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Neurobiology of Maternal Stress: Role of Social Rank and Central Oxytocin in Hypothalamic-Pituitary Adrenal Axis Modulation.

Coplan JD, Karim A, Chandra P, St Germain G, Abdallah CG, Altemus M - Front Psychiatry (2015)

Bottom Line: Post-VFD maternal plasma cortisol and CSF OT were compared to corresponding measures in non-VFD-exposed mothers.Pairing of maternal social rank to dyadic distance in VFD presumably reduces maternal contingent responsivity, with ensuing long-term sequelae.VFD-exposure dichotomizes maternal HPA-axis response as a function of social rank with relatively reduced cortisol in subordinates.

View Article: PubMed Central - PubMed

Affiliation: Department of Psychiatry and Behavioral Sciences, Nonhuman Primate Facility, State University of New York Downstate Medical Center , Brooklyn, NY , USA.

ABSTRACT

Background: Chronic stress may conceivably require plasticity of maternal physiology and behavior to cope with the conflicting primary demands of infant rearing and foraging for food. In addition, social rank may play a pivotal role in mandating divergent homeostatic adaptations in cohesive social groups. We examined cerebrospinal fluid (CSF) oxytocin (OT) levels and hypothalamic-pituitary adrenal (HPA) axis regulation in the context of maternal social stress and assessed the contribution of social rank to dyadic distance as reflective of distraction from normative maternal-infant interaction.

Methods: Twelve socially housed mother-infant bonnet macaque dyads were studied after variable foraging demand (VFD) exposure compared to 11 unstressed dyads. Dyadic distance was determined by behavioral observation. Social ranking was performed blindly by two observers. Post-VFD maternal plasma cortisol and CSF OT were compared to corresponding measures in non-VFD-exposed mothers.

Results: High-social rank was associated with increased dyadic distance only in VFD-exposed dyads and not in control dyads. In mothers unexposed to VFD, social rank was not related to maternal cortisol levels, whereas VFD-exposed dominant versus subordinate mothers exhibited increased plasma cortisol. Maternal CSF OT directly predicted maternal cortisol only in VFD-exposed mothers. CSF OT was higher in dominant versus subordinate mothers. VFD-exposed mothers with "high" cortisol specifically exhibited CSF OT elevations in comparison to control groups.

Conclusion: Pairing of maternal social rank to dyadic distance in VFD presumably reduces maternal contingent responsivity, with ensuing long-term sequelae. VFD-exposure dichotomizes maternal HPA-axis response as a function of social rank with relatively reduced cortisol in subordinates. OT may serve as a homeostatic buffer during maternal stress exposure.

No MeSH data available.


Related in: MedlinePlus

Relationship between maternal–infant proximity as a function of maternal social rank in VFD-exposed versus non-exposed dyads. A general linear model was performed with VFD exposure as the categorical variable, maternal social rank as the predictor variable and maternal–infant dyadic distance as the dependent variable. A significant interactive term of VFD exposure × maternal social rank [F(1; 19) = 11.97; p = 0.003] indicated that predictive effects of social rank on dyadic proximity were specific to VFD mothers with low-social rank predicting decreased dyadic distance (see figure for respective Pearson’s correlations).
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Figure 1: Relationship between maternal–infant proximity as a function of maternal social rank in VFD-exposed versus non-exposed dyads. A general linear model was performed with VFD exposure as the categorical variable, maternal social rank as the predictor variable and maternal–infant dyadic distance as the dependent variable. A significant interactive term of VFD exposure × maternal social rank [F(1; 19) = 11.97; p = 0.003] indicated that predictive effects of social rank on dyadic proximity were specific to VFD mothers with low-social rank predicting decreased dyadic distance (see figure for respective Pearson’s correlations).

Mentions: In the first GLM, we analyzed the effect of social rank as a continuous predictor variable on dyadic distance as a function of maternal stress exposure through assessment of the interactive term (see Figure 1). There was a social rank effect: mothers with relatively high-social rank exhibited increased dyadic-distance relative to subordinate mothers, who exhibited relatively decreased dyadic distance [F(1; 19) = 8.87; p = 0.008]. There was a VFD exposure effect whereby reductions in dyadic distance in the VFD-exposed group were observed in comparison to the non-VFD-exposed group [F(1; 19) = 9.35; p = 0.006]. A marked social rank by VFD exposure interaction was noted [F(1; 19) = 11.97; p = 0.003; effect size: partial η2 = 0.39]. Post hoc Pearson’s correlation revealed that high-social rank predicted greater dyadic distance, and vice-versa, in VFD (r = 0.89, N = 12, p < 0.001; r2 = 79%) and was significantly distinguishable from non-VFD-exposed dyads (Figure 1), where no correlation (r = 0.09, N = 11, p = 0.79) between social rank and dyadic distance was observed. Effects remained significant when covaried for infant age.


