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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 and effect sizes among maternal variables exposed to variable foraging demand versus unstressed control mothers. The figure schematizes the effect of VFD exposure versus controls as described by the effect size of the interactive effect of VFD exposure × predictor variable (line inception) in the prediction of the dependent variable (arrow point) except for those effect sizes denoted by an asterisk (where no group effects were evident). Directional arrows in front of each variable are all in an upward direction and at the rear of each variable are all in a downward direction indicating a direct relationship for all variables studied in VFD-exposed mothers versus control mothers (except those relationships that are designated by an asterisk). a = social rank by VFD exposure interaction predicting dyadic distance [F(1; 19) = 11.97; p = 0.003]. b = hierarchical status by VFD exposure effect in the prediction of maternal cortisol concentrations [F(1; 19) = 5.52; p = 0.030] (dominants exhibited higher cortisol than subordinates). c = maternal weight by VFD exposure interaction in the prediction of maternal cortisol concentrations [F(1; 19) = 29.53; p = 0.0001]. *d = greater body weight predicted greater maternal dominance [F(1; 19) = 6.88; p = 0.017] without interactive effect. e = VFD exposure × maternal CSF OT interactive effect in the prediction of maternal cortisol concentrations [F(1; 17) = 6.56, p = 0.02]. *f = dominant mothers exhibited greater CSF OT concentrations than subordinate mothers [F(1; 17) = 6.45; p = 0.021] without interactive effect. Partial η2: large effect size ≥ 0.14. Note, except for (d) and (f), all other correlational relationships are significant in VFD-exposed but not non-exposed mothers.
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Figure 5: Relationship and effect sizes among maternal variables exposed to variable foraging demand versus unstressed control mothers. The figure schematizes the effect of VFD exposure versus controls as described by the effect size of the interactive effect of VFD exposure × predictor variable (line inception) in the prediction of the dependent variable (arrow point) except for those effect sizes denoted by an asterisk (where no group effects were evident). Directional arrows in front of each variable are all in an upward direction and at the rear of each variable are all in a downward direction indicating a direct relationship for all variables studied in VFD-exposed mothers versus control mothers (except those relationships that are designated by an asterisk). a = social rank by VFD exposure interaction predicting dyadic distance [F(1; 19) = 11.97; p = 0.003]. b = hierarchical status by VFD exposure effect in the prediction of maternal cortisol concentrations [F(1; 19) = 5.52; p = 0.030] (dominants exhibited higher cortisol than subordinates). c = maternal weight by VFD exposure interaction in the prediction of maternal cortisol concentrations [F(1; 19) = 29.53; p = 0.0001]. *d = greater body weight predicted greater maternal dominance [F(1; 19) = 6.88; p = 0.017] without interactive effect. e = VFD exposure × maternal CSF OT interactive effect in the prediction of maternal cortisol concentrations [F(1; 17) = 6.56, p = 0.02]. *f = dominant mothers exhibited greater CSF OT concentrations than subordinate mothers [F(1; 17) = 6.45; p = 0.021] without interactive effect. Partial η2: large effect size ≥ 0.14. Note, except for (d) and (f), all other correlational relationships are significant in VFD-exposed but not non-exposed mothers.

Mentions: In our attempt to decipher important factors in the transmission of VFD-exposure stress from mothers to their infants, we discovered a complex interaction among maternal social rank, dyadic distance, maternal plasma cortisol, and maternal CSF OT (see Figure 5) with the most salient finding of the current study highlighting the pivotal role of maternal social rank, particularly under VFD-exposure conditions. Clearly, social rank plays a disproportionate role in the context of a perceived shortage of food resources engendered by VFD exposure. Either as a continuous variable, social rank, or as a dichotomous variable, “hierarchical status,” (dominant versus subordinate), the variable significantly predicted among the VFD group, (1) maternal dyadic distance between mother and infant (high rank = increased dyadic distance), (2) maternal plasma cortisol (dominance = high cortisol), and (3) CSF OT directly predicts plasma cortisol but specifically in VFD exposure (upon VFD exposure, high OT predicts high cortisol). Among both VFD and non-VFD groups, social rank predicts CSF OT levels (dominance = increased CSF OT).


