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

References

• American Psychiatric Association (APA). (2013). Diagnostic and statistical manual of mental disorders (DSM-5®). American Psychiatric Pub.
   Google Scholar
• Avants, B. B., Epstein, C. L., Grossman, M., & Gee, J. C. (2008). Symmetric diffeomorphic image registration with cross-correlation: evaluating automated labeling of elderly and neurodegenerative brain. Medical Image Analysis, 12(1), 1–10. https://doi.org/10.1016/j.media.2007.06.004
   PubMed Web of Science ®Google Scholar
• Baas, D., Aleman, A., & Kahn, R. S. (2004). Lateralization of amygdala activation: a systematic review of functional neuroimaging studies. Brain Research. Brain Research Reviews, 45(2), 96–103. https://doi.org/10.1016/j.brainresrev.2004.02.004
   PubMedGoogle Scholar
• Belleau, E. L., Ehret, L. E., Hanson, J. L., Brasel, K. J., Larson, C. L., & deRoon-Cassini, T. A. (2020). Amygdala functional connectivity in the acute aftermath of trauma prospectively predicts severity of posttraumatic stress symptoms. Neurobiology of Stress, 12, 100217. https://doi.org/10.1016/j.ynstr.2020.100217
   PubMed Web of Science ®Google Scholar
• Beversdorf, D. Q., Manning, S. E., Hillier, A., Anderson, S. L., Nordgren, R. E., Walters, S. E., Nagaraja, H. N., Cooley, W. C., Gaelic, S. E., & Bauman, M. L. (2005). Timing of prenatal stressors and autism. Journal of Autism and Developmental Disorders, 35(4), 471–478. https://doi.org/10.1007/s10803-005-5037-8
   PubMed Web of Science ®Google Scholar
• Bromet, E., & Dew, M. A. (1995). Review of psychiatric epidemiologic research on disasters. Epidemiologic Reviews, 17(1), 113–119. https://doi.org/10.1093/oxfordjournals.epirev.a036166
   PubMed Web of Science ®Google Scholar
• Brunet, A., St-Hilaire, A., Jehel, L., & King, S. (2003). Validation of a French version of the impact of event scale-revised. Canadian Journal of Psychiatry. Revue canadienne de psychiatrie, 48(1), 56–61. https://doi.org/10.1177/070674370304800111
   PubMed Web of Science ®Google Scholar
• Cao-Lei, L., Dancause, K. N., Elgbeili, G., Laplante, D. P., Szyf, M., & King, S. (2016). Pregnant women’s cognitive appraisal of a natural disaster affects their children’s BMI and central adiposity via DNA methylation: Project Ice Storm. Early Human Development, 103, 189–192. https://doi.org/10.1016/j.earlhumdev.2016.09.013
   PubMed Web of Science ®Google Scholar
• Cao-Lei, L., Dancause, K. N., Elgbeili, G., Laplante, D. P., Szyf, M., & King, S. (2018). DNA methylation mediates the effect of maternal cognitive appraisal of a disaster in pregnancy on the child’s C-peptide secretion in adolescence: Project Ice Storm. PloS One, 13(2), e0192199. https://doi.org/10.1371/journal.pone.0192199
   PubMed Web of Science ®Google Scholar
• Class, Q. A., Abel, K. M., Khashan, A. S., Rickert, M. E., Dalman, C., Larsson, H., Hultman, C. M., Långström, N., Lichtenstein, P., & D’Onofrio, B. M. (2014). Offspring psychopathology following preconception, prenatal and postnatal maternal bereavement stress. Psychological Medicine, 44(1), 71–84. https://doi.org/10.1017/s0033291713000780
   PubMed Web of Science ®Google Scholar
• Dovgan, K. N., & Villanti, K. M. (2021). The prevalence of broad autism phenotype in young adults: The roles of genetic relationship to autism, gender, and academic major. The Journal of Genetic Psychology, 182(3), 174–181. https://doi.org/10.1080/00221325.2021.1904817
   PubMed Web of Science ®Google Scholar
