Decreased amygdala-sensorimotor connectivity mediates the association between prenatal stress and broad autism phenotype in young adults: Project Ice Storm

Stress. 2024 Jan;27(1):2293698. doi: 10.1080/10253890.2023.2293698. Epub 2023 Dec 22.

Abstract

Studies show that prenatal maternal stress (PNMS) is related to risk for child autism, and to atypical amygdala functional connectivity in the autistic child. Yet, it remains unclear whether amygdala functional connectivity mediates the association between PNMS and autistic traits, particularly in young adult offspring. We recruited women who were pregnant during, or within 3 months of, the 1998 Quebec ice storm crisis, and assessed three aspects of PNMS: objective hardship (events experienced during the ice storm), subjective distress (post-traumatic stress symptoms experienced as a result of the ice storm) and cognitive appraisal. At age 19, 32 young adults (21 females) self-reported their autistic-like traits (i.e., aloof personality, pragmatic language impairment and rigid personality), and underwent structural MRI and resting-state functional MRI scans. Seed-to-voxel analyses were conducted to map the amygdala functional connectivity network. Mediation analyses were implemented with bootstrapping of 20,000 resamplings. We found that greater maternal objective hardship was associated with weaker functional connectivity between the left amygdala and the right postcentral gyrus, which was then associated with more pragmatic language impairment. Greater maternal subjective distress was associated with weaker functional connectivity between the right amygdala and the left precentral gyrus, which was then associated with more aloof personality. Our results demonstrate that the long-lasting effect of PNMS on offspring autistic-like traits may be mediated by decreased amygdala-sensorimotor circuits. The differences between amygdala-sensory and amygdala-motor pathways mediating different aspects of PNMS on different autism phenotypes need to be studied further.

Keywords: Amygdala; broad autism phenotype; functional connectivity; postcentral gyrus; precentral gyrus; prenatal maternal stress.

MeSH terms

  • Amygdala / diagnostic imaging
  • Autistic Disorder* / diagnostic imaging
  • Female
  • Humans
  • Language Development Disorders*
  • Magnetic Resonance Imaging
  • Phenotype
  • Pregnancy
  • Prenatal Exposure Delayed Effects* / psychology
  • Stress, Psychological / complications
  • Young Adult