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Naturally occurring variations in maternal behavior in the rat are associated with differences in estrogen-inducible central oxytocin receptors
Open accessAbstract
Naturally occurring variations in maternal licking/grooming influence neural development and are transmitted from mother to female offspring. We found that the induction of maternal behavior in virgin females through constant exposure to pups (pup sensitization) was significantly shorter in the offspring of High compared with Low licking/grooming mothers, suggesting differences in maternal responsivity. In randomly selected females screened for individual differences in maternal responsivity and subsequently mated, there was a significant and negative correlation (r = -0.73) between the latency to exhibit maternal behavior in the pup sensitization paradigm and the frequency of pup licking/grooming during lactation. Females that were more maternally responsive to pups and that showed increased levels of pup licking/grooming also showed significantly higher oxytocin receptor levels in the medial preoptic area, the lateral septum, the central nucleus (n.) of the amygdala, the paraventricular n. of the hypothalamus, and the bed n. of the stria terminalis. Intracerebroventricular administration of an oxytocin receptor antagonist to mothers on postpartum day 3 completely eliminated the differences in pup licking/grooming, suggesting that differences in oxytocin receptor levels are functionally related to maternal behavior. Finally, estrogen treatment of virgin females significantly increased oxytocin receptor binding in the medial preoptic area and lateral septum of female offspring of High, but not Low, licking/grooming mothers. These findings suggest that maternal licking/grooming influences the development of estrogen sensitivity in brain regions that regulate maternal behavior, providing a potential mechanism for the intergenerational transmission of individual differences in maternal behavior.
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“research in mammals showed that more touch and contact increased OT receptor density (Champagne et al., 2001).”
From Oxytocin during the initial stages of romantic attachment: Relations to couples’ interactive reciprocity (2012) · cites this paper as Champagne et al., 2001
Experimental — accuracy not yet measuredThe cited source says what the claim attributes to it.
In the citing paper
“recent evidence suggests that the oxytocinergic system that is involved in caregiving behavior (Bartels & Zeki, 2004; Champagne, Diorio, Sharma, & Meaney, 2001) also enhances social awareness.”
From A developmental, mentalization-based approach to the understanding and treatment of borderline personality disorder (2009) · cites this paper as Champagne, Diorio, Sharma, & Meaney, 2001
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In the citing paper
“Specifically, maternal licking and grooming (LG), a form of tactile stimulation and affiliative care, is related to oxytocin receptor levels such that mothers who demonstrated higher LG have significantly higher receptor oxytocin levels.”
From The evolved nest, oxytocin functioning, and prosocial development (2023) · cites this paper as Champagne et al. (2001)
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In the citing paper
“For example, variations in maternal care are associated with differences in oxytocin receptor levels in the rat (Champagne et al., 2001).”
From The evolved nest, oxytocin functioning, and prosocial development (2023) · cites this paper as Champagne et al. (2001)
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In the citing paper
“In a separate study, OTKO mice housed in a social semi-natural environment were significantly more likely to display infanticidal behavior than wild-type mice in the same environment [20].”
From Oxytocin and the Neural Mechanisms Regulating Social Cognition and Affiliative Behavior (2009) · cites this paper as [20]
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In the citing paper
“Early expression of maternal behavior in virgin rodents is correlated with OTR density in the NAC shell, the lateral septum (LS) and parts of the extended amygdala, all regions implicated in pair bonding and in the regulation of motivated behaviors (Champagne et al 2001; Sheehan et al 2004; Olazabal and Young 2006b; Modi and Young 2011).”
From The behavioral, anatomical and pharmacological parallels between social attachment, love and addiction (2012) · cites this paper as Champagne et al 2001
In the citing paper
“For instance, maternal licking and grooming of rat pups during the postpartum period has been associated with greater OT receptor binding or increased activity in brain areas critical for the development of parenting in mammals, including the medial preoptic area, lateral septum, the paraventricular nucleus of the hypothalamus, and the nucleus accumbens (13–16).”
From Oxytocin and the development of parenting in humans (2010) · cites this paper as [13]
In the citing paper
“The links between maternal OT and maternal affectionate contact are consistent with studies in animal models (13,14,47) that pointed to the involvement of central OT in regulating the degree of “licking-and-grooming” maternal behaviors in female rats.”
