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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 CSF OT concentrations to maternal basal cortisol concentrations as a function of VFD exposure. There was an overall VFD exposure effect with higher maternal plasma cortisol following VFD exposure versus non-exposure, when adjusted for maternal CSF OT [F(1; 17) = 6.03, p = 0.025]. There was an overall OT effect positively predicting maternal cortisol [F(1; 17) = 6.28, p = 0.022]. However, there was a significant VFD exposure × maternal CSF OT interactive effect [F(1; 17) = 6.56, p = 0.02] with OT directly predicting cortisol in VFD-exposed mothers and an absence of relationship in non-VFD-exposed mothers (see figure for respective Pearson’s correlations).
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Figure 2: Relationship between maternal CSF OT concentrations to maternal basal cortisol concentrations as a function of VFD exposure. There was an overall VFD exposure effect with higher maternal plasma cortisol following VFD exposure versus non-exposure, when adjusted for maternal CSF OT [F(1; 17) = 6.03, p = 0.025]. There was an overall OT effect positively predicting maternal cortisol [F(1; 17) = 6.28, p = 0.022]. However, there was a significant VFD exposure × maternal CSF OT interactive effect [F(1; 17) = 6.56, p = 0.02] with OT directly predicting cortisol in VFD-exposed mothers and an absence of relationship in non-VFD-exposed mothers (see figure for respective Pearson’s correlations).

Mentions: In the next GLM, we used maternal plasma cortisol as the dependent variable, VFD exposure as the categorical variable and maternal CSF OT as the independent predictor variable. Consistent with a factorial design, we entered the interactive term of VFD exposure × maternal CSF OT into the GLM. There was an overall VFD exposure effect with higher maternal plasma cortisol following VFD exposure versus non-exposure when adjusted for maternal CSF OT [VFD-exposed mean (SE) = 44.60 (1.55) versus non-VFD-exposed mean (SE) = 42.97 (1.63); F(1; 17) = 6.03, p = 0.025]. There was an overall OT effect positively predicting maternal cortisol [F(1; 17) = 6.28, p = 0.022] and a significant VFD exposure × maternal CSF OT interactive effect [F(1; 17) = 6.56, p = 0.02]. Post hoc Pearson’s correlations revealed a significant positive correlation in VFD-exposed mothers between maternal CSF OT and maternal plasma cortisol (r = 0.78; N = 11, p = 0.004), whereas the corresponding correlation in non-exposed mothers was absent (r = −0.01; N = 10, p = 0.97) (Figure 2). Thus, OT was positively predictive of cortisol although this effect was confined to the VFD-exposed mothers. Two OT values were not available for analysis. Effects remained significant when covarying 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 CSF OT concentrations to maternal basal cortisol concentrations as a function of VFD exposure. There was an overall VFD exposure effect with higher maternal plasma cortisol following VFD exposure versus non-exposure, when adjusted for maternal CSF OT [F(1; 17) = 6.03, p = 0.025]. There was an overall OT effect positively predicting maternal cortisol [F(1; 17) = 6.28, p = 0.022]. However, there was a significant VFD exposure × maternal CSF OT interactive effect [F(1; 17) = 6.56, p = 0.02] with OT directly predicting cortisol in VFD-exposed mothers and an absence of relationship in non-VFD-exposed mothers (see figure for respective Pearson’s correlations).
© Copyright Policy
Related In: Results  -  Collection

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

Figure 2: Relationship between maternal CSF OT concentrations to maternal basal cortisol concentrations as a function of VFD exposure. There was an overall VFD exposure effect with higher maternal plasma cortisol following VFD exposure versus non-exposure, when adjusted for maternal CSF OT [F(1; 17) = 6.03, p = 0.025]. There was an overall OT effect positively predicting maternal cortisol [F(1; 17) = 6.28, p = 0.022]. However, there was a significant VFD exposure × maternal CSF OT interactive effect [F(1; 17) = 6.56, p = 0.02] with OT directly predicting cortisol in VFD-exposed mothers and an absence of relationship in non-VFD-exposed mothers (see figure for respective Pearson’s correlations).
Mentions: In the next GLM, we used maternal plasma cortisol as the dependent variable, VFD exposure as the categorical variable and maternal CSF OT as the independent predictor variable. Consistent with a factorial design, we entered the interactive term of VFD exposure × maternal CSF OT into the GLM. There was an overall VFD exposure effect with higher maternal plasma cortisol following VFD exposure versus non-exposure when adjusted for maternal CSF OT [VFD-exposed mean (SE) = 44.60 (1.55) versus non-VFD-exposed mean (SE) = 42.97 (1.63); F(1; 17) = 6.03, p = 0.025]. There was an overall OT effect positively predicting maternal cortisol [F(1; 17) = 6.28, p = 0.022] and a significant VFD exposure × maternal CSF OT interactive effect [F(1; 17) = 6.56, p = 0.02]. Post hoc Pearson’s correlations revealed a significant positive correlation in VFD-exposed mothers between maternal CSF OT and maternal plasma cortisol (r = 0.78; N = 11, p = 0.004), whereas the corresponding correlation in non-exposed mothers was absent (r = −0.01; N = 10, p = 0.97) (Figure 2). Thus, OT was positively predictive of cortisol although this effect was confined to the VFD-exposed mothers. Two OT values were not available for analysis. Effects remained significant when covarying 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