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 and effect sizes among maternal variables exposed to variable foraging demand versus unstressed control mothers. The figure schematizes the effect of VFD exposure versus controls as described by the effect size of the interactive effect of VFD exposure × predictor variable (line inception) in the prediction of the dependent variable (arrow point) except for those effect sizes denoted by an asterisk (where no group effects were evident). Directional arrows in front of each variable are all in an upward direction and at the rear of each variable are all in a downward direction indicating a direct relationship for all variables studied in VFD-exposed mothers versus control mothers (except those relationships that are designated by an asterisk). a = social rank by VFD exposure interaction predicting dyadic distance [F(1; 19) = 11.97; p = 0.003]. b = hierarchical status by VFD exposure effect in the prediction of maternal cortisol concentrations [F(1; 19) = 5.52; p = 0.030] (dominants exhibited higher cortisol than subordinates). c = maternal weight by VFD exposure interaction in the prediction of maternal cortisol concentrations [F(1; 19) = 29.53; p = 0.0001]. *d = greater body weight predicted greater maternal dominance [F(1; 19) = 6.88; p = 0.017] without interactive effect. e = VFD exposure × maternal CSF OT interactive effect in the prediction of maternal cortisol concentrations [F(1; 17) = 6.56, p = 0.02]. *f = dominant mothers exhibited greater CSF OT concentrations than subordinate mothers [F(1; 17) = 6.45; p = 0.021] without interactive effect. Partial η2: large effect size ≥ 0.14. Note, except for (d) and (f), all other correlational relationships are significant in VFD-exposed but not non-exposed mothers.
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Related In: Results  -  Collection

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

Figure 5: Relationship and effect sizes among maternal variables exposed to variable foraging demand versus unstressed control mothers. The figure schematizes the effect of VFD exposure versus controls as described by the effect size of the interactive effect of VFD exposure × predictor variable (line inception) in the prediction of the dependent variable (arrow point) except for those effect sizes denoted by an asterisk (where no group effects were evident). Directional arrows in front of each variable are all in an upward direction and at the rear of each variable are all in a downward direction indicating a direct relationship for all variables studied in VFD-exposed mothers versus control mothers (except those relationships that are designated by an asterisk). a = social rank by VFD exposure interaction predicting dyadic distance [F(1; 19) = 11.97; p = 0.003]. b = hierarchical status by VFD exposure effect in the prediction of maternal cortisol concentrations [F(1; 19) = 5.52; p = 0.030] (dominants exhibited higher cortisol than subordinates). c = maternal weight by VFD exposure interaction in the prediction of maternal cortisol concentrations [F(1; 19) = 29.53; p = 0.0001]. *d = greater body weight predicted greater maternal dominance [F(1; 19) = 6.88; p = 0.017] without interactive effect. e = VFD exposure × maternal CSF OT interactive effect in the prediction of maternal cortisol concentrations [F(1; 17) = 6.56, p = 0.02]. *f = dominant mothers exhibited greater CSF OT concentrations than subordinate mothers [F(1; 17) = 6.45; p = 0.021] without interactive effect. Partial η2: large effect size ≥ 0.14. Note, except for (d) and (f), all other correlational relationships are significant in VFD-exposed but not non-exposed mothers.
Mentions: In our attempt to decipher important factors in the transmission of VFD-exposure stress from mothers to their infants, we discovered a complex interaction among maternal social rank, dyadic distance, maternal plasma cortisol, and maternal CSF OT (see Figure 5) with the most salient finding of the current study highlighting the pivotal role of maternal social rank, particularly under VFD-exposure conditions. Clearly, social rank plays a disproportionate role in the context of a perceived shortage of food resources engendered by VFD exposure. Either as a continuous variable, social rank, or as a dichotomous variable, “hierarchical status,” (dominant versus subordinate), the variable significantly predicted among the VFD group, (1) maternal dyadic distance between mother and infant (high rank = increased dyadic distance), (2) maternal plasma cortisol (dominance = high cortisol), and (3) CSF OT directly predicts plasma cortisol but specifically in VFD exposure (upon VFD exposure, high OT predicts high cortisol). Among both VFD and non-VFD groups, social rank predicts CSF OT levels (dominance = increased CSF OT).

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