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

Abstract

AbstractA 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.