Fetal brain growth portrayed by a spatiotemporal diffusion tensor MRI atlas computed from in utero images

Abstract

Altered structural fetal brain development has been linked to neuro-developmental disorders. These structural alterations can be potentially detected in utero using diffusion tensor imaging (DTI). However, acquisition and reconstruction of in utero fetal brain DTI remains challenging. Until now, motion-robust DTI methods have been employed for reconstruction of in utero fetal DTIs. However, due to the unconstrained fetal motion and permissible in utero acquisition times, these methods yielded limited success and have typically resulted in noisy DTIs. Consequently, atlases and methods that could enable groupwise studies, multi-modality imaging, and computer-aided diagnosis from in utero DTIs have not yet been developed. This paper presents the first DTI atlas of the fetal brain computed from in utero diffusion-weighted images. For this purpose an algorithm for computing an unbiased spatiotemporal DTI atlas, which integrates kernel-regression in age with a diffeomorphic tensor-to-tensor registration of motion-corrected and reconstructed individual fetal brain DTIs, was developed. Our new algorithm was applied to a set of 67 fetal DTI scans acquired from healthy fetuses each scanned at a gestational age between 21 and 39 weeks. The neurodevelopmental trends in the fetal brain, characterized by the atlas, were qualitatively and quantitatively compared with the observations reported in prior ex vivo and in utero studies, and with results from imaging gestational-age equivalent preterm infants. Our major findings revealed early presence of limbic fiber bundles, followed by the appearance and maturation of projection pathways (characterized by an age related increase in FA) during late 2nd and early 3rd trimesters. During the 3rd trimester association fiber bundles become evident. In parallel with the appearance and maturation of fiber bundles, from 21 to 39 gestational weeks gradual disappearance of the radial coherence of the telencephalic wall was qualitatively identified. These results and analyses show that our DTI atlas of the fetal brain is useful for reliable detection of major neuronal fiber bundle pathways and for characterization of the fetal brain reorganization that occurs in utero. The atlas can also serve as a useful resource for detection of normal and abnormal fetal brain development in utero.

Brain wiring and supragranular-enriched genes linked to protracted human frontal cortex development

“…To assess whether there are deviations in the development of white matter pathways between humans and mice, we measured the volume of the frontal cortex white matter in the left hemisphere at successive stages of development in 36 humans (gestational week 36 to 18 years old) and 47 mice (P2 to P60). We used in vivo and ex vivo structural and diffusion MRI scans to capture the growth of the frontal cortex white matter in humans and in mice, respectively (Shi et al, 2011; Chuang et al, 2011; Khan et al, 2018a,b; Richardson et al, 2018). In humans as in mice, we used atlases to demarcate the white matter of the frontal cortex from the remaining cortical areas (Ding et al, 2016).…”

Simultaneous Motion and Distortion Correction Using Dual‐Echo Diffusion‐Weighted MRI

“…It has an emerging role in the assessment of neurological disorders, such as epilepsy, multiple sclerosis, Parkinson's, and Alzheimer's disease 6–8 . DW‐MRI has provided new insight into the maturation of the brain during early development, including fetal studies 9–13 and newborn studies 14,15 …”

Motion‐robust diffusion compartment imaging using simultaneous multi‐slice acquisition

“…Slice‐level motion tracking is achieved through robust slice‐to‐volume registration due to the high sampling rate of slice acquisitions in DWI, a framework for detecting and filtering motion‐corrupted slice data, and a state‐space estimation method based on method by Agamennoni et al As a method that solely relies on imaging data rather than prospectively‐designed intrinsic or extrinsic motion navigators, this technique has been successfully adopted and used in extremely challenging applications such as fetal DTI where motion effects are complex. It has also shown significant value in restoring useful information through retrospective processing of previously acquired motion‐corrupted DWI scans …”

“…It has also shown significant value in restoring useful information through retrospective processing of previously acquired motion-corrupted DWI scans. 36 In this paper, we extend a framework based on slice-level motion correction by exploiting the rigid coupling between simultaneously acquired slices for robust reconstruction in DCI. Without loss of generality, we build our reconstruction framework based upon the DIAMOND model 20 which performed well compared to other models in a recent multi-group comparison of DCI models.…”