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

Published inNeuroImage, vol. 225, 117440
Publication date2021
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/physiopathology
  • Case-Control Studies
  • Connectome
  • Female
  • Functional Neuroimaging
  • Gestational Age
  • Gyrus Cinguli/diagnostic imaging/growth & development/physiopathology
  • Humans
  • Infant
  • Newborn
  • Infant
  • Premature
  • Magnetic Resonance Imaging
  • Male
  • Neural Pathways/diagnostic imaging/growth & development/physiopathology
  • Parietal Lobe/diagnostic imaging/growth & development/physiopathology
  • Thalamus/diagnostic imaging/growth & development/physiopathology
Citation (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
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Identifiers
ISSN of the journal1053-8119
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Technical informations

Creation10/15/2021 3:05:00 PM
First validation10/15/2021 3:05:00 PM
Update time03/16/2023 1:31:56 AM
Status update03/16/2023 1:31:55 AM
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