Measuring the dynamic longitudinal cortex development in infants by reconstruction of temporally consistent cortical surfaces

Abstract

Quantitative measurement of the dynamic longitudinal cortex development during early postnatal stages is of great importance to understand the early cortical structural and functional development. Conventional methods usually reconstruct the cortical surfaces of longitudinal images from the same subject independently, which often generate longitudinally-inconsistent cortical surfaces and thus lead to inaccurate measurement of cortical changes, especially for vertex-wise mapping of cortical development. This paper aims to address this problem by presenting a method to reconstruct temporally-consistent cortical surfaces from longitudinal infant brain MR images, for accurate and consistent measurement of the dynamic cortex development in infants. Specifically, the longitudinal development of the inner cortical surface is first modeled by a deformable growth sheet with elasto-plasticity property to establish longitudinally smooth correspondences of the inner cortical surfaces. Then, the modeled longitudinal inner cortical surfaces are jointly deformed to locate both inner and outer cortical surfaces with a spatial-temporal deformable surface method. The method has been applied to 13 healthy infants, each with 6 serial MR scans acquired at 2 weeks, 3 months, 6 months, 9 months, 12 months and 18 months of age. Experimental results showed that our method with the incorporated longitudinal constraints can reconstruct the longitudinally-dynamic cortical surfaces from serial infant MR images more consistently and accurately than the previously published methods. By using our method, for the first time, we can characterize the vertex-wise longitudinal cortical thickness development trajectory at multiple time points in the first 18 months of life. Specifically, we found the highly age-related and regionally-heterogeneous developmental trajectories of the cortical thickness during this period, with the cortical thickness increased most from 3 to 6 months (16.2%) and least from 9 to 12 months (less than 0.1%). Specifically, the central sulcus only underwent significant increase of cortical thickness from 6 to 9 months and the occipital cortex underwent significant increase from 0 to 9 months, while the frontal, temporal and parietal cortices grew continuously in this first 18 months of life. The adult-like spatial patterns of cortical thickness were generally present at 18 months of age. These results provided detailed insights into the dynamic trajectory of the cortical thickness development in infants.

Keywords: Cortical folding; Cortical surface reconstruction; Cortical thickness; Infant; Longitudinal development.

Fig. 1

Flowchart of the proposed method for consistent reconstruction of longitudinal dynamic cortical surfaces from infant serial brain MR images.

Fig. 2

Reconstructed longitudinal inner and outer cortical surfaces of a representative infant from 2 weeks to 18 months of age by the proposed method. The first row shows the longitudinal inner (red curves) and outer (blue curves) cortical surfaces embedded in their respective image spaces. The second and third rows show the longitudinal inner and outer surfaces, respectively, color-coded by the cortical thickness.

Fig. 3

Reconstructed longitudinal outer surfaces of 6 randomly selected infants by the proposed method, each from 2 weeks to 18 months of age, color-coded by the cortical thickness. Each row indicates one infant.

Fig. 4

Average true positive (a), false positive and false negative (b) of enclosed voxels by the reconstructed inner and outer cortical surfaces using the proposed method and also the independently-reconstructed inner and outer surfaces, compared with their respective GM voxels on the 13 infants.

Fig. 5

Modeled longitudinal inner surfaces, and our reconstructed longitudinal inner surfaces and outer surfaces of a representative infant from 3 to 18 months of age, all color-coded by bidirectional surface distances (mm) compared with their respective independently-reconstructed cortical surfaces.

Fig. 6

Average bidirectional surface distances for each of 13 infants aged from 3 to 18 months, by comparing the modeled longitudinal inner surfaces (Nie et al., 2012) and our reconstructed longitudinal inner and outer surfaces with their respective independently-reconstructed cortical surfaces.

Fig. 7

An example of tissue labeling for simulated infant image sequence in the first 18 months of age.

Fig. 8

Average bidirectional surface distance errors of inner (a) and outer (b) surfaces at each time point of the simulated image sequences, compared with their corresponding “ground-truth” longitudinal cortical surfaces, for each of 13 infants.

Fig. 9

Percentages of vertices with the bidirectional surface distance errors larger than 1 voxel at each time point of the simulated image sequences, compared with their “ground-truth” cortical surfaces, for each of 13 infants. Panels (a) and (b) are results on the inner and outer cortical surfaces, respectively.

Fig. 10

Visual comparison of (a, c, e) our reconstructed longitudinal infant outer cortical surfaces from 2 weeks to 18 months of age and (b, d, f) their corresponding independently-reconstructed outer cortical surfaces, all color-coded by their cortical thickness. The yellow circles highlight the temporally inconsistent cortical morphologies in the independently-reconstructed longitudinal surfaces.

Fig. 11

Representative temporal trajectories of vertices on the reconstructed outer cortical surfaces. (a) Proposed method; (b) Proposed method without longitudinal constraint; (c) Independently-reconstructed cortical surfaces with surface-based registration.

Fig. 12

The average values of the regression residuals of (a) temporal vertex position trajectories and (b) temporal cortical-thickness trajectories of all vertices by 3 different methods in each of the 13 infants.

Fig. 13

Vertex-wise mapping of the average developmental trajectory of the cortical thickness (mm) of 13 infants from 2 weeks to 18 months of age, obtained using our proposed method. Also, the mean value and standard deviation of cortical thickness at each age, obtained from 13 infants, are shown in the top-right panel.

Fig. 14

Regions with statistically-significant cortical-thickness increase between each pair of successive time points of 13 infants from 2 weeks to 18 months of age, using TFCE (p<0.05). No region showed the statistically significant decrease of cortical thickness during the first 18 months of life.