Maternal anxiety-driven modulation of fetal limbic connectivity designs a backbone linking neonatal brain functional topology to socio-emotional development in early childhood.

Publisher: Wiley Interscience Country of Publication: United States NLM ID: 7600111 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1097-4547 (Electronic) Linking ISSN: 03604012 NLM ISO Abbreviation: J Neurosci Res Subsets: MEDLINE

Publication: New York, NY : Wiley Interscience
Original Publication: New York, Liss.

Magnetic Resonance Imaging* ; Brain*/pathology; Infant, Newborn ; Female ; Pregnancy ; Humans ; Child, Preschool ; Emotions ; Fetus ; Anxiety

A link between maternal anxiety during pregnancy and adverse socio-emotional outcomes in childhood has been consistently sustained on the very early neurodevelopmental alteration of structural pathways between fetal limbic and cortical brain regions. In this study, we provide follow-up evidence for a feed-forward model linking (i) maternal anxiety, (ii) fetal functional neurodevelopment, (iii) neonatal functional network organization with (iv) socio-emotional neurobehavioral development in early childhood. Namely, we investigate a sample of 16 mother-fetus dyads and show how a maternal state-trait anxiety profile with pregnancy-specific worries can significantly influence functional synchronization patterns between regions of the fetal limbic system (i.e., hippocampus and amygdala) and the neocortex, as assessed through resting-state functional magnetic resonance imaging. Generalization of the findings was supported by leave-one-out cross-validation. We further show how this maternal-fetal cross-talk propagates to functional network topology in the neonate, specifically targeting connector hubs, and further maps onto socio-emotional profiles, assessed through Bayley-III socio-emotional scale in early childhood (i.e., in the 12-24 months range). Based on this evidence, we put forward the hypothesis of a "Maternal-Fetal-Neonatal Anxiety Backbone", through which neurobiological changes driven by maternal anxiety could trigger a divergence in the establishment of a cognitive-emotional development blueprint, in terms of the nascent functional homeostasis between bottom-up limbic and top-down higher-order neuronal circuitry.
(© 2023 The Authors. Journal of Neuroscience Research published by Wiley Periodicals LLC.)

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Keywords: anxiety; fMRI; neurodevelopment; pregnancy; socio-emotional

Date Created: 20230614 Date Completed: 20230725 Latest Revision: 20230730

20231215

10.1002/jnr.25207

37313950