Maternal Childhood Adversity Associates With Frontoamygdala Connectivity in Neonates

Abstract

Background: It is well established that exposure to adversity, especially during sensitive periods of development such as childhood, has both behavioral (e.g., increasing one's risk for psychiatric illnesses) and neurobiological consequences. But could these effects of early-life exposure to adversity also be transmitted across generations? We directly address this question, investigating the associations between maternal exposure to adversity during her own childhood and neural connectivity in her neonate.

Methods: Mothers from a sample of Black mother-neonate dyads (n = 48)-a group that is disproportionately affected by early-life adversity-completed questionnaires assessing their current distress (i.e., a composite measure of anxiety, depression, and perceived stress) during the first and third trimesters of pregnancy and retrospectively reported on their own childhood experiences of abuse and neglect. At 1 month postpartum, neonatal offspring of these women underwent a resting-state functional magnetic resonance imaging scan during natural sleep.

Results: Greater maternal exposure to emotional neglect during her own childhood correlated with stronger functional connectivity of two different frontoamygdala circuits in these neonates, as early as 1 month after birth. This effect was specific to early experiences of emotional neglect and was not explained by maternal exposure to other forms of childhood maltreatment or by maternal distress during pregnancy.

Conclusions: These results provide novel evidence that the absence of emotional support early in a mother's life, years before conception, are associated with neural changes-namely, in functional connectivity between the amygdala and medial prefrontal regions-in her offspring shortly after birth.

Keywords: Brain development; Childhood adversity; Intergenerational transmission; Newborn; Pregnancy; Resting-state functional connectivity MRI.

Figure 1.

Recruitment flow chart.

Figure 2.

The functional correlation between the amygdala and dACC in each neonate was calculated by averaging the BOLD time series of each voxel within the ROI mask and correlating the average time series of the amygdala with the average time series of the dACC. The same procedure was used to calculate the functional correlation (FC) between the amygdala and vmPFC, between the dACC and vmPFC, and between the amygdala and IFG. Next, maternal experiences of adversity were examined as predictors of these FCs in 1-month-old sleeping neonates. (a) Emotional neglect from the mother’s childhood was robustly associated with stronger positive amygdala-dACC FC in neonates (b) and with stronger positive amygdala-vmPFC FC. (c) Maternal childhood emotional neglect did not associate with neonatal vmPFC-dACC FC (d) or with neonatal amygdala-IFG FC.