The dynamics of cortical folding waves and prematurity-related deviations revealed by spatial and spectral analysis of gyrification

Abstract

In the human brain, the appearance of cortical sulci is a complex process that takes place mostly during the second half of pregnancy, with a relatively stable temporal sequence across individuals. Since deviant gyrification patterns have been observed in many neurodevelopmental disorders, mapping cortical development in vivo from the early stages on is an essential step to uncover new markers for diagnosis or prognosis. Recently this has been made possible by MRI combined with post-processing tools, but the reported results are still fragmented. Here we aimed to characterize the typical folding progression ex utero from the pre- to the post-term period, by considering 58 healthy preterm and full-term newborns and infants imaged between 27 and 62 weeks of post-menstrual age. Using a method of spectral analysis of gyrification (SPANGY), we detailed the spatial-frequency structure of cortical patterns in a quantitative way. The modeling of developmental trajectories revealed three successive waves that might correspond to primary, secondary and tertiary folding. Some deviations were further detected in 10 premature infants without apparent neurological impairment and imaged at term equivalent age, suggesting that our approach is sensitive enough to highlight the subtle impact of preterm birth and extra-uterine life on folding.

Fetal cortical surface atlas parcellation based on growth patterns

“…For each cluster on both hemispheres, we showed its growth trend and growth rate (per week) of surface area. To determine which function can more accurately model the growth trends that reflect the relationship between surface area and gestational weeks, we have used three previously‐adopted models, that is, a quadratic function (Clouchoux, Du Plessis, et al, ), a Gompertz function (Dubois et al, ; Wright et al, ), and a linear function (Garcia et al, ), to fit the growth trend in each cluster. From Table , we found that overall the quadratic function was best to fit the growth trends (with highest R 2 values) during 26–29 GW.…”

“…For large temporal intervals during fetal brain development with potential nonlinear growth patterns (Clouchoux, Du Plessis, et al, ; Dubois et al, ), the Pearson's correlation coefficient might not be the best method for measuring similarity, although some researchers have used the linear function to model the development trajectories of fetal cortical surface (Garcia et al, ). In this case, researchers can instead use other measures, for example, the Spearman's rank correlation coefficient, which can measure nonlinear correlations.…”

“…Our parcellation results showed that it might be more suitable to use the Pearson's correlation coefficient to measure the similarity of growth patterns during 26–29 GW. A possible reason could be the relatively small range of age and accelerative development patterns during this stage, which renders the development patterns of surface area close to linear (Clouchoux, Kudelski, et al, ; Dubois et al, ).…”

“…Herein, we adopt another widely used method to compute the local surface area (Garcia et al, 2018;, which can be easily comparable across subjects at each vertex. Specifically, we first resampled all For large temporal intervals during fetal brain development with potential nonlinear growth patterns (Clouchoux, Du Plessis, et al, 2012;Dubois et al, 2018), the Pearson's correlation coefficient might not be the best method for measuring similarity, although some researchers have used the linear function to model the development trajectories of fetal cortical surface (Garcia et al, 2018) (Clouchoux, Kudelski, et al, 2012;Dubois et al, 2018).…”

“…Overall, during the latter half of gestation, the complexity of the cortical plate increases following a highly orchestrated sequence of sulcal-gyral formation (Clouchoux, Kudelski, et al, 2012;Rajagopalan et al, 2011;Wright et al, 2014). In particular, this sequence occurs in a hierarchical manner, in which primary and secondary sulci form in a consistent spatiotemporal pattern (Dubois et al, 2018;Wright et al, 2015), followed by tertiary folds that show increasing variability across individuals (Bendersky et al, 2006;Studholme, 2011).…”