Neural correlates of disaster-related prenatal maternal stress in young adults from Project Ice Storm: Focus on amygdala, hippocampus, and prefrontal cortex

Abstract

Background: Studies have shown that prenatal maternal stress alters volumes of the amygdala and hippocampus, and alters functional connectivity between the amygdala and prefrontal cortex. However, it remains unclear whether prenatal maternal stress (PNMS) affects volumes and functional connectivity of these structures at their subdivision levels.

Methods: T1-weighted MRI and resting-state functional MRI were obtained from 19-year-old young adult offspring with (n = 39, 18 male) and without (n = 65, 30 male) exposure to PNMS deriving from the 1998 ice storm. Volumes of amygdala nuclei, hippocampal subfields and prefrontal subregions were computed, and seed-to-seed functional connectivity analyses were conducted.

Results: Compared to controls, young adult offspring exposed to disaster-related PNMS had larger volumes of bilateral whole amygdala, driven by the lateral, basal, central, medial, cortical, accessory basal nuclei, and corticoamygdaloid transition; larger volumes of bilateral whole hippocampus, driven by the CA1, HATA, molecular layer, fissure, tail, CA3, CA4, and DG; and larger volume of the prefrontal cortex, driven by the left superior frontal. Inversely, young adult offspring exposed to disaster-related PNMS had lower functional connectivity between the whole amygdala and the prefrontal cortex (driven by bilateral frontal poles, the left superior frontal and left caudal middle frontal); and lower functional connectivity between the hippocampal tail and the prefrontal cortex (driven by the left lateral orbitofrontal).

Conclusion: These results suggest the possibility that effects of disaster-related PNMS on structure and function of subdivisions of offspring amygdala, hippocampus and prefrontal cortex could persist into young adulthood.

Keywords: amygdala nuclei; hippocampal subfields; prefrontal cortex; prenatal maternal stress; resting-state functional connectivity; volume.

FIGURE 1

Segmentation of the hippocampus and the amygdala of one Ice Storm participant. The columns from left to right represent axial, coronal, and sagittal views, respectively. The hippocampal subfields and the amygdala nuclei (left and right) were labeled with different colors. The second-row zooms in the right hippocampus and the right amygdala without any labels as the reference. The third-row zooms in the right hippocampus and the right amygdala with labels as the reference.

FIGURE 2

Segmentation of the prefrontal cortex of one Ice Storm participant. The columns from left to right represent axial, coronal, and sagittal views, respectively. The prefrontal subregions (left and right) were labeled with different colors.

FIGURE 3

Effects size estimates measured by partial eta squared (η²_p) for the left (blue) and right (orange) whole amygdala and amygdala nuclei. η²_p = 0.01 indicates a small effect; η²_p = 0.06 indicates a medium effect, and η²_p = 0.14 indicates a large effect. ***q < 0.001, **q < 0.01, *q < 0.05.

FIGURE 4

Effects size estimates measured by partial eta squared (η²_p) for the left (blue) and right (orange) whole hippocampus and hippocampal subfields. η²_p = 0.01 indicates a small effect; η²_p = 0.06 indicates a medium effect, and η²_p = 0.14 indicates a large effect. ***q < 0.001, **q < 0.01, *q < 0.05.