Abstract
Introduction: The amygdala is a brain structure involved in emotional regulation. Studies have shown that larger amygdala volumes are associated with behavioral disorders. Prenatal maternal depression is associated with structural changes in the amygdala, which in turn, is predictive of an increase in behavioral problems. Girls may be particularly vulnerable. However, it is not known whether disaster-related prenatal maternal stress (PNMS), or which aspect of the maternal stress experience (i.e., objective hardship, subjective distress, and cognitive appraisal), influences amygdala volumes. Nor is it known whether amygdala volumes mediate the effect of PNMS on behavioral problems in girls and boys.Aims: To assess whether aspects of PNMS are associated with amygdala volume, to determine whether timing of exposure moderates the effect, and to test whether amygdala volume mediates the association between PNMS and internalizing and externalizing problems in 11½ year old children exposed in utero, to varying levels of disaster-related PNMS.Methods: Bilateral amygdala volumes (AGV) and total brain volume (TBV) were acquired using magnetic resonance imaging, from 35 boys and 33 girls whose mothers were pregnant during the January 1998 Quebec Ice Storm. The mothers' disaster-related stress was assessed in June 1998. Child internalizing and externalizing problems were assessed at 11½ years using the Child Behavior Checklist (CBCL). Hierarchical regression analyses and mediation analyses were conducted on boys and girls separately, controlling for perinatal and postnatal factors.Results: In boys, subjective distress was associated with larger right AGV/TBV when mothers where exposed during late pregnancy, which in turn explained higher levels of externalizing behavior. However, when adjusting for postnatal factors, the effect was no longer significant. In girls, later gestational exposure to the ice storm was associated with larger AGV/TBV, but here, higher levels of objective PNMS were associated with more externalizing problems, which was, in part, mediated by larger AGV/TBV. No effects were detected on internalizing behaviors.Conclusion: These results suggest that the effects of PNMS on amygdala development and externalizing symptoms, as assessed in boys and girls in early adolescence, can be influenced by the timing of the stress in pregnancy, and the particular aspect of the mother's stress experience.
Highlights
The amygdala is a brain structure involved in emotional regulation
Amygdala Volume and Behavioral Outcomes (Partial Correlations) When testing the second path of the indirect effect we found that right and left normalized amygdala volume (AGV) in boys were associated with externalizing, but not internalizing, problems when controlling for timing of exposure, handedness, maternal psychological functioning, and maternal alcohol usage during pregnancy (Table 4)
We have previously reported with this sample that objective hardship and subjective distress are associated with internalizing problems when controlling for sex (King et al, 2012), whereas our bivariate correlations here suggest that subjective distress is more strongly associated with internalizing in girls than in boys
Summary
The amygdala is a brain structure involved in emotional regulation. Studies have shown that larger amygdala volumes are associated with behavioral disorders. It is not known whether disaster-related prenatal maternal stress (PNMS), or which aspect of the maternal stress experience (i.e., objective hardship, subjective distress, and cognitive appraisal), influences amygdala volumes. Nor is it known whether amygdala volumes mediate the effect of PNMS on behavioral problems in girls and boys. Some studies show that the associations are sensitive to prenatal maternal anxiety (e.g., O’Connor et al, 2002; Van den Bergh and Marcoen, 2004) Many of those studies controlled for potential confounders associated with anxiety, such as smoking, alcohol use, and household income, and showed that the results persisted. Buss et al (2012) reported that higher maternal cortisol levels during early pregnancy predicted more internalizing problems in girls at age 7, but not in boys, which was in part, mediated by amygdala volume (AGV)
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