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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

Maternal CSF OT concentrations as a function of VFD exposure and hierarchical status and their interaction. There was an overall effect of hierarchical status, with dominant mothers exhibiting greater CSF OT concentrations than subordinate mothers. [F(1; 17) = 6.45; p = 0.021]. *Post hoc testing revealed that dominant VFD-exposed mothers exhibited significantly greater CSF OT than subordinate VFD-exposed mothers. No interactive effects were noted. Vertical bars denote 0.95 confidence intervals.
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Figure 4: Maternal CSF OT concentrations as a function of VFD exposure and hierarchical status and their interaction. There was an overall effect of hierarchical status, with dominant mothers exhibiting greater CSF OT concentrations than subordinate mothers. [F(1; 17) = 6.45; p = 0.021]. *Post hoc testing revealed that dominant VFD-exposed mothers exhibited significantly greater CSF OT than subordinate VFD-exposed mothers. No interactive effects were noted. Vertical bars denote 0.95 confidence intervals.

Mentions: The next GLM aimed to determine the effects of VFD exposure and hierarchical status on maternal CSF OT concentrations independent of cortisol levels. The interactive term of VFD exposure × hierarchical status was entered into a factorial design. There was an overall effect of hierarchical status, with dominant mothers exhibiting greater CSF OT concentrations than subordinate mothers. [Dominants mean (SE) = 38.04 (2.02), N = 10 versus Subordinates mean (SE) = 30.94 (1.93), N = 11; F(1; 17) = 6.45; p = 0.021] (Figure 4). There was no effect of VFD exposure on maternal CSF OT levels and the VFD exposure × hierarchical status interaction was not significant. Post hoct-tests revealed significantly greater maternal CSF OT in dominants versus subordinates in VFD-exposed mothers [Dominant mean (SD) = 40.09 (2.97), N = 5 versus subordinate mean (SD) = 31.94 (6.27), N = 6, t-value = 2.65; df = 9, p = 0.026], whereas in non-VFD, there were no hierarchical status differences for maternal CSF OT. Two maternal CSF OT values were not available for analysis.


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)

Maternal CSF OT concentrations as a function of VFD exposure and hierarchical status and their interaction. There was an overall effect of hierarchical status, with dominant mothers exhibiting greater CSF OT concentrations than subordinate mothers. [F(1; 17) = 6.45; p = 0.021]. *Post hoc testing revealed that dominant VFD-exposed mothers exhibited significantly greater CSF OT than subordinate VFD-exposed mothers. No interactive effects were noted. Vertical bars denote 0.95 confidence intervals.
© Copyright Policy
Related In: Results  -  Collection

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

Figure 4: Maternal CSF OT concentrations as a function of VFD exposure and hierarchical status and their interaction. There was an overall effect of hierarchical status, with dominant mothers exhibiting greater CSF OT concentrations than subordinate mothers. [F(1; 17) = 6.45; p = 0.021]. *Post hoc testing revealed that dominant VFD-exposed mothers exhibited significantly greater CSF OT than subordinate VFD-exposed mothers. No interactive effects were noted. Vertical bars denote 0.95 confidence intervals.
Mentions: The next GLM aimed to determine the effects of VFD exposure and hierarchical status on maternal CSF OT concentrations independent of cortisol levels. The interactive term of VFD exposure × hierarchical status was entered into a factorial design. There was an overall effect of hierarchical status, with dominant mothers exhibiting greater CSF OT concentrations than subordinate mothers. [Dominants mean (SE) = 38.04 (2.02), N = 10 versus Subordinates mean (SE) = 30.94 (1.93), N = 11; F(1; 17) = 6.45; p = 0.021] (Figure 4). There was no effect of VFD exposure on maternal CSF OT levels and the VFD exposure × hierarchical status interaction was not significant. Post hoct-tests revealed significantly greater maternal CSF OT in dominants versus subordinates in VFD-exposed mothers [Dominant mean (SD) = 40.09 (2.97), N = 5 versus subordinate mean (SD) = 31.94 (6.27), N = 6, t-value = 2.65; df = 9, p = 0.026], whereas in non-VFD, there were no hierarchical status differences for maternal CSF OT. Two maternal CSF OT values were not available for analysis.

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