• Esteban, O., Markiewicz, C. J., Blair, R. W., Moodie, C. A., Isik, A. I., Erramuzpe, A., Kent, J. D., Goncalves, M., DuPre, E., Snyder, M., Oya, H., Ghosh, S. S., Wright, J., Durnez, J., Poldrack, R. A., & Gorgolewski, K. J. (2019). fMRIPrep: A robust preprocessing pipeline for functional MRI. Nature Methods, 16(1), 111–116. https://doi.org/10.1038/s41592-018-0235-4
   PubMed Web of Science ®Google Scholar
• Fishman, I., Linke, A. C., Hau, J., Carper, R. A., & Müller, R. A. (2018). Atypical functional connectivity of amygdala related to reduced symptom severity in children with autism. Journal of the American Academy of Child and Adolescent Psychiatry, 57(10), 764–774.e763. https://doi.org/10.1016/j.jaac.2018.06.015
   PubMed Web of Science ®Google Scholar
• Gao, L., Xi, Q. Q., Wu, J., Han, Y., Dai, W., Su, Y. Y., & Zhang, X. (2015). Association between prenatal environmental factors and child autism: A case control study in Tianjin, China. Biomedical and Environmental Sciences. 28(9), 642–650. https://doi.org/10.3967/bes2015.090
   PubMed Web of Science ®Google Scholar
• Glover, G. H. (2011). Overview of functional magnetic resonance imaging. Neurosurgery Clinics of North America, 22(2), 133–139, vii. https://doi.org/10.1016/j.nec.2010.11.001
   PubMed Web of Science ®Google Scholar
• Greve, D. N., & Fischl, B. (2009). Accurate and robust brain image alignment using boundary-based registration. NeuroImage, 48(1), 63–72. https://doi.org/10.1016/j.neuroimage.2009.06.060
   PubMed Web of Science ®Google Scholar
• Guo, X., Duan, X., Long, Z., Chen, H., Wang, Y., Zheng, J., Zhang, Y., Li, R., & Chen, H. (2016). Decreased amygdala functional connectivity in adolescents with autism: A resting-state fMRI study. Psychiatry Research. Neuroimaging, 257, 47–56. https://doi.org/10.1016/j.pscychresns.2016.10.005
   PubMed Web of Science ®Google Scholar
• Hayes, A. F. (2017). Introduction to mediation, moderation, and conditional process analysis: A regression-based approach. Guilford publications.
   Google Scholar
• Herman, J. P., Ostrander, M. M., Mueller, N. K., & Figueiredo, H. (2005). Limbic system mechanisms of stress regulation: Hypothalamo-pituitary-adrenocortical axis. Progress in Neuro-Psychopharmacology & Biological Psychiatry, 29(8), 1201–1213. https://doi.org/10.1016/j.pnpbp.2005.08.006
   PubMed Web of Science ®Google Scholar
• Hilton, C. L., Harper, J. D., Kueker, R. H., Lang, A. R., Abbacchi, A. M., Todorov, A., & LaVesser, P. D. (2010). Sensory responsiveness as a predictor of social severity in children with high functioning autism spectrum disorders. Journal of Autism and Developmental Disorders, 40(8), 937–945. https://doi.org/10.1007/s10803-010-0944-8
   PubMed Web of Science ®Google Scholar
• Howland, M. A., Sandman, C. A., & Glynn, L. M. (2017). Developmental origins of the human hypothalamic-pituitary-adrenal axis. Expert Review of Endocrinology & Metabolism, 12(5), 321–339. https://doi.org/10.1080/17446651.2017.1356222
   PubMed Web of Science ®Google Scholar
• Humphreys, K. L., Camacho, M. C., Roth, M. C., & Estes, E. C. (2020). Prenatal stress exposure and multimodal assessment of amygdala-medial prefrontal cortex connectivity in infants. Developmental Cognitive Neuroscience, 46, 100877. https://doi.org/10.1016/j.dcn.2020.100877
   PubMed Web of Science ®Google Scholar
• Huntenburg, J. M. (2014). Evaluating nonlinear coregistration of BOLD EPI and T1w images. Freie Universität Berlin.
