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
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.
Overview
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
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?
In the citing paper
“For example, maternal caregiving behaviors (e.g., nursing, licking, grooming) among rats influence the responsiveness to stress in the offspring; the effects can be seen in behavioral as well as from the neurological and endocrine responses of the offspring (e.g., Champagne et al. 2003, Pruessner et al. 2004).”
From Mediators and Mechanisms of Change in Psychotherapy Research (2007) · cites this paper as Champagne et al. 2003
In the citing paper
“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 et al., 2003
Citations
Cites
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
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-citationMeaney, M. J. (2001) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.24.1.1161 · Cited by 2,708
Self-citationNongenomic 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-citationThe 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
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-citationThe Ecology and Evolution of Inducible Defenses
Tollrian, R., & Harvell, C. D. (1999) · Princeton University Press eBooks · doi:10.1515/9780691228198 · Cited by 971
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
Cited by
Sorted by citations
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
Mediators and Mechanisms of Change in Psychotherapy Research
Kazdin, A. E. (2007) · Annual Review of Clinical Psychology · doi:10.1146/annurev.clinpsy.3.022806.091432 · Cited by 2,504
Developmental Origins of the Metabolic Syndrome: Prediction, Plasticity, and Programming
Mcmillen, I. C., & Robinson, J. S. (2005) · Physiological Reviews · doi:10.1152/physrev.00053.2003 · Cited by 1,910
Epigenetic regulation in psychiatric disorders
Tsankova, N., Renthal, W., Kumar, A., & Nestler, E. J. (2007) · Nature reviews. Neuroscience · doi:10.1038/nrn2132 · Cited by 1,400
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
Self-citationThe reactive scope model — A new model integrating homeostasis, allostasis, and stress
Romero, L. M., Dickens, M. J., & Cyr, N. E. (2009) · Hormones and Behavior · doi:10.1016/j.yhbeh.2008.12.009 · Cited by 1,096
Meaney, M. J., & Szyf, M. (2005) · Dialogues in Clinical Neuroscience · doi:10.31887/dcns.2005.7.2/mmeaney · Cited by 958
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
Self-citationThe Biological Effects of Childhood Trauma
De Bellis, M. D., & Zisk, A. (2014) · Child and Adolescent Psychiatric Clinics of North America · doi:10.1016/j.chc.2014.01.002 · Cited by 892
Epigenetic mechanisms and the transgenerational effects of maternal care
Champagne, F. A. (2008) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2008.03.003 · Cited by 812
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
Understanding how and why psychotherapy leads to change
Kazdin, A. E. (2009) · Psychotherapy Research · doi:10.1080/10503300802448899 · Cited by 728
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
Champagne, D. L., Bagot, R. C., van Hasselt, F., Ramakers, G., Meaney, M. J., de Kloet, E. R., Joels, M., & Krugers, H. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.0526-08.2008 · Cited by 661
Maternal care as a model for experience-dependent chromatin plasticity?
