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

Xinyuan Li; Muhammad Naveed Iqbal Qureshi; David P Laplante; Guillaume Elgbeili; Sherri Lee Jones; Suzanne King; Pedro Rosa-Neto

doi:10.3389/fnhum.2023.1094039

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

Front Hum Neurosci. 2023 Feb 1:17:1094039. doi: 10.3389/fnhum.2023.1094039. eCollection 2023.

Authors

Xinyuan Li^{1

2

3

4}, Muhammad Naveed Iqbal Qureshi^{3

4}, David P Laplante⁵, Guillaume Elgbeili², Sherri Lee Jones⁶, Suzanne King^{2

6}, Pedro Rosa-Neto^{3

4

7}

Affiliations

¹ Integrated Program in Neuroscience, McGill University, Montreal, QC, Canada.
² Mental Health and Society Division, Douglas Mental Health University Institute, Montreal, QC, Canada.
³ Translational Neuroimaging Laboratory, McGill University Research Centre for Studies in Aging, Montreal, QC, Canada.
⁴ Montreal Neurological Institute, McGill University, Montreal, QC, Canada.
⁵ Centre for Child Development and Mental Health, Lady Davis Institute-Jewish General Hospital, Montreal, QC, Canada.
⁶ Department of Psychiatry, McGill University, Montreal, QC, Canada.
⁷ Department of Neurology and Neurosurgery, McGill University, Montreal, QC, Canada.

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.

Grants and funding

Project Ice Storm was supported by grants to SK and colleagues by the Canadian Institutes of Health Research (MOP-57849, MOP-111177, and MOP-125892). XL was supported by the China Scholarship Council (201906170056).