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.
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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 et al., 2003
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 · see citing works
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
Self-citationDiabetes mellitus: a "thrifty" genotype rendered detrimental by "progress"?
Neel, J. V. (1962) · Europe PMC (PubMed Central) · Cited by 3,147 · see citing works
Meaney, M. J. (2001) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.24.1.1161 · Cited by 2,708 · see citing works
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 · see citing works
Self-citationThe Ecology and Evolution of Inducible Defenses
Harvell, C. D. (1990) · The Quarterly Review of Biology · doi:10.1086/416841 · Cited by 1,731 · see citing works
Maternal Effects As Adaptations
(1998) · doi:10.1093/oso/9780195111637.001.0001 · Cited by 1,673 · see citing works
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
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
The Ecology and Evolution of Inducible Defenses
Tollrian, R., & Harvell, C. D. (1999) · Princeton University Press eBooks · doi:10.1515/9780691228198 · Cited by 971 · see citing works
Transgenerational induction of defences in animals and plants
Agrawal, A. A., Laforsch, C., & Tollrian, R. (1999) · Nature · doi:10.1038/43425 · Cited by 862 · see citing works
Mother Nature: A History of Mothers, Infants, and Natural Selection
Hrdy, S. B. (1999) · DigitalGeorgetown (Georgetown University Library) · Cited by 788 · see citing works
Long-term behavioral and neuroendocrine adaptations to adverse early experience
Ladd, C. O., Huot, R. L., Thrivikraman, K. V., Nemeroff, C. B., Meaney, M. J., & Plotsky, P. M. (2000) · Progress in brain research · doi:10.1016/s0079-6123(08)62132-9 · Cited by 717 · see citing works
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
Coplan, J. D., Andrews, M. W., Rosenblum, L. A., Owens, M. J., Friedman, S., Gorman, J. M., & Nemeroff, C. B. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.4.1619 · Cited by 649 · see citing works
Parenting and its Effects on Children: On Reading and Misreading Behavior Genetics
Maccoby, E. E. (2000) · Annual Review of Psychology · doi:10.1146/annurev.psych.51.1.1 · Cited by 582 · see citing works
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
Early determinants of behaviour: evidence from primate studies
Suomi, S. J. (1997) · British Medical Bulletin · doi:10.1093/oxfordjournals.bmb.a011598 · Cited by 483 · see citing works
The Developmental Impact of Different Forms of Child Abuse and Neglect
Trickett, P. K., & McBride-Chang, C. (1995) · Developmental Review · doi:10.1006/drev.1995.1012 · Cited by 472 · see citing works
Hockaday, T. D. R., & Yajnik, C. S. (2003) · Diabetologia · doi:10.1007/s00125-002-1024-1 · Cited by 470 · see citing works
Parker, B. J., McFARLANE, J. M., & Soeken, K. L. (1994) · PubMed · Cited by 438 · see citing works
Fleming, A. S., O’Day, D. H., & Kraemer, G. W. (1999) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(99)00011-1 · Cited by 429 · see citing works
Mother rats interact differently with male amd female offspring.
Moore, C. L., & Morelli, G. A. (1979) · Journal of Comparative and Physiological Psychology · doi:10.1037/h0077599 · Cited by 353 · see citing works
The Ontogeny of the Hypothalamic‐Pituitary‐Adrenal Axis. The Influence of Maternal Factorsa
Levine, S. D. (1994) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1994.tb39245.x · Cited by 343 · see citing works
Maternal Depression Effects on Infants and Early Interventions
Field, T. (1998) · Preventive Medicine · doi:10.1006/pmed.1998.0293 · Cited by 325 · see citing works
Possible Role for Endogenous Oxytocin in Estrogen-Facilitated Maternal Behavior in Rats
Fahrbach, S. E., Morrell, J. I., & Pfaff, D. W. (2008) · Neuroendocrinology · doi:10.1159/000124125 · Cited by 322 · see citing works
Haapasalo, J., & Tremblay, R. E. (1994) · Journal of Consulting and Clinical Psychology · doi:10.1037//0022-006x.62.5.1044 · Cited by 309 · see citing works
Settling nature and nurture into an ontogenetic niche
West, M. J., & King, A. P. (1987) · Developmental Psychobiology · doi:10.1002/dev.420200508 · Cited by 305 · see citing works
Individual Differences in Maternal Style
Fairbanks, L. A. (1996) · Advances in the study of behavior · doi:10.1016/s0065-3454(08)60343-5 · Cited by 278 · see citing works
Fetal growth and placental function
Bauer, M. K., Harding, J. E., Bassett, N. S., Breier, B. H., Oliver, M. H., Gallaher, B. W., Evans, P. C., Woodall, S., & Gluckman, P. D. (1998) · Molecular and Cellular Endocrinology · doi:10.1016/s0303-7207(98)00039-2 · Cited by 231 · see citing works