Meaney, M. J., & Szyf, M. (2005) · Trends in Neurosciences · doi:10.1016/j.tins.2005.07.006 · Cited by 658
Self-citationFeldman, R., Gordon, I., Schneiderman, I., Weisman, O., & Zagoory-Sharon, O. (2010) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2010.01.013 · Cited by 638
Bridgett, D. J., Burt, N. M., Edwards, E. S., & Deater-Deckard, K. D. (2015) · Psychological Bulletin · doi:10.1037/a0038662 · Cited by 730
Daskalakis, N. P., Bagot, R. C., Parker, K. J., Vinkers, C. H., & de Kloet, E. R. (2013) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2013.06.008 · Cited by 579
Robinson, G. E., Fernald, R. D., & Clayton, D. F. (2008) · Science · doi:10.1126/science.1159277 · Cited by 595
HOW THE BRAIN PROCESSES SOCIAL INFORMATION: Searching for the Social Brain
Insel, T. R., & Fernald, R. D. (2004) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.27.070203.144148 · Cited by 556
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
Self-citationPlotsky, P. M., Thrivikraman, K. V., Nemeroff, C. B., Caldji, C., Sharma, S., & Meaney, M. J. (2005) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300769 · Cited by 522
Self-citationWeaver, I. C. G., D'Alessio, A. C., Brown, S. E., Hellstrom, I. C., Dymov, S., Sharma, S., Szyf, M., & Meaney, M. J. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.4164-06.2007 · Cited by 508
Champagne, F. A., & Meaney, M. J. (2006) · Biological Psychiatry · doi:10.1016/j.biopsych.2005.10.016 · Cited by 510
Epigenetic mechanisms mediating the long-term effects of maternal care on development
Champagne, F. A., & Curley, J. P. (2008) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2007.10.009 · Cited by 520
Toward understanding how early-life stress reprograms cognitive and emotional brain networks
Chen, Y., & Baram, T. Z. (2016) · Neuropsychopharmacology · doi:10.1038/npp.2015.181 · Cited by 474
The Science of Early Life Toxic Stress for Pediatric Practice and Advocacy
Johnson, S. B., Riley, A. W., Granger, D. A., & Riis, J. L. (2013) · PEDIATRICS · doi:10.1542/peds.2012-0469 · Cited by 493
Monk, C. E., Spicer, J., & Champagne, F. A. (2012) · Development and Psychopathology · doi:10.1017/s0954579412000764 · Cited by 475
Broad Epigenetic Signature of Maternal Care in the Brain of Adult Rats
McGowan, P. O., Suderman, M., Sasaki, A., Huang, T. C. T., Hallett, M., Meaney, M. J., & Szyf, M. (2011) · PLoS ONE · doi:10.1371/journal.pone.0014739 · Cited by 452
Barrett, J., & Fleming, A. S. (2011) · Journal of Child Psychology and Psychiatry · doi:10.1111/j.1469-7610.2010.02306.x · Cited by 433
Maternal separation as a model of brain-gut axis dysfunction
O’Mahony, S. M., Hyland, N. P., Dinan, T. G., & Cryan, J. F. (2011) · Psychopharmacology · doi:10.1007/s00213-010-2010-9 · Cited by 415
Pryce, C. R., Rüedi‐Bettschen, D., Dettling, A. C., Weston, A. A., Russig, H., Ferger, B., & Feldon, J. (2005) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2005.03.011 · Cited by 430
Environment and Brain Plasticity: Towards an Endogenous Pharmacotherapy
Sale, A., Berardi, N., & Maffei, L. (2014) · Physiological Reviews · doi:10.1152/physrev.00036.2012 · Cited by 402
Ivy, A. S., Brunson, K. L., Sandman, C., & Baram, T. Z. (2008) · Neuroscience · doi:10.1016/j.neuroscience.2008.04.019 · Cited by 407
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
Atzil, S., Gao, W., Fradkin, I., & Barrett, L. F. (2018) · Nature Human Behaviour · doi:10.1038/s41562-018-0384-6 · Cited by 415
Kaffman, A., & Meaney, M. J. (2007) · Journal of Child Psychology and Psychiatry · doi:10.1111/j.1469-7610.2007.01730.x · Cited by 391
Champagne, F. A., & Meaney, M. J. (2007) · Behavioral Neuroscience · doi:10.1037/0735-7044.121.6.1353 · Cited by 381
Self-citationEpigenetic regulation of gene expression in physiological and pathological brain processes
Gräff, J., Kim, D., Dobbin, M. M., & Tsai, L.-H. (2011) · Physiological Reviews · doi:10.1152/physrev.00012.2010 · Cited by 373
Oxytocin–dopamine interactions mediate variations in maternal behavior in the rat
Shahrokh, D. K., Zhang, T.-Y., Diorio, J., Gratton, A., & Meaney, M. J. (2010) · Endocrinology · doi:10.1210/en.2009-1271 · Cited by 366
The origins of altruism in offspring care.
