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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.
Acknowledgements
We would like to thank all Project Ice Storm participants.
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No potential conflict of interest was reported by the author(s).
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Notes on contributors
Xinyuan Li
Xinyuan Li, M.D., Ph.D. , completed her PhD in Neuroscience at McGill University in Montreal, specializing in the effect of prenatal maternal stress on offspring neurodevelopment. She is currently a postdoctoral fellow at Alberta Children's Hospital in Calgary, Canada.
Muhammad Naveed Iqbal Qureshi
Muhammad Naveed Iqbal Qureshi, Ph.D. (Biomedical Engineering, Computational Neuroscience, and Artificial Intelligence) completed post-doctoral fellowships at the Department of Psychiatry and Neurosurgery at McGill University, and at the Department of Neuroscience at The Hospital for Sick Children, University of Toronto, Canada.
David P. Laplante
David P. Laplante, Ph.D. is a Senior Research Associate at McGill University’s Lady Davis Institute-Jewish General Hospital in Montreal. His interest lies in examining the interplay between prenatal exposure to maternal adversity (mood, disaster stress), child characteristics, early environmental influences, and youth mental health.
Guillaume Elgbeili
Guillaume Elgbeili, M.Sc. is a statistician working at the Douglas Research Center in Montreal specialized in modeling concurrent and longitudinal associations between parental and child physical and mental health, perinatal and early life environment, and genetics and epigenetics.
Vincent Paquin
Vincent Paquin, M.D. is a Psychiatry Resident and candidate in the Clinician Investigator Program at McGill University, Canada. His research focuses on socio-environmental determinants of mental health in youth.
Sherri Lee Jones
Sherri Lee Jones, Ph.D. (Psychology, Behavioral Neuroscience) completed post-doctoral fellowships at the Department of Psychiatry at McGill University, specializing in the roles of parental factors (e.g. stress, mental health) in offspring neuroendocrine and behavioral development. She is currently a Research Associate at the Douglas Research Center in Montreal, Canada.
Suzanne King
Suzanne King, Ph.D. is Professor Emerita (retired, active) in the Department of Psychiatry at McGill University, and Principal Investigator at the Douglas Hospital Research Centre. To increase understanding about prenatal stress in humans as risk factor for child development her research program focuses on women pregnant during natural disasters (www.mcgill.ca/spiral).
Pedro Rosa-Neto
Pedro Rosa-Neto, M.D., Ph.D. is a Professor of Neurology and neurosurgery and Psychiatry. Dr. Rosa-Neto directs the Translational Neuroimaging Laboratory (TNL) at McGill. University.