Haapasalo, J., & Tremblay, R. E. (1994) · Journal of Consulting and Clinical Psychology · doi:10.1037/0022-006x.62.5.1044 · Cited by 215 · see citing works
Abuse of pregnant women and adverse birth outcome. Current knowledge and implications for practice
Newberger, E. H. (1992) · JAMA · doi:10.1001/jama.267.17.2370 · Cited by 211 · see citing works
Maternal behavior of SHR rats and its relationship to offspring blood pressures
Myers, M. M., Brunelli, S. A., Squire, J. M., Shindeldecker, R. D., & Hofer, M. A. (1989) · Developmental Psychobiology · doi:10.1002/dev.420220104 · Cited by 195 · see citing works
10 Inducible Defenses in Cladocera: Constraints, Costs, and Multipredator Environments
Tollrian, R., & Dodson, S. I. (1999) · Princeton University Press eBooks · doi:10.1515/9780691228198-013 · Cited by 193 · see citing works
HIRSHFELD, D. R., Biederman, J., Brody, L. R., Faraone, S. V., & Rosenbaum, J. F. (1997) · Journal of the American Academy of Child & Adolescent Psychiatry · doi:10.1097/00004583-199707000-00012 · Cited by 189 · see citing works
Mother Nature: A History of Mothers, Infants, and Natural Selection
Maestripieri, D. (2000) · Animal Behaviour · doi:10.1006/anbe.1999.1378 · Cited by 163 · see citing works
The ecology and evolution of inducible defenses
Dodson, S. I. (1999) · Limnology and Oceanography · doi:10.4319/lo.1999.44.6.1597 · Cited by 158 · see citing works
Are There Any Successful Men from Criminogenic Backgrounds?
Farrington, D. P., Gallagher, B., Morley, L., Ledger, R. J. S., & West, D. J. (1988) · Psychiatry · doi:10.1080/00332747.1988.11024387 · Cited by 154 · see citing works
Coplan, J. D., Trost, R. C., Owens, M. J., Cooper, T. B., Gorman, J. M., Nemeroff, C. B., & Rosenblum, L. A. (1998) · Archives of General Psychiatry · doi:10.1001/archpsyc.55.5.473 · Cited by 145 · see citing works
Influences of environmental demand on maternal behavior and infant development
Rosenblum, L. A., & Andrews, M. W. (1994) · Acta Paediatrica · doi:10.1111/j.1651-2227.1994.tb13266.x · Cited by 144 · see citing works
Consequences of physical abuse and neglect in children
Ammerman, R. T., Cassisi, J. E., Hersen, M., & Hasselt, V. B. V. (1986) · Clinical Psychology Review · doi:10.1016/0272-7358(86)90003-6 · 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
Fride, E., Dan, Y., Gavish, M., & Weinstock, M. (1985) · Life Sciences · doi:10.1016/0024-3205(85)90306-6 · Cited by 129 · see citing works
HIRSHFELD, D. R., Biederman, J., Brody, L. R., Faraone, S. V., & Rosenbaum, J. F. (1997) · Journal of the American Academy of Child & Adolescent Psychiatry · doi:10.1097/00004583-199702000-00011 · Cited by 122 · 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
Factors influencing maternal responsiveness in humans: Usefulness of an animal model
Fleming, A. J. (1988) · Psychoneuroendocrinology · doi:10.1016/0306-4530(88)90014-5 · Cited by 106 · see citing works
Neural basis of maternal behavior in the rat
Numan, M. J. (1988) · Psychoneuroendocrinology · doi:10.1016/0306-4530(88)90006-6 · Cited by 104 · see citing works
Kinsley, C. H. (1988) · Hormones and Behavior · doi:10.1016/0018-506x(88)90032-3 · Cited by 72 · 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
Fleming, A. S. (1986) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1986.tb28015.x · Cited by 58 · see citing works
The Role Of Environmental Variation In Parental Effects Expression
Rossiter, M. (1998) · doi:10.1093/oso/9780195111637.003.0008 · Cited by 53 · see citing works
ABUSE OF PREGNANT WOMEN AND ADVERSE BIRTH OUTCOME
Newberger, E. H., Barkan, S. E., & Lieberman, E. S. (1992) · Cited by 47 · see citing works
Maternal Contributions to Mammalian Reproductive Development and the Divergence of Males and Females
Moore, C. (1995) · Advances in the study of behavior · doi:10.1016/s0065-3454(08)60392-7 · Cited by 44 · see citing works
Temperament, social competence, and adrenocortical activity in preschoolers
Gunnar, M. R., Tout, K., de Haan, M., Pierce, S., & Stanbury, K. (1997) · Developmental Psychobiology · doi:10.1002/(sici)1098-2302(199707)31:1
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Plotsky, P. M., Thrivikraman, K. V., Nemeroff, C. B., Caldji, C., Sharma, S., & Meaney, M. J. (2005) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300769 · Cited by 522 · see citing works
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Barrett, J., & Fleming, A. S. (2011) · Journal of Child Psychology and Psychiatry · doi:10.1111/j.1469-7610.2010.02306.x · Cited by 433 · see citing works
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Pryce, C. R., Rüedi‐Bettschen, D., Dettling, A. C., Weston, A. A., Russig, H. D., Ferger, B., & Feldon, J. (2005) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2005.03.011 · Cited by 414 · see citing works
