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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 plasma cortisol grouping to maternal CSF OT concentrations as a function of VFD exposure. We dichotomized, using a median split, maternal plasma cortisol into “high” versus “low” plasma levels [“high” cortisol mean (SD) = 48.96 (3.57) ng/ml (N = 10) versus “low” cortisol mean (SD) = 39.16 (3.84) ng/ml (N = 11); t-value = −6.02;df = 19; p = 0.000008]. Two cortisol values lacking matching OT values were excluded. Using a factorial ANOVA GLM with OT as the dependent variable, and cortisol grouping and VFD exposure as categorical variables, there was no VFD exposure effect, or cortisol grouping effect but a VFD exposure × cortisol grouping interaction was noted [F(1; 17) = 9.23, p = 0.007]. Post hoct-test differences (p ≤ 0.05) for CSF OT; aVFD-exposure high-cortisol grouping > non-exposed high-cortisol grouping; bVFD-exposure high-cortisol grouping > VFD-exposure low-cortisol grouping. Vertical bars denote 0.95 confidence intervals.
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Figure 3: Relationship between maternal plasma cortisol grouping to maternal CSF OT concentrations as a function of VFD exposure. We dichotomized, using a median split, maternal plasma cortisol into “high” versus “low” plasma levels [“high” cortisol mean (SD) = 48.96 (3.57) ng/ml (N = 10) versus “low” cortisol mean (SD) = 39.16 (3.84) ng/ml (N = 11); t-value = −6.02;df = 19; p = 0.000008]. Two cortisol values lacking matching OT values were excluded. Using a factorial ANOVA GLM with OT as the dependent variable, and cortisol grouping and VFD exposure as categorical variables, there was no VFD exposure effect, or cortisol grouping effect but a VFD exposure × cortisol grouping interaction was noted [F(1; 17) = 9.23, p = 0.007]. Post hoct-test differences (p ≤ 0.05) for CSF OT; aVFD-exposure high-cortisol grouping > non-exposed high-cortisol grouping; bVFD-exposure high-cortisol grouping > VFD-exposure low-cortisol grouping. Vertical bars denote 0.95 confidence intervals.

Mentions: A second question was whether maternal plasma cortisol was predictive of maternal CSF OT. However, maternal plasma cortisol as a continuous predictor variable did not predict maternal CSF OT, even in an interactive fashion. A second OT/cortisol non-parametric analysis was therefore performed to examine the predictive relationship of cortisol to OT under VFD exposure conditions. We dichotomized, using a median split, maternal plasma cortisol into “high” versus “low” plasma levels [“high” cortisol mean (SD) = 48.96 (3.57) ng/ml (N = 10) versus “low” cortisol mean (SD) = 39.16 (3.84) ng/ml (N = 11); t-value = −6.02; df = 19; p = 0.000008]. Of note, there were no VFD exposure effects on maternal plasma cortisol [VFD-exposure mean (SD) = 44.60 (6.95) ng/ml (N = 11) versus non-VFD-exposed mean (SD) = 42.97 (5.45); t-value = −0.59; df = 19; p = 0.55], which contrasts to the cortisol effect when controlling for CSF OT concentrations and body mass. Two cortisol value lacking matching OT values were excluded. Using a factorial ANOVA GLM with OT as the dependent variable, and cortisol grouping and VFD exposure as categorical variables, there was no VFD exposure effect or cortisol grouping effect but a VFD exposure × cortisol grouping interaction was noted [F(1; 17) = 9.23, p = 0.007] (see Figure 3). Effects remained significant when covarying for infant age. High “cortisol” subjects that were VFD-exposed [mean (SD) = 40.36 (2.73) (N = 6)] exhibited elevated maternal CSF OT (pg/ml) compared to low “cortisol” VFD subjects [mean (SD) = 29.98 (4.52) (N = 5); t-value = −4.70; df = 9, p = 0.001]. The same comparison was not significant in non-exposed mothers. VFD-exposed mothers from the high cortisol grouping also exhibited significantly greater CSF OT than non-exposed mothers with high cortisol [mean (SD) = 29.63 (8.96) N = 4; t-value = −2.81, df = 8, p = 0.02].