From Oxytocin and the development of parenting in humans (2010) · cites this paper as [13]
In the citing paper
“In highly social animals, these ancestral functions of OT have been co-opted to serve social functions, such as promoting maternal behavior (Champagne et al., 2001; Pedersen et al., 1982), fostering pair-bonding and affiliative behaviors (Cushing and Carter, 2000; Smith et al., 2010; Snowdon et al., 2010; Young and Wang, 2004), encouraging in-group bias (Dreu et al., 2010), reducing social vigil”
From Oxytocin and social cognition in rhesus macaques: Implications for understanding and treating human psychopathology (2014) · cites this paper as Champagne et al., 2001
In the citing paper
“Among high ‘licking and grooming’ (i.e. maternal caregiving) female dams, significantly higher levels of OT receptors were also seen in brain regions implicated in the expression of maternal behavior across species, during pregnancy, at parturition and when nursing pups, such as the central nucleus of the amygdala and the paraventricular nucleus of the hypothalamus (Champagne et al., 2001).”
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., 2001
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., 2001
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Citations
Cites
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Self-citationNongenomic Transmission Across Generations of Maternal Behavior and Stress Responses in the Rat
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Self-citationMaternal care, hippocampal synaptogenesis and cognitive development in rats
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Oxytocin induces maternal behavior in virgin female rats
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Research works printed but not linked: 3
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Filippa, M., Monaci, M. G., Spagnuolo, C., Serravalle, P., Daniele, R., & Grandjean, D. (2021) · Scientific Reports · doi:10.1038/s41598-021-96840-4 · Cited by 71
Oxytocin in the medial preoptic area facilitates male sexual behavior in the rat
Gil, M., Bhatt, R., Picotte, K. B., & Hull, E. M. (2011) · Hormones and Behavior · doi:10.1016/j.yhbeh.2010.12.012 · Cited by 70
“In female rats, there is a positive relationship between OTR binding in the MPOA and maternal licking and grooming and responsivity to pups (Champagne et al., 2001; Francis et al., 2000).”
Schneider-Hassloff, H., Straube, B., Jansen, A., Nuscheler, B., Wemken, G., Witt, S. H., Rietschel, M., & Kircher, T. (2016) · NeuroImage · doi:10.1016/j.neuroimage.2016.04.009 · Cited by 71
Sex, love and oxytocin: Two metaphors and a molecule
Carter, C. S. (2022) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2022.104948 · Cited by 70
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Dölen, G. (2015) · Journal of Neuroendocrinology · doi:10.1111/jne.12284 · Cited by 65
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Self-citationMaternal touch predicts social orienting in young children
Reece, C., Ebstein, R., Cheng, X., Ng, T., & Schirmer, A. (2016) · Cognitive Development · doi:10.1016/j.cogdev.2016.05.001 · Cited by 51
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Fineberg, S. K., & Ross, D. A. (2017) · Biological Psychiatry · doi:10.1016/j.biopsych.2016.11.004 · Cited by 40
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Tarsha, M. S., & Narvaez, D. (2023) · Frontiers in Psychology · doi:10.3389/fpsyg.2023.1113944 · Cited by 25
Perry, A. N., Paramadilok, A., & Cushing, B. S. (2009) · Behavioural Brain Research · doi:10.1016/j.bbr.2009.08.021 · Cited by 26
Boschen, K. E., Keller, S. M., Roth, T. L., & Klintsova, A. Y. (2018) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2017.12.009 · Cited by 24
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Early experience and the developmental programming of oxytocin and vasopressin
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Metadata
- Authors
- Champagne, F., Diorio, J., Sharma, S., & Meaney, M. J.
- Affiliations
- Douglas Mental Health University Institute (CA)
- Corresponding author
- Meaney, Michael J.
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2001-10-16
- Volume
- 98
- Issue
- 22
- Pages
- 12736-12741
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC60123
- OpenAlex
- W2056856182
- Cited by
- 707
- References
- 41
- Citations by year
- 2026: 16 · 2025: 16 · 2024: 28 · 2023: 24 · 2022: 26 · 2021: 29 · 2020: 53 · 2019: 32 · 2018: 32 · 2017: 35 · 2016: 44 · 2015: 46 · 2014: 41 · 2013: 42 · 2012: 37
- FWCI
- 13.18
- Type
- journal article
- Language
- en
- Open access
- green
- europepmc.org
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (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 › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Keywords
- maternal behavior, oxytocin receptor, estrogen sensitivity, intergenerational transmission, maternal responsiveness, medial preoptic area, lateral septum, amygdala, paraventricular nucleus, bed nucleus of the stria terminalis, oxytocin receptor antagonist, individual differences, rats
- MeSH terms
- Animals, Autoradiography, Brain, Estrogens, Female, Grooming, Maternal Behavior, Receptors, Oxytocin, Rats, Long-Evans, Rats
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