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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In mammals, more touch and contact increased oxytocin receptor density.
“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
The Results report that rat mothers with more pup licking/grooming had higher oxytocin receptor binding in several brain regions, but found no group difference in time spent in physical contact with pups. The Discussion describes an association and suggests that receptor differences may help drive licking/grooming; it does not show that more touch or contact caused receptor density to increase. (LLM, conf=0.87)
Experimental — accuracy not yet measuredThe oxytocinergic system involved in caregiving behavior also enhances social awareness.
“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
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.
“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)
Variations in maternal care are associated with differences in oxytocin receptor levels in the rat.
“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)
OTKO mice housed in a social semi-natural environment are significantly more likely to display infanticidal behavior than wild-type mice in the same environment.
“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]
The Materials and Methods (page unavailable) identify the animals as Long–Evans rats, and the Results concern maternal licking/grooming and oxytocin receptor antagonism. Searches for OTKO mice, semi-natural housing, and infanticide found no passage addressing the claimed comparison with wild-type mice. (LLM, conf=0.78)
Experimental — accuracy not yet measured
Early expression of maternal behavior in virgin rodents correlates with OTR density in the NAC shell, lateral septum, and parts of the extended amygdala.
“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
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.
“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]
The links between maternal OT and maternal affectionate contact are consistent with studies in animal models that pointed to the involvement of central OT in regulating the degree of "licking-and-grooming" maternal behaviors in female rats.
“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 highly social animals, ancestral functions of OT have been co-opted to serve social functions, such as promoting maternal behavior, pair-bonding, affiliative behaviors, in-group bias, reducing social vigilance, and amplifying other-regarding behaviors.
“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
Among high licking and grooming female dams, significantly higher levels of OT receptors were seen in brain regions implicated in maternal behavior across species, during pregnancy, at parturition, and when nursing pups, such as central nucleus of amygdala and paraventricular nucleus of hypothalamus (Champagne et al., 2001).
“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
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., 2001
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“It has long been observed in animal models that both the septal nuclei and the mesolimbic dopamine pathway are implicated in motivating proactive offspring nurture (Champagne et al., 2001).”
DNA methylation and childhood maltreatment: From animal models to human studies
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Both oxytocin and vasopressin may influence alloparental behavior in male prairie voles
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Consequences of Early Experiences and Exposure to Oxytocin and Vasopressin Are Sexually Dimorphic
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Natural variations in postpartum maternal care in inbred and outbred mice
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The brain-body disconnect: A somatic sensory basis for trauma-related disorders
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“Increased receptor levels for oxytocin are reported with repeated provision of tactile-rich grooming stimuli in young rats (Francis et al., 2000; Champagne et al., 2001).”
BackgroundTesticular volume is inversely correlated with nurturing-related brain activity in human fathers
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Oxytocin׳s role in anxiety: A critical appraisal
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Developmental experiences and the oxytocin receptor system
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Dissecting the Role of Oxytocin in the Formation and Loss of Social Relationships
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Oxytocin, vasopressin, and the motivational forces that drive social behaviors
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Autism and Oxytocin: New Developments in Translational Approaches to Therapeutics
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Oxytocin and Estrogen Receptor β in the Brain: An Overview
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- 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
- Social Sciences › Psychology › Social Psychology › 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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