Within‐litter variance in early rat pup–mother interactions and adult offspring responses to novelty

Ragan, Christina M.; Loken, Eric; Stifter, Cynthia A.; Cavigelli, Sonia A.

doi:10.1002/dev.20581

Cited by 16 publications

(35 citation statements)

References 52 publications

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“…These opposite patterns of prediction by care reliability and quantity can be reconciled because mothers who showed higher average care behavior happened to have provided their care with lower day-today reliability (i.e., a negative association between the quantity and the reliability of postdisturbance of maternal care). Lack of association between greater maternal care and offspring body weight is also consistent with other studies supporting the general notion that higher maternal care quantity does not always lead to beneficial effects (46,47).…”

Section: Distinct Contributions From Maternal Physiology and Maternalsupporting

confidence: 89%

Maternal modulation of novelty effects on physical development

Tang

Yang²,

Reeb‐Sutherland³

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

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Familiarity to the mother and the novelty afforded by the postnatal environment are two contrasting sources of neonatal influence. One hypothesis regarding their relationship is the maternal modulation hypothesis, which predicts that the same neonatal stimulation may have different effects depending on the maternal context. Here we tested this hypothesis using physical development, indexed by body weight, as an endpoint and found that, among offspring of mothers with a high initial swim-stress-induced corticosterone (CORT) response, neonatal novelty exposure induced an enhancement in early growth, and among offspring with mothers of a low initial CORT response, the same neonatal stimulation induced an impairment. At an older age, a novelty-induced increase in body weight was also found among offspring of mothers with high postnatal care reliability and a novelty-induced reduction found among offspring of mothers with low care reliability. These results support a maternal modulation of early stimulation effects on physical development and demonstrate that the maternal influence originates from multiple instead of any singular sources. These results (i) significantly extend the findings of maternal modulation from the domain of cognitive development to the domain of physical development; (ii) offer a unifying explanation for a previously inconsistent literature regarding early stimulation effects on body weight; and (iii) highlight the notion that the early experience effect involves no causal primacy but higher order interactions among the initial triggering events and subsequent events involving a multitude of maternal and nonmaternal influences.maternal stress | maternal care | maternal mediation | developmental plasticity | growth enhancement I t seems self-evident that, for a developing infant, both the maternal and nonmaternal environment affects his or her development. Over the past century, ample evidence from both human and animal early-experience studies has confirmed this intuition (1-3). What remains challenging is how these two environmental sources interact to jointly influence offspring development (4-7). Emerging from the rodent developmental literature are two alternative views regarding the relation between maternal and nonmaternal influences. The "maternal mediation view" assumes that nonmaternal environment exerts its effect indirectly through its effect on the mother, who in turn affects the offspring (e.g., see refs. 8 and 9). When taken to the extreme, this view would directly contradict the stress-activation hypothesis (10, 11), which states that the nonmaternal environment has a direct effect on the offspring by activating some aspects of the offspring's hypothalamic-pituitary-adrenal (HPA) function. In contrast, the "maternal modulation view" incorporates the stressactivation hypothesis and assumes that the nonmaternal environment first activates aspects of the HPA axis, and the mother then modulates this effect (12). According to the latter view, the individual mother sets distinct conte...

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Section: Distinct Contributions From Maternal Physiology and Maternalsupporting

confidence: 89%

Maternal modulation of novelty effects on physical development

Tang

Yang²,

Reeb‐Sutherland³

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

View full text Add to dashboard Cite

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“…Harding, J.S. Lonstein 6 strains and in laboratory mice Pan et al, 2014;Ragan et al, 2012;Ragan et al 2010;van Hasselt et al, 2012a,b). We then examined if this variability in maternal care received was associated with some relevant physical characteristics of the pups and their display of maternal solicitation behaviors.…”

Section: Accepted Manuscriptmentioning

confidence: 92%

“…Indeed, Ragan and Cavigelli have reported that the withinlitter differences in maternal licking received by rat and mouse pups are of the same magnitude as those found between litters, with the highest-licked pups receiving up to three times as many licking bouts as their lowest-licked siblings Ragan et al, 2010;Ragan et al, 2012). For daughters, the consequences of such differences include that the highest-licked sisters are more neophobic (Ragan et al, 2012) yet have lower basal plasma corticosterone than their lower-licked sisters (Ragan et al 2011). Notably, these correlations for the females within litters are in opposite directions of what is found for males when these relationships are compared across litters (Weaver, Diorio, Seckl, Szyf, and Meaney, 2004).…”

