00149-5
OpenAlex: W2110374066
Cited by: 1,021
References: 55
Citations by year: 2026: 30 · 2025: 32 · 2024: 20 · 2023: 29 · 2022: 36 · 2021: 30 · 2020: 56 · 2019: 52 · 2018: 49 · 2017: 60 · 2016: 50 · 2015: 68 · 2014: 58 · 2013: 61 · 2012: 64
FWCI: 37.12
Type: journal article
Language: en
Open access: closed
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Physiology & Behavior (publishedVersion)
PubMed (publishedVersion)
Topics: Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Neuroendocrine regulation and behavior
Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Animal Behavior and Reproduction
Keywords: maternal behavior, intergenerational transmission, individual differences, postpartum behavior, litter size, pup weight, maternal effects, rat model
MeSH terms: Adaptation, Physiological, Animals, Female, Grooming, Imprinting, Psychological, Individuality, Lactation, Litter Size, Maternal Behavior, Phenotype, Sex Factors, Rats, Long-Evans, Models, Animal, Rats

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

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

Abstract

Overview

Integrity signals

Verification

Claims the paper makes

Claims other papers make about this one

Citations

Cites

Cited by

Related

Metadata

Record

About these checks