Characterization of dynamic patterns of human fetal to neonatal brain asymmetry with deformation-based morphometry

Céline Steger; Charles Moatti; Kelly Payette; Alexandra De Silvestro; Thi Dao Nguyen; Seline Coraj; Ninib Yakoub; Giancarlo Natalucci; Raimund Kottke; Ruth Tuura; Walter Knirsch; Andras Jakab

doi:10.3389/fnins.2023.1252850

Characterization of dynamic patterns of human fetal to neonatal brain asymmetry with deformation-based morphometry

Front Neurosci. 2023 Dec 6:17:1252850. doi: 10.3389/fnins.2023.1252850. eCollection 2023.

Authors

Céline Steger^{1

2

3

4}, Charles Moatti^{1

5}, Kelly Payette^{1

2}, Alexandra De Silvestro^{1

2

3}, Thi Dao Nguyen⁶, Seline Coraj⁷, Ninib Yakoub⁷, Giancarlo Natalucci^{6

7}, Raimund Kottke⁸, Ruth Tuura^{1

2}, Walter Knirsch^{2

3}, Andras Jakab^{1

2

4}

Affiliations

¹ Center for MR Research, University Children's Hospital Zurich, University of Zurich, Zürich, Switzerland.
² Children's Research Center, University Children's Hospital Zurich, University of Zurich, Zurich, Switzerland.
³ Pediatric Heart Center, Division of Pediatric Cardiology, University Children's Hospital Zurich, University of Zurich, Zurich, Switzerland.
⁴ Neuroscience Center Zurich, University of Zurich and Swiss Federal Institute of Technology, Zurich, Switzerland.
⁵ Department of Information Technology and Electrical Engineering, ETH Zurich, Zurich, Switzerland.
⁶ Newborn Research, Department of Neonatology, University of Zurich and University Hospital Zurich, Zurich, Switzerland.
⁷ Larsson-Rosenquist Foundation Center for Neurodevelopment, Growth and Nutrition of the Newborn, Department of Neonatology, University Hospital Zurich, University of Zurich, Zurich, Switzerland.
⁸ Department of Diagnostic Imaging, University Children's Hospital Zurich, University of Zurich, Zurich, Switzerland.

Abstract

Introduction: Despite established knowledge on the morphological and functional asymmetries in the human brain, the understanding of how brain asymmetry patterns change during late fetal to neonatal life remains incomplete. The goal of this study was to characterize the dynamic patterns of inter-hemispheric brain asymmetry over this critically important developmental stage using longitudinally acquired MRI scans.

Methods: Super-resolution reconstructed T2-weighted MRI of 20 neurotypically developing participants were used, and for each participant fetal and neonatal MRI was acquired. To quantify brain morphological changes, deformation-based morphometry (DBM) on the longitudinal MRI scans was utilized. Two registration frameworks were evaluated and used in our study: (A) fetal to neonatal image registration and (B) registration through a mid-time template. Developmental changes of cerebral asymmetry were characterized as (A) the inter-hemispheric differences of the Jacobian determinant (JD) of fetal to neonatal morphometry change and the (B) time-dependent change of the JD capturing left-right differences at fetal or neonatal time points. Left-right and fetal-neonatal differences were statistically tested using multivariate linear models, corrected for participants' age and sex and using threshold-free cluster enhancement.

Results: Fetal to neonatal morphometry changes demonstrated asymmetry in the temporal pole, and left-right asymmetry differences between fetal and neonatal timepoints revealed temporal changes in the temporal pole, likely to go from right dominant in fetal to a bilateral morphology in neonatal timepoint. Furthermore, the analysis revealed right-dominant subcortical gray matter in neonates and three clusters of increased JD values in the left hemisphere from fetal to neonatal timepoints.

Discussion: While these findings provide evidence that morphological asymmetry gradually emerges during development, discrepancies between registration frameworks require careful considerations when using DBM for longitudinal data of early brain development.

Keywords: DBM = deformation-based morphometry; brain asymmetry; fetal brain; longitudinal; magnetic resonance imaging (MRI); neonatal brain.

Grants and funding

This work was supported by the Swiss National Science Foundation (SNSF 320030_184932, PZOOP3_161146, and 200886), the Anna Mueller Grocholski Foundation, the EMDO Foundation, the Prof. Max Cloetta Foundation, and the Vontobel Foundation.