Section: Accepted Manuscriptmentioning

confidence: 96%

“…Lonstein 4 (Birnie et al, 2013;Cavigelli et al, 2010;Moore and Power, 1992;Pan et al, 2014;Plotsky and Meaney, 1993;Ragan et al, 2012;Rubin, Cheah, and Fox, 2001;Stanton and Levine, 1990;van Hasselt et al, 2012). Indeed, Ragan and Cavigelli have reported that the withinlitter differences in maternal licking received by rat and mouse pups are of the same magnitude as those found between litters, with the highest-licked pups receiving up to three times as many licking bouts as their lowest-licked siblings Ragan et al, 2010;Ragan et al, 2012). For daughters, the consequences of such differences include that the highest-licked sisters are more neophobic (Ragan et al, 2012) yet have lower basal plasma corticosterone than their lower-licked sisters (Ragan et al 2011).…”

Section: Accepted Manuscriptmentioning

confidence: 97%

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Associations among within-litter differences in early mothering received and later emotional behaviors, mothering, and cortical tryptophan hydroxylase-2 expression in female laboratory rats

Ragan

Harding

Lonstein

2016

Hormones and Behavior

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This article is part of a Special Issue "Parental Care". The effects of differential maternal care received on offspring phenotype in rodents has been extensively studied between litters, but the consequences of differential mothering within litters on offspring neurobehavioral development have been rarely examined. We here investigated how variability in maternal care received among female rat siblings (measured four times daily on postnatal days 4, 6, 8, and 10) relates to the siblings' later emotional and maternal behaviors. As previously reported, we found that some female pups received up to three times more maternal licking bouts compared to their sisters; this difference was positively correlated with the pups' body weights. The number of maternal licking bouts that females received was negatively correlated with their later neophobic behaviors in an open field during periadolescence, but positively correlated with their anxiety-related behavior in an elevated plus maze during adulthood. Licking received was also positively correlated with females' later likelihood to retrieve pups in a maternal sensitization paradigm. In addition, females' neophobia during adolescence and anxiety-related behavior during adulthood predicted some aspects of both postpartum and sensitized maternal responsiveness. Medial prefrontal cortex expression of tryptophan hydroxylase-2 (TPH2; enzyme necessary for serotonin synthesis) was negatively associated with early maternal licking received. Interestingly, cortical TPH2 was positively associated with the maternal responsiveness of sensitized virgins but negatively associated with it in postpartum females. These results indicate that within-litter differences in maternal care received is an often neglected, but important, contributor to individual differences in offspring socioemotional behaviors as well as to the cortical serotonin neurochemistry that may influence these behaviors.

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“…Differences in the socio-emotional development of two siblings within a family have been explained by non-shared family environmental factors such as birth order, peer relations, and differential parenting (Knafo et al 2011;Ragan et al 2012). When children have younger brothers or sisters, they are not only exposed to parenting directed towards themselves, but also to parenting directed towards their siblings.…”

Section: Introductionmentioning

confidence: 99%

Parental Sensitivity Towards Toddlers and Infant Siblings Predicting Toddler Sharing and Compliance

et al. 2014

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Children with younger brothers or sisters are exposed to parenting directed towards themselves as well as parenting directed towards their siblings. We examined the hypothesis that mothers' and fathers' sensitive parenting towards their second-borns predicts compliance and sharing behavior in their firstborns, over and above their parenting towards their firstborns. In a sample of 388 families with a toddler and infant, parental sensitivity, child sharing behavior, and child compliance were observed during two different home visits, one with father and one with mother present. The results showed that toddlers shared more with their younger siblings and showed more compliance when their fathers were more sensitive towards them, but only if fathers showed low sensitivity towards the younger siblings. We suggest two explanations: toddlers may show more positive behavior to ensure continuation of their favored position, or they may compensate for the lack of fathers' sensitivity towards the younger siblings. Our study highlights the importance of the broader family context of parenting for child socio-emotional development.

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Within‐litter variance in early rat pup–mother interactions and adult offspring responses to novelty

Cited by 16 publications

References 52 publications

Maternal modulation of novelty effects on physical development

Maternal modulation of novelty effects on physical development

Associations among within-litter differences in early mothering received and later emotional behaviors, mothering, and cortical tryptophan hydroxylase-2 expression in female laboratory rats

Parental Sensitivity Towards Toddlers and Infant Siblings Predicting Toddler Sharing and Compliance

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