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Ivy, A. S., Brunson, K. L., Sandman, C., & Baram, T. Z. (2008) · Neuroscience · doi:10.1016/j.neuroscience.2008.04.019 · Cited by 407 · see citing works
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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 296 · see citing works
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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 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 292 · see citing works
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 · see citing works
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 273 · 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
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 269 · see citing works
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 · see citing works
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 237 · see citing works
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 260 · see citing works
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 · see citing works
Curley, J. P., & Champagne, F. A. (2015) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2015.11.001 · Cited by 257 · see citing works
Macrı̀, S., & Würbel, H. (2006) · Hormones and Behavior · doi:10.1016/j.yhbeh.2006.06.015 · Cited by 253 · see citing works
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 · see citing works
Weaver, I. C. G. (2007) · Epigenetics · doi:10.4161/epi.2.1.3881 · Cited by 239 · see citing works
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 · see citing works
Caldji, C., Diorio, J. C., & Meaney, M. J. (2003) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300237 · Cited by 241 · see citing works
Macrı̀, S., Mason, G. J., & Würbel, H. (2004) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2004.03541.x · Cited by 240 · see citing works
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 · see citing works
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 · see citing works
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 227 · see citing works
Plasticity, Robustness, Development and Evolution
(2012) · International Journal of Epidemiology · doi:10.1093/ije/dys033 · Cited by 223 · see citing works
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 · see citing works
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 217 · see citing works
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 213 · see citing works
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 209 · 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
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 · see citing works
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 200 · see citing works
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 · see citing works
Braun, T., Challis, J. R., Newnham, J. P., & Sloboda, D. M. (2013) · Endocrine Reviews · doi:10.1210/er.2013-1012 · Cited by 196 · see citing works
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 · see citing works
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 195 · see citing works
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 · see citing works
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 188 · see citing works
Behavior genetics and postgenomics
Charney, E. (2012) · Behavioral and Brain Sciences · doi:10.1017/s0140525x11002226 · Cited by 207 · see citing works
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 · see citing works
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 193 · see citing works
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 185 · see citing works
Vinall, J., Pavlova, M., Asmundson, G. J. G., Rasic, N. F., & Noel, M. E. (2016) · Children · doi:10.3390/children3040040 · Cited by 186 · see citing works
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 180 · see citing works
Hypothalamic‐Pituitary‐Adrenal (HPA) Axis and Aging
Gupta, D., & Morley, J. E. (2014) · Comprehensive physiology · doi:10.1002/cphy.c130049 · Cited by 196 · see citing works
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 · 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
Epigenetic Inheritance of Disease and Disease Risk
Bohacek, J., & Mansuy, I. M. (2012) · Neuropsychopharmacology · doi:10.1038/npp.2012.110 · Cited by 176 · see citing works
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 · see citing works
Beyond the Stress Concept: Allostatic Load—A Developmental Biological and Cognitive Perspective
Lupien, S., Ouellet-Morin, I., Hupbach, A., Tu, M., Buss, C., Walker, D., Pruessner, J., & McEwen, B. (2015) · Wiley eBooks · doi:10.1002/9780470939390.ch14 · Cited by 149 · see citing works
- 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
- Social Sciences › Psychology › Social Psychology › 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
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