Simultaneous and consistent labeling of longitudinal dynamic developing cortical surfaces in infants

The human cerebral cortex develops extremely dynamically in the first two years of life. Accurate and consistent parcellation of longitudinal dynamic cortical surfaces during this critical stage is essential to understand the early development of cortical structure and function in both normal and high-risk infant brains. However, directly applying the existing methods developed for the cross-sectional studies often generates longitudinally-inconsistent results, thus leading to inaccurate measurements of the cortex development. In this paper, we propose a new method for accurate, consistent, and simultaneous labeling of longitudinal cortical surfaces in the serial infant brain MR images. The proposed method is explicitly formulated as a minimization problem with an energy function that includes a data fitting term, a spatial smoothness term, and a temporal consistency term. Specifically, inspired by multi-atlas based label fusion, the data fitting term is designed to integrate the contributions from multi-atlas surfaces adaptively, according to the similarities of their local cortical folding with that of the subject cortical surface. The spatial smoothness term is then designed to adaptively encourage label smoothness based on the local cortical folding geometries, i.e. allowing label discontinuity at sulcal bottoms (which often are the boundaries of cytoarchitecturally and functionally distinct regions). The temporal consistency term is to adaptively encourage the label consistency among the temporally-corresponding vertices, based on their similarity of local cortical folding. Finally, the entire energy function is efficiently minimized by a graph cuts method. The proposed method has been applied to the parcellation of longitudinal cortical surfaces of 13 healthy infants, each with 6 serial MRI scans acquired at 0, 3, 6, 9, 12 and 18 months of age. Qualitative and quantitative evaluations demonstrated both accuracy and longitudinal consistency of the proposed method. By using our method, for the first time, we reveal several hitherto unseen properties of the dynamic and regionally heterogeneous development of the cortical surface area in the first 18 months of life

Predicting infant cortical surface development using a 4D varifold-based learning framework and local topography-based shape morphing

Longitudinal neuroimaging analysis methods have remarkably advanced our understanding of early postnatal brain development. However, learning predictive models to trace forth the evolution trajectories of both normal and abnormal cortical shapes remains broadly absent. To fill this critical gap, we pioneered the first prediction model for longitudinal developing cortical surfaces in infants using a spatiotemporal current-based learning framework solely from the baseline cortical surface. In this paper, we detail this prediction model and even further improve its performance by introducing two key variants. First, we use the varifold metric to overcome the limitations of the current metric for surface registration that was used in our preliminary study. We also extend the conventional varifold-based surface registration model for pairwise registration to a spatiotemporal surface regression model. Second, we propose a morphing process of the baseline surface using its topographic attributes such as normal direction and principal curvature sign. Specifically, our method learns from longitudinal data both the geometric (vertices positions) and dynamic (temporal evolution trajectories) features of the infant cortical surface, comprising a training stage and a prediction stage. In the training stage, we use the proposed varifold-based shape regression model to estimate geodesic cortical shape evolution trajectories for each training subject. We then build an empirical mean spatiotemporal surface atlas. In the prediction stage, given an infant, we select the best learnt features from training subjects to simultaneously predict the cortical surface shapes at all later timepoints, based on similarity metrics between this baseline surface and the learnt baseline population average surface atlas. We used a leave-one-out cross validation method to predict the inner cortical surface shape at 3, 6, 9 and 12 months of age from the baseline cortical surface shape at birth. Our method attained a higher prediction accuracy and better captured the spatiotemporal dynamic change of the highly folded cortical surface than the previous proposed prediction method

Multidirectional and Topography-based Dynamic-scale Varifold Representations with Application to Matching Developing Cortical Surfaces