   Google Scholar
• Hurley, R. S., Losh, M., Parlier, M., Reznick, J. S., & Piven, J. (2007). The broad autism phenotype questionnaire. Journal of Autism and Developmental Disorders, 37(9), 1679–1690. https://doi.org/10.1007/s10803-006-0299-3
   PubMed Web of Science ®Google Scholar
• Jenkinson, M., Bannister, P., Brady, M., & Smith, S. (2002). Improved optimization for the robust and accurate linear registration and motion correction of brain images. NeuroImage, 17(2), 825–841. https://doi.org/10.1016/s1053-8119(02)91132-8
   PubMed Web of Science ®Google Scholar
• Jenkinson, M., & Smith, S. (2001). A global optimisation method for robust affine registration of brain images. Medical Image Analysis, 5(2), 143–156. https://doi.org/10.1016/s1361-8415(01)00036-6
   PubMed Web of Science ®Google Scholar
• Jones, S. L., Dufoix, R., Laplante, D. P., Elgbeili, G., Patel, R., Chakravarty, M. M., King, S., & Pruessner, J. C. (2019). Larger amygdala volume mediates the association between prenatal maternal stress and higher levels of externalizing behaviors: Sex specific effects in project ice storm. Frontiers in Human Neuroscience, 13, 144. https://doi.org/10.3389/fnhum.2019.00144
   PubMed Web of Science ®Google Scholar
• King, S., & Laplante, D. P. (2005). The effects of prenatal maternal stress on children’s cognitive development: Project Ice Storm. Stress (Amsterdam, Netherlands), 8(1), 35–45. https://doi.org/10.1080/10253890500108391
   PubMed Web of Science ®Google Scholar
• King, S., & Laplante, D. P. (2015). Using natural disasters to study prenatal maternal stress in humans. Adv Neurobiol, 10, 285–313. https://doi.org/10.1007/978-1-4939-1372-5_14
   PubMedGoogle Scholar
• Kinney, D. K., Miller, A. M., Crowley, D. J., Huang, E., & Gerber, E. (2008). Autism prevalence following prenatal exposure to hurricanes and tropical storms in Louisiana. Journal of Autism and Developmental Disorders, 38(3), 481–488. https://doi.org/10.1007/s10803-007-0414-0
   PubMed Web of Science ®Google Scholar
• Laplante, D. P., Zelazo, P. R., Brunei, A., & King, S. (2007). Functional play at 2 years of age: effects of prenatal maternal stress. Infancy: The Official Journal of the International Society on Infant Studies, 12(1), 69–93. https://doi.org/10.1111/j.1532-7078.2007.tb00234.x
   PubMed Web of Science ®Google Scholar
• Lautarescu, A., Craig, M. C., & Glover, V. (2020). Prenatal stress: Effects on fetal and child brain development. International Review of Neurobiology, 150, 17–40. https://doi.org/10.1016/bs.irn.2019.11.002
   PubMed Web of Science ®Google Scholar
• Li, X., Laplante, D. P., Elgbeili, G., & King, S. (2023). Preconception and prenatal maternal stress are associated with broad autism phenotype in young adults: Project Ice Storm. Journal of Developmental Origins of Health and Disease, 14(4), 481–489. https://doi.org/10.1017/s2040174423000156
   PubMed Web of Science ®Google Scholar
• Liu, T., Ke, J., Qi, R., Zhang, L., Zhang, Z., Xu, Q., Zhong, Y., Lu, G., & Chen, F. (2021). Altered functional connectivity of the amygdala and its subregions in typhoon-related post-traumatic stress disorder. Brain and Behavior, 11(1), e01952. https://doi.org/10.1002/brb3.1952
   PubMed Web of Science ®Google Scholar
• Mandy, M., & Nyirenda, M. (2018). Developmental Origins of Health and Disease: The relevance to developing nations. International Health, 10(2), 66–70. https://doi.org/10.1093/inthealth/ihy006
   PubMed Web of Science ®Google Scholar
• Marco, E. J., Hinkley, L. B., Hill, S. S., & Nagarajan, S. S. (2011). Sensory processing in autism: a review of neurophysiologic findings. Pediatric Research, 69(5 Pt 2), 48r–54r. https://doi.org/10.1203/PDR.0b013e3182130c54
   PubMed Web of Science ®Google Scholar
• McRae, K., Misra, S., Prasad, A. K., Pereira, S. C., & Gross, J. J. (2012). Bottom-up and top-down emotion generation: Implications for emotion regulation. Social Cognitive and Affective Neuroscience, 7(3), 253–262. https://doi.org/10.1093/scan/nsq103