Preston, S. D. (2013) · Psychological Bulletin · doi:10.1037/a0031755 · Cited by 368
Numan, M., & Stolzenberg, D. S. (2008) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2008.10.002 · Cited by 361
Epigenetic programming of stress responses through variations in maternal care
FISH, E. W., SHAHROKH, D., BAGOT, R., CALDJI, C., BREDY, T., SZYF, M., & MEANEY, M. J. (2004) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1330.011 · Cited by 361
Self-citationBrain development under stress: Hypotheses of glucocorticoid actions revisited
Oitzl, M. S., Champagne, D. L., van der Veen, R., & de Kloet, E. R. (2009) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2009.07.006 · Cited by 372
The Consequences of Early‐Life Adversity: Neurobiological, Behavioural and Epigenetic Adaptations
Maccari, S., Krugers, H. J., Morley‐Fletcher, S., Szyf, M., & Brunton, P. J. (2014) · Journal of Neuroendocrinology · doi:10.1111/jne.12175 · Cited by 367
Zhang, T. Y., Labonté, B., Wen, X. L., Turecki, G., & Meaney, M. J. (2013) · Neuropsychopharmacology · doi:10.1038/npp.2012.149 · Cited by 347
Maternal programming of steroid receptor expression and phenotype through DNA methylation in the rat
Szyf, M., Weaver, I. C. G., Champagne, F. A., Diorio, J., & Meaney, M. J. (2005) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2005.10.002 · Cited by 348
Self-citationWeaver, I. C. G., Diorio, J. C., Seckl, J. R., Szyf, M., & Meaney, M. J. (2004) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1321.099 · Cited by 332
Guo, S.-W. (2009) · Molecular Human Reproduction · doi:10.1093/molehr/gap064 · Cited by 328
Cameron, N. M., Champagne, F. A., Parent, C., Fish, E. W., Ozaki-Kuroda, K., & Meaney, M. J. (2005) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2005.03.022 · Cited by 320
Self-citationEpigenetic codes in cognition and behaviour
Gräff, J., & Mansuy, I. M. (2008) · Behavioural Brain Research · doi:10.1016/j.bbr.2008.01.021 · Cited by 328
Early-life experience, epigenetics, and the developing brain
Kundakovic, M., & Champagne, F. A. (2015) · Neuropsychopharmacology · doi:10.1038/npp.2014.140 · Cited by 304
Self-citationEarly life genetic, epigenetic and environmental factors shaping emotionality in rodents
Holmes, A., Guisquet, A. M. L., Vogel, E., Millstein, R. A., Leman, S., & Belzung, C. (2005) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2005.04.012 · Cited by 308
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 305
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
Epigenetic principles and mechanisms underlying nervous system functions in health and disease
Mehler, M. F. (2008) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2008.10.001 · Cited by 300
Pro-social behavior in rats is modulated by social experience
Ben-Ami Bartal, I., Rodgers, D. A., Bernardez Sarria, M. S., Decety, J., & Mason, P. (2014) · eLife · doi:10.7554/elife.01385 · Cited by 286
A hitchhiker's guide to behavioral analysis in laboratory rodents
Sousa, N., Almeida, O. F. X., & Wotjak, C. T. (2006) · Genes Brain & Behavior · doi:10.1111/j.1601-183x.2006.00228.x · Cited by 280
Epigenetic influence of social experiences across the lifespan
Champagne, F. A. (2010) · Developmental Psychobiology · doi:10.1002/dev.20436 · Cited by 273
Maternal Care and DNA Methylation of a Glutamic Acid Decarboxylase 1 Promoter in Rat Hippocampus
Zhang, T., Hellstrom, I. C., Bagot, R. C., Wen, X., Diorio, J. C., & Meaney, M. J. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.1039-10.2010 · Cited by 271
The stress response systems: Universality and adaptive individual differences☆
ELLIS, B., JACKSON, J., & BOYCE, W. (2006) · Developmental Review · doi:10.1016/j.dr.2006.02.004 · Cited by 265
