Influences of prenatal and postnatal maternal depression on amygdala volume and microstructure in young children

Abstract

Maternal depressive symptoms influence neurodevelopment in the offspring. Such effects may appear to be gender-dependent. The present study examined contributions of prenatal and postnatal maternal depressive symptoms to the volume and microstructure of the amygdala in 4.5-year-old boys and girls. Prenatal maternal depressive symptoms were measured using the Edinburgh Postnatal Depression Scale (EPDS) at 26 weeks of gestation. Postnatal maternal depression was assessed at 3 months using the EPDS and at 1, 2, 3 and 4.5 years using the Beck's Depression Inventory-II. Structural magnetic resonance imaging and diffusion tensor imaging were performed with 4.5-year-old children to extract the volume and fractional anisotropy (FA) values of the amygdala. Our results showed that greater prenatal maternal depressive symptoms were associated with larger right amygdala volume in girls, but not in boys. Increased postnatal maternal depressive symptoms were associated with higher right amygdala FA in the overall sample and girls, but not in boys. These results support the role of variation in right amygdala structure in transmission of maternal depression to the offspring, particularly to girls. The differential effects of prenatal and postnatal maternal depressive symptoms on the volume and FA of the right amygdala suggest the importance of the timing of exposure to maternal depressive symptoms in brain development of girls. This further underscores the need for intervention targeting both prenatal and postnatal maternal depression to girls in preventing adverse child outcomes.

Sex Differences in Vulnerability to Prenatal Stress: a Review of the Recent Literature

“…Five evaluated effects of PNMS on neural structure and function, four providing evidence of sexually dimorphic programming effects in girls. Wen et al ( N  = 235) reported a sex-specific association whereby prenatal depression was positively associated with greater right amygdala volume in 4.5-year-old girls, but not boys [63]. Data from the same study team ( N  = 258) showed that, among girls only, increases in maternal depressive symptoms from 26-week gestation to 3 months postpartum were associated with greater infant right frontal lobe activity and greater right frontal asymmetry at age 6 months and greater lower right frontal functional connectivity at age 18 months [61•].…”

“…Six reported significant PNMS*sex interactions. The preponderance of evidence suggests that girls may be particularly vulnerable to PNMS programming, altering neural structure, function, and neuroendocrine sensitivity in a manner that confers risk for anxiety and affective pathology [61•, 63, 70•]. One study found evidence that these neural sequelae may mediate PNMS effects on internalizing symptoms [70•].…”

Early environmental influences on the development of children's brain structure and function

“…21 Similarly, orphanage rearing is associated with diminished autonomic and hypothalamic-pituitary-adrenal axis responses to psychosocial stress, enlarged amygdala volumes, and accelerated amygdala-medial prefrontal cortex connectivity mediated by cortisol. 26 Maternal sensitivity levels correlated with connectivity between the hippocampus and areas related to emotional regulation and socio-emotional functioning. 1 These effects are mediated by epigenetic changes at the hippocampal glucocorticoids receptor gene promoter of the offspring, through acetylation of histones H3K9 and DNA methylation preventing the transcription factor NGFI-A binding to the exon 1 7 .…”

Effects of infant negative affect and contextual factors on infant regulatory capacity: The moderating role of infant sex

“…reported an interaction between infant sex and postnatal maternal anxiety symptoms in association with executive functioning of 8-month-old infants such that only girls were negatively impacted. Similarly, Wen et al (2017) identified an effect of postnatal maternal depressive symptoms on female, but not male, 4.5-year-olds' amygdala microstructure. Two separate studies found links between levels of cortisol in human breastmilk and negative affect in infant girls, but not boys (Grey, Davis, Sandman, & Glynn, 2013;Nolvi, Uusitupa, et al, 2017).…”

“…Furthermore, few studies have considered infant sex as a moderator of such associations—an important consideration in light of predictions stemming from the viability–vulnerability theory (Sandman et al, ) and several prior findings (e.g., Stifter & Spinrad, ). This is particularly notable because Sandman and colleagues' () viability–vulnerability tradeoff theory encompasses both the prenatal and the early postnatal period, but few studies have considered the postnatal period in tests of this perspective (see Nolvi, Pesonen, et al, , and Wen et al, for studies showing support of this theory, with Matheny & Phillips, not showing supportive evidence). As such, the current study addresses several of the gaps in existing work that are noted above.…”