   PubMed Web of Science ®Google Scholar
• Mikkelsen, M., Wodka, E. L., Mostofsky, S. H., & Puts, N. A. J. (2018). Autism spectrum disorder in the scope of tactile processing. Developmental Cognitive Neuroscience, 29, 140–150. https://doi.org/10.1016/j.dcn.2016.12.005
   PubMed Web of Science ®Google Scholar
• Ochsner, K. N., Ray, R. R., Hughes, B., McRae, K., Cooper, J. C., Weber, J., Gabrieli, J. D., & Gross, J. J. (2009). Bottom-up and top-down processes in emotion generation: Common and distinct neural mechanisms. Psychological Science, 20(11), 1322–1331. https://doi.org/10.1111/j.1467-9280.2009.02459.x
   PubMed Web of Science ®Google Scholar
• Phelps, E. A., O’Connor, K. J., Gatenby, J. C., Gore, J. C., Grillon, C., & Davis, M. (2001). Activation of the left amygdala to a cognitive representation of fear. Nature Neuroscience, 4(4), 437–441. https://doi.org/10.1038/86110
   PubMed Web of Science ®Google Scholar
• Posner, J., Cha, J., Roy, A. K., Peterson, B. S., Bansal, R., Gustafsson, H. C., Raffanello, E., Gingrich, J., & Monk, C. (2016). Alterations in amygdala-prefrontal circuits in infants exposed to prenatal maternal depression. Translational Psychiatry, 6(11), e935–e935. https://doi.org/10.1038/tp.2016.146
   PubMedGoogle Scholar
• Pruim, R. H. R., Mennes, M., van Rooij, D., Llera, A., Buitelaar, J. K., & Beckmann, C. F. (2015). ICA-AROMA: A robust ICA-based strategy for removing motion artifacts from fMRI data. NeuroImage, 112, 267–277. https://doi.org/10.1016/j.neuroimage.2015.02.064
   PubMed Web of Science ®Google Scholar
• Qiu, A., Anh, T. T., Li, Y., Chen, H., Rifkin-Graboi, A., Broekman, B. F., Kwek, K., Saw, S. M., Chong, Y. S., Gluckman, P. D., Fortier, M. V., & Meaney, M. J. (2015). Prenatal maternal depression alters amygdala functional connectivity in 6-month-old infants. Translational Psychiatry, 5(2), e508–e508. https://doi.org/10.1038/tp.2015.3
   PubMedGoogle Scholar
• Rai, D., Golding, J., Magnusson, C., Steer, C., Lewis, G., & Dalman, C. (2012). Prenatal and early life exposure to stressful life events and risk of autism spectrum disorders: Population-based studies in Sweden and England. PloS One, 7(6), e38893. https://doi.org/10.1371/journal.pone.0038893
   PubMed Web of Science ®Google Scholar
• Roozendaal, B., McEwen, B. S., & Chattarji, S. (2009). Stress, memory and the amygdala. Nature Reviews. Neuroscience, 10(6), 423–433. https://doi.org/10.1038/nrn2651
   PubMed Web of Science ®Google Scholar
• Sah, P., Faber, E. S., Lopez De Armentia, M., & Power, J. (2003). The amygdaloid complex: Anatomy and physiology. Physiological Reviews, 83(3), 803–834. https://doi.org/10.1152/physrev.00002.2003
   PubMed Web of Science ®Google Scholar
• Sasson, N. J., Lam, K. S., Childress, D., Parlier, M., Daniels, J. L., & Piven, J. (2013). The broad autism phenotype questionnaire: Prevalence and diagnostic classification. Autism Research: Official Journal of the International Society for Autism Research, 6(2), 134–143. https://doi.org/10.1002/aur.1272
   PubMed Web of Science ®Google Scholar
• Say, G. N., Karabekiroğlu, K., Babadağı, Z., & Yüce, M. (2016). Maternal stress and perinatal features in autism and attention deficit/hyperactivity disorder. Pediatrics International: Official Journal of the Japan Pediatric Society, 58(4), 265–269. https://doi.org/10.1111/ped.12822
   PubMed Web of Science ®Google Scholar
• Shen, M. D., Li, D. D., Keown, C. L., Lee, A., Johnson, R. T., Angkustsiri, K., Rogers, S. J., Müller, R. A., Amaral, D. G., & Nordahl, C. W. (2016). Functional connectivity of the amygdala is disrupted in preschool-aged children with autism spectrum disorder. Journal of the American Academy of Child and Adolescent Psychiatry, 55(9), 817–824. https://doi.org/10.1016/j.jaac.2016.05.020
   PubMed Web of Science ®Google Scholar
