Growth trajectories of the human fetal brain tissues estimated from 3D reconstructed in utero MRI

Biomedical Image Computing Group, Department of Radiology and Biomedical Imaging, University of California San Francisco, San Francisco, CA, USA.
International journal of developmental neuroscience: the official journal of the International Society for Developmental Neuroscience (Impact Factor: 2.58). 08/2011; 29(5):529-36. DOI: 10.1016/j.ijdevneu.2011.04.001
Source: PubMed


In the latter half of gestation (20-40 gestational weeks), human brain growth accelerates in conjunction with cortical folding and the deceleration of ventricular zone progenitor cell proliferation. These processes are reflected in changes in the volume of respective fetal tissue zones. Thus far, growth trajectories of the fetal tissue zones have been extracted primarily from 2D measurements on histological sections and magnetic resonance imaging (MRI). In this study, the volumes of major fetal zones-cortical plate (CP), subplate and intermediate zone (SP+IZ), germinal matrix (GMAT), deep gray nuclei (DG), and ventricles (VENT)--are calculated from automatic segmentation of motion-corrected, 3D reconstructed MRI. We analyzed 48 T2-weighted MRI scans from 39 normally developing fetuses in utero between 20.57 and 31.14 gestational weeks (GW). The supratentorial volume (STV) increased linearly at a rate of 15.22% per week. The SP+IZ (14.75% per week) and DG (15.56% per week) volumes increased at similar rates. The CP increased at a greater relative rate (18.00% per week), while the VENT (9.18% per week) changed more slowly. Therefore, CP increased as a fraction of STV and the VENT fraction declined. The total GMAT volume slightly increased then decreased after 25 GW. We did not detect volumetric sexual dimorphisms or total hemispheric volume asymmetries, which may emerge later in gestation. Further application of the automated fetal brain segmentation to later gestational ages will bridge the gap between volumetric studies of premature brain development and normal brain development in utero.

