Abstract
IntroductionThe dynamic nature and complexity of the cellular events that take place during the last trimester of pregnancy make the developing cortex particularly vulnerable to perturbations. Abrupt interruption to normal gestation can lead to significant deviations to many of these processes, resulting in atypical trajectory of cortical maturation in preterm birth survivors. MethodsWe sought to first map typical cortical micro- and macrostructure development using invivo MRI in a large sample of healthy term-born infants scanned after birth (n = 259). Then we offer a comprehensive characterization of the cortical consequences of preterm birth in 76 preterm infants scanned at term-equivalent age (37–44 weeks postmenstrual age). We describe the group-average atypicality, the heterogeneity across individual preterm infants, and relate individual deviations from normative development to age at birth and neurodevelopment at 18 months. ResultsIn the term-born neonatal brain, we observed heterogeneous and regionally specific associations between age at scan and measures of cortical morphology and microstructure, including rapid surface expansion, greater cortical thickness, lower cortical anisotropy and higher neurite orientation dispersion. By term-equivalent age, preterm infants had on average increased cortical tissue water content and reduced neurite density index in the posterior parts of the cortex, and greater cortical thickness anteriorly compared to term-born infants. While individual preterm infants were more likely to show extreme deviations (over 3.1 standard deviations) from normative cortical maturation compared to term-born infants, these extreme deviations were highly variable and showed very little spatial overlap between individuals. Measures of regional cortical development were associated with age at birth, but not with neurodevelopment at 18 months. ConclusionWe showed that preterm birth alters cortical micro- and macrostructural maturation near the time of full-term birth. Deviations from normative development were highly variable between individual preterm infants.
Highlights
The dynamic nature and complexity of the cellular events that take place during the last trimester of pregnancy make the developing cortex vulnerable to perturbations
Very few parcels showed group differences in fractional anisotropy (FA), Orientation Dispersion index (ODI) and surface area (SA), but the spatial overlap maps were indicative of widespread individual deviations in extreme positive FA, negative ODI and positive/negative SA deviations
There were very few parcels across all metrics with more than 8% of the infants showing extreme deviations highlighting the high variability in cortical development associated with preterm birth
Summary
The dynamic nature and complexity of the cellular events that take place during the last trimester of pregnancy make the developing cortex vulnerable to perturbations. We offer a comprehensive characterization of the cortical consequences of preterm birth in 76 preterm infants scanned at term-equivalent age (37–44 weeks postmenstrual age). While individual preterm infants were more likely to show extreme deviations (over 3.1 standard deviations) from normative cortical maturation compared to term-born infants, these extreme deviations were highly variable and Abbreviations: BSID-III, Bayley III Scales of Infant and Toddler Development; dHCP, developing Human Connectome Project; dMRI, diffusion MRI; FA, fractional anisotropy; fICVF, intracellular volume fraction; GA, gestational age; GPR, gaussian process regression; MAE, mean absolute error; MD, mean diffusivity; MRI, magnetic resonance imaging; MSE, mean squared error; MSM, multimodal surface matching; NODDI, Neurite Orientation Dispersion and Density Imaging; ODI, orientation dispersion index; PALM, Permutation Analysis of Linear Models; PMA, postmenstrual age; PWMLs, punctate WM lessions; RF, random forest; SA, surface area; TEA, term-equivalent age; WM, white matter. A comprehensive characterization of the cortical sequelae of preterm birth compared to normative development is necessary to better understand the role of cortical (dys)maturation in the encephalopathy of prematurity
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