Abstract

The human brain grows the most dramatically during the perinatal and early post-natal periods, during which pre-term birth or perinatal injury that may alter brain structure and lead to developmental anomalies. Thus, characterizing cortical thickness of developing brains remains an important goal. However, this task is often complicated by inaccurate cortical surface extraction due to small-size brains. Here, we propose a novel complex framework for the reconstruction of neonatal WM and pial surfaces, accounting for large partial volumes due to small-size brains. The proposed approach relies only on T1-weighted images unlike previous T2-weighted image-based approaches while only T1-weighted images are sometimes available under the different clinical/research setting. Deep neural networks are first introduced to the neonatal magnetic resonance imaging (MRI) pipeline to address the mis-segmentation of brain tissues. Furthermore, this pipeline enhances cortical boundary delineation using combined models of the cerebrospinal fluid (CSF)/GM boundary detection with edge gradient information and a new skeletonization of sulcal folding where no CSF voxels are seen due to the limited resolution. We also proposed a systematic evaluation using three independent datasets comprising 736 pre-term and 97 term neonates. Qualitative assessment for reconstructed cortical surfaces shows that 86.9% are rated as accurate across the three site datasets. In addition, our landmark-based evaluation shows that the mean displacement of the cortical surfaces from the true boundaries was less than a voxel size (0.532 ± 0.035 mm). Evaluating the proposed pipeline (namely NEOCIVET 2.0) shows the robustness and reproducibility across different sites and different age-groups. The mean cortical thickness measured positively correlated with post-menstrual age (PMA) at scan (p < 0.0001); Cingulate cortical areas grew the most rapidly whereas the inferior temporal cortex grew the least rapidly. The range of the cortical thickness measured was biologically congruent (1.3 mm at 28 weeks of PMA to 1.8 mm at term equivalent). Cortical thickness measured on T1 MRI using NEOCIVET 2.0 was compared with that on T2 using the established dHCP pipeline. It was difficult to conclude that either T1 or T2 imaging is more ideal to construct cortical surfaces. NEOCIVET 2.0 has been open to the public through CBRAIN (https://mcin-cnim.ca/technology/cbrain/), a web-based platform for processing brain imaging data.

Highlights

  • The human brain grows the most dramatically during the perinatal and post-natal periods (Knickmeyer et al, 2008), where the majority of cortical growth and folding partition the brain for various sophisticated functions (Alexander-Bloch et al, 2018)

  • Our new framework extended upon the NEOCIVET 1.0 pipeline (Kim et al, 2016) which was designed for neonatal WM surface (WM-GM interface) reconstruction and measurement of sulcal depths

  • We propose a new NEOCIVET pipeline (NEOCIVET 2.0) for automatically reconstructing neonatal WM and pial surfaces

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Summary

Introduction

The human brain grows the most dramatically during the perinatal and post-natal periods (Knickmeyer et al, 2008), where the majority of cortical growth and folding partition the brain for various sophisticated functions (Alexander-Bloch et al, 2018) This critical time window of neurodevelopment is susceptible to developmental anomalies, such as pre-term birth or perinatal injuries. Unlike MRI methods implemented to study the adult brain, MRI methods and processing frameworks for the neonatal brain are still under investigation in order to circumvent substantial challenges, such as opposite/reduced tissue contrast between WM and GM, large within-tissue intensity variations, and regionally heterogeneous image appearances that dynamically change in accordance with neural development These challenges lead to significant difficulties in quantifying cortical morphology measurements, including cortical thickness, surface curvature, and sulcal depth, which demand accurate surface reconstruction methods. These methods provide only the successful reconstruction of the inner cortical surface, while remaining incapable of robustly measuring cortical thickness, which is a crucial morphological characteristic of brain development (Raznahan et al, 2011a)

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