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

IntroductionDespite 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-hemis...

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Main Authors: 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
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-12-01
Series:Frontiers in Neuroscience
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fnins.2023.1252850/full
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author Céline Steger
Céline Steger
Céline Steger
Céline Steger
Charles Moatti
Charles Moatti
Kelly Payette
Kelly Payette
Alexandra De Silvestro
Alexandra De Silvestro
Alexandra De Silvestro
Thi Dao Nguyen
Seline Coraj
Ninib Yakoub
Giancarlo Natalucci
Giancarlo Natalucci
Raimund Kottke
Ruth Tuura
Ruth Tuura
Walter Knirsch
Walter Knirsch
Andras Jakab
Andras Jakab
Andras Jakab
author_facet Céline Steger
Céline Steger
Céline Steger
Céline Steger
Charles Moatti
Charles Moatti
Kelly Payette
Kelly Payette
Alexandra De Silvestro
Alexandra De Silvestro
Alexandra De Silvestro
Thi Dao Nguyen
Seline Coraj
Ninib Yakoub
Giancarlo Natalucci
Giancarlo Natalucci
Raimund Kottke
Ruth Tuura
Ruth Tuura
Walter Knirsch
Walter Knirsch
Andras Jakab
Andras Jakab
Andras Jakab
author_sort Céline Steger
collection DOAJ
description IntroductionDespite 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.MethodsSuper-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.ResultsFetal 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.DiscussionWhile 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.
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spelling doaj.art-30128692ee6248d0bccf73455d462e202023-12-06T08:23:41ZengFrontiers Media S.A.Frontiers in Neuroscience1662-453X2023-12-011710.3389/fnins.2023.12528501252850Characterization of dynamic patterns of human fetal to neonatal brain asymmetry with deformation-based morphometryCéline Steger0Céline Steger1Céline Steger2Céline Steger3Charles Moatti4Charles Moatti5Kelly Payette6Kelly Payette7Alexandra De Silvestro8Alexandra De Silvestro9Alexandra De Silvestro10Thi Dao Nguyen11Seline Coraj12Ninib Yakoub13Giancarlo Natalucci14Giancarlo Natalucci15Raimund Kottke16Ruth Tuura17Ruth Tuura18Walter Knirsch19Walter Knirsch20Andras Jakab21Andras Jakab22Andras Jakab23Center for MR Research, University Children’s Hospital Zurich, University of Zurich, Zürich, SwitzerlandChildren’s Research Center, University Children’s Hospital Zurich, University of Zurich, Zurich, SwitzerlandPediatric Heart Center, Division of Pediatric Cardiology, University Children’s Hospital Zurich, University of Zurich, Zurich, SwitzerlandNeuroscience Center Zurich, University of Zurich and Swiss Federal Institute of Technology, Zurich, SwitzerlandCenter for MR Research, University Children’s Hospital Zurich, University of Zurich, Zürich, SwitzerlandDepartment of Information Technology and Electrical Engineering, ETH Zurich, Zurich, SwitzerlandCenter for MR Research, University Children’s Hospital Zurich, University of Zurich, Zürich, SwitzerlandChildren’s Research Center, University Children’s Hospital Zurich, University of Zurich, Zurich, SwitzerlandCenter for MR Research, University Children’s Hospital Zurich, University of Zurich, Zürich, SwitzerlandChildren’s Research Center, University Children’s Hospital Zurich, University of Zurich, Zurich, SwitzerlandPediatric Heart Center, Division of Pediatric Cardiology, University Children’s Hospital Zurich, University of Zurich, Zurich, SwitzerlandNewborn Research, Department of Neonatology, University of Zurich and University Hospital Zurich, Zurich, SwitzerlandLarsson-Rosenquist Foundation Center for Neurodevelopment, Growth and Nutrition of the Newborn, Department of Neonatology, University Hospital Zurich, University of Zurich, Zurich, SwitzerlandLarsson-Rosenquist Foundation Center for Neurodevelopment, Growth and Nutrition of the Newborn, Department of Neonatology, University Hospital Zurich, University of Zurich, Zurich, SwitzerlandNewborn Research, Department of Neonatology, University of Zurich and University Hospital Zurich, Zurich, SwitzerlandLarsson-Rosenquist Foundation Center for Neurodevelopment, Growth and Nutrition of the Newborn, Department of Neonatology, University Hospital Zurich, University of Zurich, Zurich, SwitzerlandDepartment of Diagnostic Imaging, University Children’s Hospital Zurich, University of Zurich, Zurich, SwitzerlandCenter for MR Research, University Children’s Hospital Zurich, University of Zurich, Zürich, SwitzerlandChildren’s Research Center, University Children’s Hospital Zurich, University of Zurich, Zurich, SwitzerlandChildren’s Research Center, University Children’s Hospital Zurich, University of Zurich, Zurich, SwitzerlandPediatric Heart Center, Division of Pediatric Cardiology, University Children’s Hospital Zurich, University of Zurich, Zurich, SwitzerlandCenter for MR Research, University Children’s Hospital Zurich, University of Zurich, Zürich, SwitzerlandChildren’s Research Center, University Children’s Hospital Zurich, University of Zurich, Zurich, SwitzerlandNeuroscience Center Zurich, University of Zurich and Swiss Federal Institute of Technology, Zurich, SwitzerlandIntroductionDespite 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.MethodsSuper-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.ResultsFetal 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.DiscussionWhile 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.https://www.frontiersin.org/articles/10.3389/fnins.2023.1252850/fullbrain asymmetrymagnetic resonance imaging (MRI)fetal brainneonatal brainDBM = deformation-based morphometrylongitudinal
spellingShingle Céline Steger
Céline Steger
Céline Steger
Céline Steger
Charles Moatti
Charles Moatti
Kelly Payette
Kelly Payette
Alexandra De Silvestro
Alexandra De Silvestro
Alexandra De Silvestro
Thi Dao Nguyen
Seline Coraj
Ninib Yakoub
Giancarlo Natalucci
Giancarlo Natalucci
Raimund Kottke
Ruth Tuura
Ruth Tuura
Walter Knirsch
Walter Knirsch
Andras Jakab
Andras Jakab
Andras Jakab
Characterization of dynamic patterns of human fetal to neonatal brain asymmetry with deformation-based morphometry
Frontiers in Neuroscience
brain asymmetry
magnetic resonance imaging (MRI)
fetal brain
neonatal brain
DBM = deformation-based morphometry
longitudinal
title Characterization of dynamic patterns of human fetal to neonatal brain asymmetry with deformation-based morphometry
title_full Characterization of dynamic patterns of human fetal to neonatal brain asymmetry with deformation-based morphometry
title_fullStr Characterization of dynamic patterns of human fetal to neonatal brain asymmetry with deformation-based morphometry
title_full_unstemmed Characterization of dynamic patterns of human fetal to neonatal brain asymmetry with deformation-based morphometry
title_short Characterization of dynamic patterns of human fetal to neonatal brain asymmetry with deformation-based morphometry
title_sort characterization of dynamic patterns of human fetal to neonatal brain asymmetry with deformation based morphometry
topic brain asymmetry
magnetic resonance imaging (MRI)
fetal brain
neonatal brain
DBM = deformation-based morphometry
longitudinal
url https://www.frontiersin.org/articles/10.3389/fnins.2023.1252850/full
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