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 plasma cortisol grouping to maternal CSF OT concentrations as a function of VFD exposure. We dichotomized, using a median split, maternal plasma cortisol into “high” versus “low” plasma levels [“high” cortisol mean (SD) = 48.96 (3.57) ng/ml (N = 10) versus “low” cortisol mean (SD) = 39.16 (3.84) ng/ml (N = 11); t-value = −6.02;df = 19; p = 0.000008]. Two cortisol values lacking matching OT values were excluded. Using a factorial ANOVA GLM with OT as the dependent variable, and cortisol grouping and VFD exposure as categorical variables, there was no VFD exposure effect, or cortisol grouping effect but a VFD exposure × cortisol grouping interaction was noted [F(1; 17) = 9.23, p = 0.007]. Post hoct-test differences (p ≤ 0.05) for CSF OT; aVFD-exposure high-cortisol grouping > non-exposed high-cortisol grouping; bVFD-exposure high-cortisol grouping > VFD-exposure low-cortisol grouping. Vertical bars denote 0.95 confidence intervals.
© Copyright Policy
Related In: Results  -  Collection

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

Figure 3: Relationship between maternal plasma cortisol grouping to maternal CSF OT concentrations as a function of VFD exposure. We dichotomized, using a median split, maternal plasma cortisol into “high” versus “low” plasma levels [“high” cortisol mean (SD) = 48.96 (3.57) ng/ml (N = 10) versus “low” cortisol mean (SD) = 39.16 (3.84) ng/ml (N = 11); t-value = −6.02;df = 19; p = 0.000008]. Two cortisol values lacking matching OT values were excluded. Using a factorial ANOVA GLM with OT as the dependent variable, and cortisol grouping and VFD exposure as categorical variables, there was no VFD exposure effect, or cortisol grouping effect but a VFD exposure × cortisol grouping interaction was noted [F(1; 17) = 9.23, p = 0.007]. Post hoct-test differences (p ≤ 0.05) for CSF OT; aVFD-exposure high-cortisol grouping > non-exposed high-cortisol grouping; bVFD-exposure high-cortisol grouping > VFD-exposure low-cortisol grouping. Vertical bars denote 0.95 confidence intervals.
Mentions: A second question was whether maternal plasma cortisol was predictive of maternal CSF OT. However, maternal plasma cortisol as a continuous predictor variable did not predict maternal CSF OT, even in an interactive fashion. A second OT/cortisol non-parametric analysis was therefore performed to examine the predictive relationship of cortisol to OT under VFD exposure conditions. We dichotomized, using a median split, maternal plasma cortisol into “high” versus “low” plasma levels [“high” cortisol mean (SD) = 48.96 (3.57) ng/ml (N = 10) versus “low” cortisol mean (SD) = 39.16 (3.84) ng/ml (N = 11); t-value = −6.02; df = 19; p = 0.000008]. Of note, there were no VFD exposure effects on maternal plasma cortisol [VFD-exposure mean (SD) = 44.60 (6.95) ng/ml (N = 11) versus non-VFD-exposed mean (SD) = 42.97 (5.45); t-value = −0.59; df = 19; p = 0.55], which contrasts to the cortisol effect when controlling for CSF OT concentrations and body mass. Two cortisol value lacking matching OT values were excluded. Using a factorial ANOVA GLM with OT as the dependent variable, and cortisol grouping and VFD exposure as categorical variables, there was no VFD exposure effect or cortisol grouping effect but a VFD exposure × cortisol grouping interaction was noted [F(1; 17) = 9.23, p = 0.007] (see Figure 3). Effects remained significant when covarying for infant age. High “cortisol” subjects that were VFD-exposed [mean (SD) = 40.36 (2.73) (N = 6)] exhibited elevated maternal CSF OT (pg/ml) compared to low “cortisol” VFD subjects [mean (SD) = 29.98 (4.52) (N = 5); t-value = −4.70; df = 9, p = 0.001]. The same comparison was not significant in non-exposed mothers. VFD-exposed mothers from the high cortisol grouping also exhibited significantly greater CSF OT than non-exposed mothers with high cortisol [mean (SD) = 29.63 (8.96) N = 4; t-value = −2.81, df = 8, p = 0.02].

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