Personalized medicine in psychiatry: problems and promises
Ozomaro, U., Wahlestedt, C., & Nemeroff, C. B. (2013) · BMC Medicine · doi:10.1186/1741-7015-11-132 · Cited by 270
Understanding the potency of stressful early life experiences on brain and body function
McEwen, B. S. (2008) · Metabolism · doi:10.1016/j.metabol.2008.07.006 · Cited by 278
Ordinary Variations in Maternal Caregiving Influence Human Infants' Stress Reactivity
Hane, A. A., & Fox, N. A. (2006) · Psychological Science · doi:10.1111/j.1467-9280.2006.01742.x · Cited by 257
Curley, J. P., & Champagne, F. A. (2015) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2015.11.001 · Cited by 279
Macrı̀, S., & Würbel, H. (2006) · Hormones and Behavior · doi:10.1016/j.yhbeh.2006.06.015 · Cited by 258
Roth, T. L., & David Sweatt, J. (2011) · Journal of Child Psychology and Psychiatry · doi:10.1111/j.1469-7610.2010.02282.x · Cited by 246
Animal models of anxiety disorders in rats and mice: some conceptual issues
Steimer, T. J. (2011) · Dialogues in Clinical Neuroscience · doi:10.31887/dcns.2011.13.4/tsteimer · Cited by 242
Caldji, C., Diorio, J. C., & Meaney, M. J. (2003) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300237 · Cited by 243
Macrı̀, S., Mason, G. J., & Würbel, H. (2004) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2004.03541.x · Cited by 245
Weaver, I. C. G. (2007) · Epigenetics · doi:10.4161/epi.2.1.3881 · Cited by 239
The evolutionary origins of mood and its disorders
Nettle, D., & Bateson, M. (2012) · Current Biology · doi:10.1016/j.cub.2012.06.020 · Cited by 230
Fragmentation and high entropy of neonatal experience predict adolescent emotional outcome
Molet, J., Heins, K., Zhuo, X., Mei, Y., Regev, L., Baram, T. Z., & Stern, H. S. (2016) · Translational Psychiatry · doi:10.1038/tp.2015.200 · Cited by 230
Genes, hormones, and circuits: An integrative approach to study the evolution of social behavior
O’Connell, L. A., & Hofmann, H. A. (2010) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2010.12.004 · Cited by 238
Plasticity, Robustness, Development and Evolution
(2012) · International Journal of Epidemiology · doi:10.1093/ije/dys033 · Cited by 223
Bagot, R. C., van Hasselt, F. N., Champagne, D. L., Meaney, M. J., Krugers, H. J., & Joëls, M. (2009) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2009.03.004 · Cited by 216
How social experiences influence the brain
Champagne, F. A., & Curley, J. P. (2005) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2005.10.001 · Cited by 225
The importance of early bonding on the long-term mental health and resilience of children
Winston, R. M. L., & Chicot, R. (2016) · London Journal of Primary Care · doi:10.1080/17571472.2015.1133012 · Cited by 255
Reproductive experience alters hippocampal neurogenesis during the postpartum period in the dam
Pawluski, J. L., & Galea, L. A. M. (2007) · Neuroscience · doi:10.1016/j.neuroscience.2007.07.031 · Cited by 216
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 209
Maternal programming of defensive responses through sustained effects on gene expression
Zhang, T.-Y., Bagot, R., Parent, C., Nesbitt, C., Bredy, T. W., Caldji, C., Fish, E., Anisman, H., Szyf, M., & Meaney, M. J. (2006) · Biological Psychology · doi:10.1016/j.biopsycho.2006.01.009 · Cited by 206
Maternal separation alters drug intake patterns in adulthood in rats
Moffett, M. C., Vicentic, A., Kozel, M. A., Plotsky, P. M., Francis, D. D., & Kuhar, M. J. (2006) · Biochemical Pharmacology · doi:10.1016/j.bcp.2006.08.003 · Cited by 205
Crushing of piglets by the mother sow (Sus scrofa)—purely accidental or a poor mother?
