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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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“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
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Azadi, M., Gompf, H. S., & Azizi, H. (2020) · Journal of Psychopharmacology · doi:10.1177/0269881120953993 · Cited by 11
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Hooper, A. W., Berger, R., Rubin, L. S., McDonald, B. I., & Crocker, D. E. (2019) · Animal Behaviour · doi:10.1016/j.anbehav.2019.03.007 · Cited by 12
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Lauby, S. C., Fleming, A. S., & McGowan, P. O. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.04.021 · Cited by 14
Immune deficiency influences juvenile social behavior and maternal behavior.
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Diamantopoulou, A., Raftogianni, A., Stamatakis, A., Oitzl, M. S., & Stylianopoulou, F. (2012) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2012.09.007 · Cited by 12
Wu, R., Song, Z., Tai, F., Wang, L., Kong, L., & Wang, J. (2013) · Behavioural Processes · doi:10.1016/j.beproc.2013.05.008 · Cited by 12
Ugarte, A., Eguibar, J. R., Cortés, C. M. A. C., León‐Chávez, B. A., & Melo, Á. I. (2010) · Developmental Psychobiology · doi:10.1002/dev.20497 · Cited by 14
Vilela, F. C., Ruginsk, S. G., de Melo, C. M., & Giusti‐Paiva, A. (2013) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s00424-013-1238-8 · Cited by 12
Jenkins, S., Harker, A., & Gibb, R. L. (2018) · Neuroscience · doi:10.1016/j.neuroscience.2018.10.023 · Cited by 12
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Fleming, A. S., González, A., Afonso, V. M., & Lovic, V. (2008) · Elsevier eBooks · doi:10.1016/b978-012374285-8.00034-2 · Cited by 12
Rose, C., Röhl, F., Schwegler, H., Hanke, J., & Yilmazer‐Hanke, D. (2006) · Behavior Genetics · doi:10.1007/s10519-005-9037-4 · Cited by 13
Şahin, N. H., Tasso, A. F., & Güler, M. (2023) · Cognitive Processing · doi:10.1007/s10339-023-01144-2 · Cited by 13
Burenkova, O. V., & Grigorenko, E. L. (2024) · Developmental Psychobiology · doi:10.1002/dev.22479 · Cited by 11
Wu, R., Song, Z., Tai, F., An, X., Yu, P., & Li, Y. (2012) · Animal Behaviour · doi:10.1016/j.anbehav.2012.10.007 · Cited by 11
Alves, R. L., Portugal, C. C., Lopes, I. M., Oliveira, P., Alves, C. J., Barbosa, F., Summavielle, T., & Magalhães, A. (2022) · Translational Psychiatry · doi:10.1038/s41398-022-02220-5 · Cited by 18
Hipolito, L. T. M., Batista, T. H., dos Anjos‐Garcia, T., Giusti‐Paiva, A., & Vilela, F. C. (2022) · International Journal of Developmental Neuroscience · doi:10.1002/jdn.10243 · Cited by 9
Rivi, V., Rigillo, G., Toscano, Y., Benatti, C., & Blom, J. M. C. (2023) · Children · doi:10.3390/children10071217 · Cited by 14
Garoflos, E., Stamatakis, A., Pondiki, S., Apostolou, A., Philippidis, H., & Stylianopoulou, F. (2007) · Neuroscience · doi:10.1016/j.neuroscience.2007.06.020 · Cited by 11
Chidgey, K. L., Morel, P. C. H., Stafford, K. J., & Barugh, I. W. (2016) · Livestock Science · doi:10.1016/j.livsci.2016.09.011 · Cited by 11
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Espitia-Pérez, P., Albino, S. M., Espitia-Pérez, L., Brango, H., da Rosa, H. T., Silveira, A. K., de Moraes, D. P., Cerveira, C., Mingori, M. R., Ribeiro, C. T., et al. (2018) · NeuroToxicology · doi:10.1016/j.neuro.2018.10.004 · Cited by 12
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Raymann, S., Schalbetter, S. M., Schaer, R., Bernhardt, A. C., Mueller, F. S., Meyer, U., & Weber‐Stadlbauer, U. (2022) · Cerebral Cortex · doi:10.1093/cercor/bhac207 · Cited by 10
Myers, A. M., Bowen, S. E., & Brummelte, S. (2023) · Developmental Psychobiology · doi:10.1002/dev.22433 · Cited by 10
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Raftogianni, A., Stamatakis, A., Papadopoulou, A., Vougas, K. N., Anagnostopoulos, A. K., Stylianopoulou, F., & Tsangaris, G. T. (2012) · PLoS ONE · doi:10.1371/journal.pone.0048337 · Cited by 10
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Silveira, J. S., Júnior, O. V. R., Schmitz, F., Ferreira, F. S., Rodrigues, F. C., Coutinho‐Silva, R., Savio, L. E. B., & Wyse, Â. T. D. S. (2022) · Molecular Neurobiology · doi:10.1007/s12035-022-02724-7 · Cited by 13
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Unternäehrer, E., Cost, K. T., Jonas, W., Dhir, S. K., Bouvette–Turcot, A., Gaudreau, H., Dass, S. A. H., Lydon, J. E., Steiner, M. S., Szatmári, P., et al. (2019) · Human Nature · doi:10.1007/s12110-019-09355-3 · Cited by 9
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Lauby, S. C., Lapp, H. E., Leija‐Salazar, M., Semyrenko, S., Chauhan, D., Margolis, A. E., & Champagne, F. A. (2024) · PLoS ONE · doi:10.1371/journal.pone.0305256 · Cited by 8
Kougias, D. G., Atillasoy, E. O., Southall, M. D., Scialli, A. R., Ejaz, S., Chu, C. S., Jeminiwa, B. O., Massarsky, A., Unice, K. M., Schaeffer, T. H., et al. (2025) · Critical Reviews in Toxicology · doi:10.1080/10408444.2024.2442344 · Cited by 8
Rullo, L., Losapio, L. M., Morosini, C., Mottarlini, F., Schiavi, S., Buzzelli, V., Ascone, F., Ciccocioppo, R., Fattore, L., Caffino, L., et al. (2023) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2023.1270195 · Cited by 8
James, L. S., Fan, R., & Sakata, J. T. (2019) · Journal of Experimental Biology · doi:10.1242/jeb.206318 · Cited by 7
Perinatal exposure to omega-3 fatty acid imbalance leads to early behavioral alterations in rat pups
Colucci, P., Castro, V. D., Peloso, A., Splendori, M., Trezza, V., & Campolongo, P. (2020) · Behavioural Brain Research · doi:10.1016/j.bbr.2020.112723 · Cited by 7
Ferroni, N. M., Berardino, B. G., Belluscio, L. M., Fernández, M. S., Fesser, E. A., Sonzogni, S. V., & Cánepa, E. T. (2020) · Nutritional Neuroscience · doi:10.1080/1028415x.2020.1829343 · Cited by 7
Manoni, G., Puzzo, C., Gigantesco, A., & Adriani, W. (2022) · Brain Sciences · doi:10.3390/brainsci12040469 · Cited by 7
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
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