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Available from: Piotr Habas, Feb 26, 2014
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    • "However, until recently, challenges associated with fetal brain motion have limited the choice of MRI contrast mechanism, and achievable image resolution. Strategies for retrospective motion correction have ameliorated these limitations (Studholme, 2011) and have enabled high resolution 3D reconstructions of T 2 -weighted images throughout the second half of gestation (Kim et al., 2011; Scott et al., 2011), as well as whole-brain diffusion tensor imaging (DTI) measurements on fetal brain (Fogtmann et al., 2014). Three tissue zones, termed the germinal matrix, the subplate (SP), and the cortical plate (CP), are typically resolved in in utero MRI studies (Kim et al., 2011). "
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    ABSTRACT: Distinct populations of progenitor and postmitotic neural and glial cells are stratified in the fetal primate brain across developmentally transient tissue zones between the ventricular and pial surfaces. These zones were originally identified by light microscopy. However, it has subsequently been shown that various forms of magnetic resonance image (MRI) contrast can be used to distinguish layers of developing neural tissue in ex vivo, as well as in vivo (including in utero) conditions. Here we compare mid-gestation rhesus macaque tissue zones identified using histological techniques to ex vivo as well as in utero MRI performed on the same brains. These data are compared to mid-gestation fetal human brain MRI results, obtained in utero. We observe strong similarity between MRI contrast in vivo and post mortem, which facilitates interpretation of in utero images based on the histological characterization performed here. Additionally, we observe differential correspondence between the various forms of ex vivo MRI contrast and microscopy data, with maps of the water apparent diffusion coefficient providing the closest match to histologically-identified lamina of the nonhuman primate brain. Examination of histology and post mortem MRI helps to provide a better understanding of cytoarchitectrual characteristics that give rise to in utero MRI contrast.
    Full-text · Article · Nov 2015 · Frontiers in Neuroanatomy
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    • "This spatio-temporal atlas technique has also been used to segment the developing brain in young children and neonates (Serag et al., 2012; Murgasova et al., 2007; Kuklisova-Murgasova et al., 2011). This segmentation framework has been the basis for a number of normal (Habas et al., 2012; Rajagopalan et al., 2011; Scott et al., 2011) and abnormal (Scott et al., 2013) brain development studies in fetuses ranging from 20 to 30 weeks gestational age. EM-MRF is sufficient to segment fetuses around this gestational age range, however it fails to explicitly tackle the problem of mislabelled PV voxels at the cortical boundary and therefore it is ill-suited to segmenting older fetal brains. "
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    ABSTRACT: We automatically quantify patterns of normal cortical folding in the developing fetus from in utero MR images (N=80) over a wide gestational age (GA) range (21.7 to 38.9 weeks). This work on data from healthy subjects represents a first step towards characterising abnormal folding that may be related to pathology, facilitating earlier diagnosis and intervention. The cortical boundary was delineated by automatically segmenting the brain MR image into a number of key structures. This utilised a spatio-temporal atlas as tissue priors in an expectation-maximization approach with second order Markov random field (MRF) regularization to improve the accuracy of the cortical boundary estimate. An implicit high resolution surface was then used to compute cortical folding measures. We validated the automated segmentations with manual delineations and the average surface discrepancy was of the order of 1mm. Eight curvature-based folding measures were computed for each fetal cortex and used to give summary shape descriptors. These were strongly correlated with GA (R(2)=0.99) confirming the close link between neurological development and cortical convolution. This allowed an age-dependent non-linear model to be accurately fitted to the folding measures. The model supports visual observations that, after a slow initial start, cortical folding increases rapidly between 25 and 30 weeks and subsequently slows near birth. The model allows the accurate prediction of fetal age from an observed folding measure with a smaller error where growth is fastest. We also analysed regional patterns in folding by parcellating each fetal cortex using a nine-region anatomical atlas and found that Gompertz models fitted the change in lobar regions. Regional differences in growth rate were detected, with the parietal and posterior temporal lobe exhibiting the fastest growth, while the cingulate, frontal and medial temporal lobe developed more slowly.
    Full-text · Article · Jan 2014 · NeuroImage
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    • "With all these difficulties in mind, we can try to appreciate the WM growth by estimating its volume from T1w and T2w images acquired before and after term (Fig. 5a). In normally developing fetuses in utero, the global volume of the intermediate zone and subplate (whose frontier remains difficult to delineate) increases from around 15 to 90 cm 3 between 21 w and 31 w GA, i.e. 15% per week (Scott et al., 2011). In premature neonates, the WM volume increases from around 50 cm 3 at 29 w GA to 170 cm 3 at 44 w GA, as reported in age-specific atlases (Kuklisova-Murgasova et al., 2011). "
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    ABSTRACT: Studying how the healthy human brain develops is important to understand early pathological mechanisms and to assess the influence of fetal or perinatal events on later life. Brain development relies on complex and intermingled mechanisms especially during gestation and first post-natal months, with intense interactions between genetic, epigenetic and environmental factors. Although the baby's brain is organized early on, it is not a miniature adult brain: regional brain changes are asynchronous and protracted, i.e. sensory-motor regions develop early and quickly, whereas associative regions develop later and slowly over decades. Concurrently, the infant/child gradually achieves new performances, but how brain maturation relates to changes in behaviour is poorly understood, requiring non-invasive in vivo imaging studies such as MRI. Two main processes of early white matter development are reviewed: 1) establishment of connections between brain regions within functional networks, leading to adult-like organisation during the last trimester of gestation, 2) maturation (myelination) of these connections during infancy to provide efficient transfers of information. Current knowledge from post-mortem descriptions and in vivo MRI studies is summed up, focusing on T1- and T2-weighted imaging, diffusion tensor imaging, and quantitative mapping of T1/T2 relaxation times, myelin water fraction and magnetization transfer ratio.
    Full-text · Article · Dec 2013 · Neuroscience
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