Andersen, I. L., Berg, S., & Bøe, K. E. (2005) · Applied Animal Behaviour Science · doi:10.1016/j.applanim.2004.11.015 · Cited by 198
Braun, T., Challis, J. R., Newnham, J. P., & Sloboda, D. M. (2013) · Endocrine Reviews · doi:10.1210/er.2013-1012 · Cited by 196
Bredy, T. W., Zhang, T. Y., Grant, R. J., Diorio, J., & Meaney, M. J. (2004) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2004.03599.x · Cited by 196
Social influences on neurobiology and behavior: Epigenetic effects during development
Curley, J. P., Jensen, C. L., Rahia Mashoodh, A., & Champagne, F. A. (2010) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2010.06.005 · Cited by 205
Opposite effects of early maternal deprivation on neurogenesis in male versus female rats
Oomen, C. A., Girardi, C. E. N., Cahyadi, R., Verbeek, E. C., Krugers, H., Joëls, M., & Lucassen, P. J. (2009) · PLoS ONE · doi:10.1371/journal.pone.0003675 · Cited by 190
Mice selected for high versus low stress reactivity: A new animal model for affective disorders
Touma, C., Bunck, M., Glasl, L., Nußbaumer, M., Palme, R., Stein, H., Wolferstätter, M., Zeh, R., Zimbelmann, M., Holsboer, F., et al. (2008) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2008.03.013 · Cited by 194
Behavior genetics and postgenomics
Charney, E. (2012) · Behavioral and Brain Sciences · doi:10.1017/s0140525x11002226 · Cited by 215
Lowell, D. I., Carter, A. S., Godoy, L., Paulicin, B., & Briggs-Gowan, M. J. (2011) · Child Development · doi:10.1111/j.1467-8624.2010.01550.x · Cited by 189
Walker, S. C., Trotter, P. D., Swaney, W. T., Marshall, A. G., & McGlone, F. P. (2017) · Neuropeptides · doi:10.1016/j.npep.2017.01.001 · Cited by 204
Epigenetic Influence of Stress and the Social Environment
Gudsnuk, K. M., & Champagne, F. A. (2012) · ILAR Journal · doi:10.1093/ilar.53.3-4.279 · Cited by 196
Vinall, J., Pavlova, M., Asmundson, G. J. G., Rasic, N. F., & Noel, M. E. (2016) · Children · doi:10.3390/children3040040 · Cited by 198
Early-life adversity and neurological disease: age-old questions and novel answers
Short, A. K., & Baram, T. Z. (2019) · Nature Reviews Neurology · doi:10.1038/s41582-019-0246-5 · Cited by 187
Hypothalamic‐Pituitary‐Adrenal (HPA) Axis and Aging
Gupta, D., & Morley, J. E. (2014) · Comprehensive physiology · doi:10.1002/cphy.c130049 · Cited by 210
Hellstrom, I. C., Dhir, S. K., Diorio, J. C., & Meaney, M. J. (2012) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2012.0223 · Cited by 171
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
Epigenetic Inheritance of Disease and Disease Risk
Bohacek, J., & Mansuy, I. M. (2012) · Neuropsychopharmacology · doi:10.1038/npp.2012.110 · Cited by 180
The influence of natural variations in maternal care on play fighting in the rat
Parent, C. I., & Meaney, M. J. (2008) · Developmental Psychobiology · doi:10.1002/dev.20342 · Cited by 175
Self-citationBeyond the Stress Concept: Allostatic Load—A Developmental Biological and Cognitive Perspective
LUPIEN, S. J., Ouellet‐Morin, I., Hupbach, A., Tu, M. T., Buß, C., Walker, D., Pruessner, J. C., & McEwen, B. S. (2015) · Wiley eBooks · doi:10.1002/9780470939390.ch14 · Cited by 176
Metadata
- Authors
- Champagne, F. A., Francis, D. D., Mar, A., & Meaney, M. J.
- Affiliations
- Douglas Mental Health University Institute (CA)
- Corresponding author
- Meaney, Michael J
- Venue
- Physiology & Behavior
- Publisher
- Elsevier BV
- Published
- 2003-08
- Volume
- 79
- Issue
- 3
- Pages
- 359-371
- ISSN
- 0031-9384 (ISSN-L)
- 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
- 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