• Simmons, A. N., Matthews, S. C., Strigo, I. A., Baker, D. G., Donovan, H. K., Motezadi, A., Stein, M. B., & Paulus, M. P. (2011). Altered amygdala activation during face processing in Iraqi and Afghanistani war veterans. Biology of Mood & Anxiety Disorders, 1(1), 6. https://doi.org/10.1186/2045-5380-1-6
   PubMedGoogle Scholar
• Toschi, N., Duggento, A., & Passamonti, L. (2017). Functional connectivity in amygdalar-sensory/(pre)motor networks at rest: New evidence from the Human Connectome Project. The European Journal of Neuroscience, 45(9), 1224–1229. https://doi.org/10.1111/ejn.13544
   PubMed Web of Science ®Google Scholar
• Treiber, J. M., White, N. S., Steed, T. C., Bartsch, H., Holland, D., Farid, N., McDonald, C. R., Carter, B. S., Dale, A. M., & Chen, C. C. (2016). Characterization and correction of geometric distortions in 814 diffusion weighted images. PloS One, 11(3), e0152472. https://doi.org/10.1371/journal.pone.0152472
   PubMed Web of Science ®Google Scholar
• Tustison, N. J., Avants, B. B., Cook, P. A., Zheng, Y., Egan, A., Yushkevich, P. A., & Gee, J. C. (2010). N4ITK: improved N3 bias correction. IEEE Transactions on Medical Imaging, 29(6), 1310–1320. https://doi.org/10.1109/tmi.2010.2046908
   PubMed Web of Science ®Google Scholar
• van den Bergh, B. R. H., Dahnke, R., & Mennes, M. (2018). Prenatal stress and the developing brain: Risks for neurodevelopmental disorders. Development and Psychopathology, 30(3), 743–762. https://doi.org/10.1017/s0954579418000342
   PubMed Web of Science ®Google Scholar
• Van den Stock, J., Tamietto, M., Sorger, B., Pichon, S., Grézes, J., & de Gelder, B. (2011). Cortico-subcortical visual, somatosensory, and motor activations for perceiving dynamic whole-body emotional expressions with and without striate cortex (V1). Proceedings of the National Academy of Sciences of the United States of America, 108(39), 16188–16193. https://doi.org/10.1073/pnas.1107214108
   PubMed Web of Science ®Google Scholar
• Varcin, K. J., Alvares, G. A., Uljarević, M., & Whitehouse, A. J. O. (2017). Prenatal maternal stress events and phenotypic outcomes in Autism Spectrum Disorder. Autism Research: official Journal of the International Society for Autism Research, 10(11), 1866–1877. https://doi.org/10.1002/aur.1830
   PubMed Web of Science ®Google Scholar
• Walder, D. J., Laplante, D. P., Sousa-Pires, A., Veru, F., Brunet, A., & King, S. (2014). Prenatal maternal stress predicts autism traits in 6½ year-old children: Project Ice Storm. Psychiatry Research, 219(2), 353–360. https://doi.org/10.1016/j.psychres.2014.04.034
   PubMed Web of Science ®Google Scholar
• Wang, S., Peterson, D. J., Gatenby, J. C., Li, W., Grabowski, T. J., & Madhyastha, T. M. (2017). Evaluation of field map and nonlinear registration methods for correction of susceptibility artifacts in diffusion MRI. Frontiers in Neuroinformatics, 11, 17. https://doi.org/10.3389/fninf.2017.00017
   PubMed Web of Science ®Google Scholar
• Weiss, D. S., Marmar, C., Wilson, J. P., & Keane, T. (1997). Assessing psychological trauma and PTSD. Guilford Press.
   Google Scholar
• Whitfield-Gabrieli, S., & Nieto-Castanon, A. (2012). Conn: A functional connectivity toolbox for correlated and anticorrelated brain networks. Brain Connectivity, 2(3), 125–141. https://doi.org/10.1089/brain.2012.0073
   PubMedGoogle Scholar
• Zhang, Y., Brady, M., & Smith, S. (2001). Segmentation of brain MR images through a hidden Markov random field model and the expectation-maximization algorithm. IEEE Transactions on Medical Imaging, 20(1), 45–57. https://doi.org/10.1109/42.906424
   PubMed Web of Science ®Google Scholar
• Zhang, X., Lv, C. C., Tian, J., Miao, R. J., Xi, W., Hertz-Picciotto, I., & Qi, L. (2010). Prenatal and perinatal risk factors for autism in China. Journal of Autism and Developmental Disorders, 40(11), 1311–1321. https://doi.org/10.1007/s10803-010-0992-0
   PubMed Web of Science ®Google Scholar