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Preterm birth leads to impaired rich-club organization and fronto-paralimbic/limbic structural connectivity in newborns

Lordier, Lara
Published in NeuroImage. 2021, vol. 225, 117440
Abstract Prematurity disrupts brain development during a critical period of brain growth and organization and is known to be associated with an increased risk of neurodevelopmental impairments. Investigating whole-brain structural connectivity alterations accompanying preterm birth may provide a better comprehension of the neurobiological mechanisms related to the later neurocognitive deficits observed in this population. Using a connectome approach, we aimed to study the impact of prematurity on neonatal whole-brain structural network organization at term-equivalent age. In this cohort study, twenty-four very preterm infants at term-equivalent age (VPT-TEA) and fourteen full-term (FT) newborns underwent a brain MRI exam at term age, comprising T2-weighted imaging and diffusion MRI, used to reconstruct brain connectomes by applying probabilistic constrained spherical deconvolution whole-brain tractography. The topological properties of brain networks were quantified through a graph-theoretical approach. Furthermore, edge-wise connectivity strength was compared between groups. Overall, VPT-TEA infants' brain networks evidenced increased segregation and decreased integration capacity, revealed by an increased clustering coefficient, increased modularity, increased characteristic path length, decreased global efficiency and diminished rich-club coefficient. Furthermore, in comparison to FT, VPT-TEA infants had decreased connectivity strength in various cortico-cortical, cortico-subcortical and intra-subcortical networks, the majority of them being intra-hemispheric fronto-paralimbic and fronto-limbic. Inter-hemispheric connectivity was also decreased in VPT-TEA infants, namely through connections linking to the left precuneus or left dorsal cingulate gyrus - two regions that were found to be hubs in FT but not in VPT-TEA infants. Moreover, posterior regions from Default-Mode-Network (DMN), namely precuneus and posterior cingulate gyrus, had decreased structural connectivity in VPT-TEA group. Our finding that VPT-TEA infants' brain networks displayed increased modularity, weakened rich-club connectivity and diminished global efficiency compared to FT infants suggests a delayed transition from a local architecture, focused on short-range connections, to a more distributed architecture with efficient long-range connections in those infants. The disruption of connectivity in fronto-paralimbic/limbic and posterior DMN regions might underlie the behavioral and social cognition difficulties previously reported in the preterm population.
Keywords Brain/diagnostic imaging/growth & development/physiopathologyCase-Control StudiesConnectomeFemaleFunctional NeuroimagingGestational AgeGyrus Cinguli/diagnostic imaging/growth & development/physiopathologyHumansInfantNewbornInfantPrematureMagnetic Resonance ImagingMaleNeural Pathways/diagnostic imaging/growth & development/physiopathologyParietal Lobe/diagnostic imaging/growth & development/physiopathologyThalamus/diagnostic imaging/growth & development/physiopathology
PMID: 33039621
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Research groups Groupe Lazeyras Francois (IRM fonctionnelle et métabolique) (539)
L'imagerie cérébrale (184)
Swiss National Science Foundation: 32473B_135817
Swiss National Science Foundation: 324730_163084
European Commission: EuroPOND
(ISO format)
ALVES SA DE ALMEIDA, Joana Rita et al. Preterm birth leads to impaired rich-club organization and fronto-paralimbic/limbic structural connectivity in newborns. In: NeuroImage, 2021, vol. 225, p. 117440. doi: 10.1016/j.neuroimage.2020.117440 https://archive-ouverte.unige.ch/unige:155481

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Deposited on : 2021-10-18

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