The human cerebral cortex is marked by great complexity as well as substantial dynamic changes during early postnatal development. To obtain a fairly comprehensive picture of its age-induced and/or disorder-related cortical changes, one needs to match cortical surfaces to one another, while maximizing their anatomical alignment. Methods that geodesically shoot surfaces into one another as currents (a distribution of oriented normals) and varifolds (a distribution of non-oriented normals) provide an elegant Riemannian framework for generic surface matching and reliable statistical analysis. However, both conventional current and varifold matching methods have two key limitations. First, they only use the normals of the surface to measure its geometry and guide the warping process, which overlooks the importance of the orientations of the inherently convoluted cortical sulcal and gyral folds. Second, the ‘conversion’ of a surface into a current or a varifold operates at a fixed scale under which geometric surface details will be neglected, which ignores the dynamic scales of cortical foldings. To overcome these limitations and improve varifold-based cortical surface registration, we propose two different strategies. The first strategy decomposes each cortical surface into its normal and tangent varifold representations, by integrating principal curvature direction field into the varifold matching framework, thus providing rich information of the orientation of cortical folding and better characterization of the complex cortical geometry. The second strategy explores the informative cortical geometric features to perform a dynamic-scale measurement of the cortical surface that depends on the local surface topography (e.g., principal curvature), thereby we introduce the concept of a topography-based dynamic-scale varifold. We tested the proposed varifold variants for registering 12 pairs of dynamically developing cortical surfaces from 0 to 6 months of age. Both variants improved the matching accuracy in terms of closeness to the target surface and the goodness of alignment with regional anatomical boundaries, when compared with three state-of-the-art methods: (1) diffeomorphic spectral matching, (2) conventional current-based surface matching, and (3) conventional varifold-based surface matching

Computerized Analysis of Magnetic Resonance Images to Study Cerebral Anatomy in Developing Neonates

The study of cerebral anatomy in developing neonates is of great importance for the understanding of brain development during the early period of life. This dissertation therefore focuses on three challenges in the modelling of cerebral anatomy in neonates during brain development. The methods that have been developed all use Magnetic Resonance Images (MRI) as source data. To facilitate study of vascular development in the neonatal period, a set of image analysis algorithms are developed to automatically extract and model cerebral vessel trees. The whole process consists of cerebral vessel tracking from automatically placed seed points, vessel tree generation, and vasculature registration and matching. These algorithms have been tested on clinical Time-of- Flight (TOF) MR angiographic datasets. To facilitate study of the neonatal cortex a complete cerebral cortex segmentation and reconstruction pipeline has been developed. Segmentation of the neonatal cortex is not effectively done by existing algorithms designed for the adult brain because the contrast between grey and white matter is reversed. This causes pixels containing tissue mixtures to be incorrectly labelled by conventional methods. The neonatal cortical segmentation method that has been developed is based on a novel expectation-maximization (EM) method with explicit correction for mislabelled partial volume voxels. Based on the resulting cortical segmentation, an implicit surface evolution technique is adopted for the reconstruction of the cortex in neonates. The performance of the method is investigated by performing a detailed landmark study. To facilitate study of cortical development, a cortical surface registration algorithm for aligning the cortical surface is developed. The method first inflates extracted cortical surfaces and then performs a non-rigid surface registration using free-form deformations (FFDs) to remove residual alignment. Validation experiments using data labelled by an expert observer demonstrate that the method can capture local changes and follow the growth of specific sulcus

Cortical thickness and surface area in neonates at high risk for schizophrenia

Schizophrenia is a neurodevelopmental disorder associated with subtle abnormal cortical thickness and cortical surface area. However, it is unclear whether these abnormalities exist in neonates associated with genetic risk for schizophrenia. To this end, this preliminary study was conducted to identify possible abnormalities of cortical thickness and surface area in the high-genetic-risk neonates. Structural magnetic resonance images were acquired from offspring of mothers (N = 21) who had schizophrenia (N = 12) or schizoaffective disorder (N = 9), and also matched healthy neonates of mothers who were free of psychiatric illness (N = 26). Neonatal cortical surfaces were reconstructed and parcellated as regions of interest (ROIs), and cortical thickness for each vertex was computed as the shortest distance between the inner and outer surfaces. Comparisons were made for the average cortical thickness and total surface area in each of 68 cortical ROIs. After false discovery rate (FDR) correction, it was found that the female high-genetic-risk neonates had significantly thinner cortical thickness in the right lateral occipital cortex than the female control neonates. Before FDR correction, the high-genetic-risk neonates had significantly thinner cortex in the left transverse temporal gyrus, left banks of superior temporal sulcus, left lingual gyrus, right paracentral cortex, right posterior cingulate cortex, right temporal pole, and right lateral occipital cortex, compared with the control neonates. Before FDR correction, in comparison with control neonates, male high-risk neonates had significantly thicker cortex in the left frontal pole, left cuneus cortex, and left lateral occipital cortex; while female high-risk neonates had significantly thinner cortex in the bilateral paracentral, bilateral lateral occipital, left transverse temporal, left pars opercularis, right cuneus, and right posterior cingulate cortices. The high-risk neonates also had significantly smaller cortical surface area in the right pars triangularis (before FDR correction), compared with control neonates. This preliminary study provides the first evidence that early development of cortical thickness and surface area might be abnormal in the neonates at genetic risk for schizophrenia