Abstract
Preterm infants are at high risk of neurodevelopmental impairment, which may be due to altered development of brain connectivity. We aimed to (i) assess structural brain development from 25 to 45 weeks gestational age (GA) using graph theoretical approaches and (ii) test the hypothesis that preterm birth results in altered white matter network topology. Sixty-five infants underwent MRI between 25+3 and 45+6 weeks GA. Structural networks were constructed using constrained spherical deconvolution tractography and were weighted by measures of white matter microstructure (fractional anisotropy, neurite density and orientation dispersion index). We observed regional differences in brain maturation, with connections to and from deep grey matter showing most rapid developmental changes during this period. Intra-frontal, frontal to cingulate, frontal to caudate and inter-hemispheric connections matured more slowly. We demonstrated a core of key connections that was not affected by GA at birth. However, local connectivity involving thalamus, cerebellum, superior frontal lobe, cingulate gyrus and short range cortico-cortical connections was related to the degree of prematurity and contributed to altered global topology of the structural brain network. The relative preservation of core connections at the expense of local connections may support more effective use of impaired white matter reserve following preterm birth.
Highlights
The third trimester of pregnancy is associated with rapid brain development including differentiation and maturation of pre-oligodendrocytes, formation of synapses between thalamo-cortical afferents and subplate neurons, axonal growth and cortical gyrification
A positive association with age at magnetic resonance imaging (MRI) was observed in global efficiency weighted by fraction of streamlines (FS) (ρ=0.656, p < 0.001), fractional anisotropy (FA) (ρ=0.547, p < 0.001), neurite density index (NDI) (ρ=0.689, p < 0.001) and a negative association with age at MRI was observed when weighted by 1-orientation dispersion index (ODI) (ρ=−0.634, p < 0.001)
Local efficiency was positively associated with age at MRI when weighted by FS (ρ=0.610, p < 0.001), FA (ρ=0.649, p < 0.001) and NDI (ρ=0.688, p < 0.001) and negatively associated with age at MRI when weighted by 1ODI (ρ=0.688, p=0.002)
Summary
The third trimester of pregnancy is associated with rapid brain development including differentiation and maturation of pre-oligodendrocytes, formation of synapses between thalamo-cortical afferents and subplate neurons, axonal growth and cortical gyrification. The wide spectrum of disability associated with preterm birth is consistent with pervasive abnormalities in brain growth and connectivity (Back, 2015; Volpe, 2009). By studying both brain growth and connectivity, magnetic resonance imaging (MRI) has been used extensively to improve our understanding of the neural substrate underlying neurodevelopmental impairments in this population. Diffusion MRI (dMRI) has demonstrated altered white matter development in preterm infants without focal lesions (Anjari et al, 2007; Huppi et al, 1998), which is related to neurodevelopmental performance in early childhood
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