Neurobiology of Maternal Stress: Role of Social Rank and Central Oxytocin in Hypothalamic-Pituitary Adrenal Axis Modulation.

Coplan JD, Karim A, Chandra P, St Germain G, Abdallah CG, Altemus M - Front Psychiatry (2015)

Relationship between maternal–infant proximity as a function of maternal social rank in VFD-exposed versus non-exposed dyads. A general linear model was performed with VFD exposure as the categorical variable, maternal social rank as the predictor variable and maternal–infant dyadic distance as the dependent variable. A significant interactive term of VFD exposure × maternal social rank [F(1; 19) = 11.97; p = 0.003] indicated that predictive effects of social rank on dyadic proximity were specific to VFD mothers with low-social rank predicting decreased dyadic distance (see figure for respective Pearson’s correlations).
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4493323&req=5

Figure 1: Relationship between maternal–infant proximity as a function of maternal social rank in VFD-exposed versus non-exposed dyads. A general linear model was performed with VFD exposure as the categorical variable, maternal social rank as the predictor variable and maternal–infant dyadic distance as the dependent variable. A significant interactive term of VFD exposure × maternal social rank [F(1; 19) = 11.97; p = 0.003] indicated that predictive effects of social rank on dyadic proximity were specific to VFD mothers with low-social rank predicting decreased dyadic distance (see figure for respective Pearson’s correlations).
Mentions: In the first GLM, we analyzed the effect of social rank as a continuous predictor variable on dyadic distance as a function of maternal stress exposure through assessment of the interactive term (see Figure 1). There was a social rank effect: mothers with relatively high-social rank exhibited increased dyadic-distance relative to subordinate mothers, who exhibited relatively decreased dyadic distance [F(1; 19) = 8.87; p = 0.008]. There was a VFD exposure effect whereby reductions in dyadic distance in the VFD-exposed group were observed in comparison to the non-VFD-exposed group [F(1; 19) = 9.35; p = 0.006]. A marked social rank by VFD exposure interaction was noted [F(1; 19) = 11.97; p = 0.003; effect size: partial η2 = 0.39]. Post hoc Pearson’s correlation revealed that high-social rank predicted greater dyadic distance, and vice-versa, in VFD (r = 0.89, N = 12, p < 0.001; r2 = 79%) and was significantly distinguishable from non-VFD-exposed dyads (Figure 1), where no correlation (r = 0.09, N = 11, p = 0.79) between social rank and dyadic distance was observed. Effects remained significant when covaried for infant age.

Bottom Line: Post-VFD maternal plasma cortisol and CSF OT were compared to corresponding measures in non-VFD-exposed mothers.Pairing of maternal social rank to dyadic distance in VFD presumably reduces maternal contingent responsivity, with ensuing long-term sequelae.VFD-exposure dichotomizes maternal HPA-axis response as a function of social rank with relatively reduced cortisol in subordinates.

View Article: PubMed Central - PubMed

Affiliation: Department of Psychiatry and Behavioral Sciences, Nonhuman Primate Facility, State University of New York Downstate Medical Center , Brooklyn, NY , USA.

ABSTRACT

Background: Chronic stress may conceivably require plasticity of maternal physiology and behavior to cope with the conflicting primary demands of infant rearing and foraging for food. In addition, social rank may play a pivotal role in mandating divergent homeostatic adaptations in cohesive social groups. We examined cerebrospinal fluid (CSF) oxytocin (OT) levels and hypothalamic-pituitary adrenal (HPA) axis regulation in the context of maternal social stress and assessed the contribution of social rank to dyadic distance as reflective of distraction from normative maternal-infant interaction.

Methods: Twelve socially housed mother-infant bonnet macaque dyads were studied after variable foraging demand (VFD) exposure compared to 11 unstressed dyads. Dyadic distance was determined by behavioral observation. Social ranking was performed blindly by two observers. Post-VFD maternal plasma cortisol and CSF OT were compared to corresponding measures in non-VFD-exposed mothers.

Results: High-social rank was associated with increased dyadic distance only in VFD-exposed dyads and not in control dyads. In mothers unexposed to VFD, social rank was not related to maternal cortisol levels, whereas VFD-exposed dominant versus subordinate mothers exhibited increased plasma cortisol. Maternal CSF OT directly predicted maternal cortisol only in VFD-exposed mothers. CSF OT was higher in dominant versus subordinate mothers. VFD-exposed mothers with "high" cortisol specifically exhibited CSF OT elevations in comparison to control groups.

Conclusion: Pairing of maternal social rank to dyadic distance in VFD presumably reduces maternal contingent responsivity, with ensuing long-term sequelae. VFD-exposure dichotomizes maternal HPA-axis response as a function of social rank with relatively reduced cortisol in subordinates. OT may serve as a homeostatic buffer during maternal stress exposure.

No MeSH data available.


Related in: MedlinePlus