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Hemispheric lateralization of white matter microstructure in children and its potential role in sensory processing dysfunction

Diffusion tensor imaging (DTI) studies have demonstrated white matter microstructural differences between the left and right hemispheres of the brain. However, the basis of these hemispheric asymmetries is not yet understood in terms of the biophysical properties of white matter microstructure, espe...

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Autores principales: Parekh, Shalin A., Wren-Jarvis, Jamie, Lazerwitz, Maia, Rowe, Mikaela A., Powers, Rachel, Bourla, Ioanna, Cai, Lanya T., Chu, Robyn, Trimarchi, Kaitlyn, Garcia, Rafael, Marco, Elysa J., Mukherjee, Pratik
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10149818/
https://www.ncbi.nlm.nih.gov/pubmed/37139524
http://dx.doi.org/10.3389/fnins.2023.1088052
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author Parekh, Shalin A.
Wren-Jarvis, Jamie
Lazerwitz, Maia
Rowe, Mikaela A.
Powers, Rachel
Bourla, Ioanna
Cai, Lanya T.
Chu, Robyn
Trimarchi, Kaitlyn
Garcia, Rafael
Marco, Elysa J.
Mukherjee, Pratik
author_facet Parekh, Shalin A.
Wren-Jarvis, Jamie
Lazerwitz, Maia
Rowe, Mikaela A.
Powers, Rachel
Bourla, Ioanna
Cai, Lanya T.
Chu, Robyn
Trimarchi, Kaitlyn
Garcia, Rafael
Marco, Elysa J.
Mukherjee, Pratik
author_sort Parekh, Shalin A.
collection PubMed
description Diffusion tensor imaging (DTI) studies have demonstrated white matter microstructural differences between the left and right hemispheres of the brain. However, the basis of these hemispheric asymmetries is not yet understood in terms of the biophysical properties of white matter microstructure, especially in children. There are reports of altered hemispheric white matter lateralization in ASD; however, this has not been studied in other related neurodevelopmental disorders such as sensory processing disorder (SPD). Firstly, we postulate that biophysical compartment modeling of diffusion MRI (dMRI), such as Neurite Orientation Dispersion and Density Imaging (NODDI), can elucidate the hemispheric microstructural asymmetries observed from DTI in children with neurodevelopmental concerns. Secondly, we hypothesize that sensory over-responsivity (SOR), a common type of SPD, will show altered hemispheric lateralization relative to children without SOR. Eighty-seven children (29 females, 58 males), ages 8–12 years, presenting at a community-based neurodevelopmental clinic were enrolled, 48 with SOR and 39 without. Participants were evaluated using the Sensory Processing 3 Dimensions (SP3D). Whole brain 3 T multi-shell multiband dMRI (b = 0, 1,000, 2,500 s/mm(2)) was performed. Tract Based Spatial Statistics were used to extract DTI and NODDI metrics from 20 bilateral tracts of the Johns Hopkins University White-Matter Tractography Atlas and the lateralization Index (LI) was calculated for each left–right tract pair. With DTI metrics, 12 of 20 tracts were left lateralized for fractional anisotropy and 17/20 tracts were right lateralized for axial diffusivity. These hemispheric asymmetries could be explained by NODDI metrics, including neurite density index (18/20 tracts left lateralized), orientation dispersion index (15/20 tracts left lateralized) and free water fraction (16/20 tracts lateralized). Children with SOR served as a test case of the utility of studying LI in neurodevelopmental disorders. Our data demonstrated increased lateralization in several tracts for both DTI and NODDI metrics in children with SOR, which were distinct for males versus females, when compared to children without SOR. Biophysical properties from NODDI can explain the hemispheric lateralization of white matter microstructure in children. As a patient-specific ratio, the lateralization index can eliminate scanner-related and inter-individual sources of variability and thus potentially serve as a clinically useful imaging biomarker for neurodevelopmental disorders.
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spelling pubmed-101498182023-05-02 Hemispheric lateralization of white matter microstructure in children and its potential role in sensory processing dysfunction Parekh, Shalin A. Wren-Jarvis, Jamie Lazerwitz, Maia Rowe, Mikaela A. Powers, Rachel Bourla, Ioanna Cai, Lanya T. Chu, Robyn Trimarchi, Kaitlyn Garcia, Rafael Marco, Elysa J. Mukherjee, Pratik Front Neurosci Neuroscience Diffusion tensor imaging (DTI) studies have demonstrated white matter microstructural differences between the left and right hemispheres of the brain. However, the basis of these hemispheric asymmetries is not yet understood in terms of the biophysical properties of white matter microstructure, especially in children. There are reports of altered hemispheric white matter lateralization in ASD; however, this has not been studied in other related neurodevelopmental disorders such as sensory processing disorder (SPD). Firstly, we postulate that biophysical compartment modeling of diffusion MRI (dMRI), such as Neurite Orientation Dispersion and Density Imaging (NODDI), can elucidate the hemispheric microstructural asymmetries observed from DTI in children with neurodevelopmental concerns. Secondly, we hypothesize that sensory over-responsivity (SOR), a common type of SPD, will show altered hemispheric lateralization relative to children without SOR. Eighty-seven children (29 females, 58 males), ages 8–12 years, presenting at a community-based neurodevelopmental clinic were enrolled, 48 with SOR and 39 without. Participants were evaluated using the Sensory Processing 3 Dimensions (SP3D). Whole brain 3 T multi-shell multiband dMRI (b = 0, 1,000, 2,500 s/mm(2)) was performed. Tract Based Spatial Statistics were used to extract DTI and NODDI metrics from 20 bilateral tracts of the Johns Hopkins University White-Matter Tractography Atlas and the lateralization Index (LI) was calculated for each left–right tract pair. With DTI metrics, 12 of 20 tracts were left lateralized for fractional anisotropy and 17/20 tracts were right lateralized for axial diffusivity. These hemispheric asymmetries could be explained by NODDI metrics, including neurite density index (18/20 tracts left lateralized), orientation dispersion index (15/20 tracts left lateralized) and free water fraction (16/20 tracts lateralized). Children with SOR served as a test case of the utility of studying LI in neurodevelopmental disorders. Our data demonstrated increased lateralization in several tracts for both DTI and NODDI metrics in children with SOR, which were distinct for males versus females, when compared to children without SOR. Biophysical properties from NODDI can explain the hemispheric lateralization of white matter microstructure in children. As a patient-specific ratio, the lateralization index can eliminate scanner-related and inter-individual sources of variability and thus potentially serve as a clinically useful imaging biomarker for neurodevelopmental disorders. Frontiers Media S.A. 2023-04-17 /pmc/articles/PMC10149818/ /pubmed/37139524 http://dx.doi.org/10.3389/fnins.2023.1088052 Text en Copyright © 2023 Parekh, Wren-Jarvis, Lazerwitz, Rowe, Powers, Bourla, Cai, Chu, Trimarchi, Garcia, Marco and Mukherjee. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Neuroscience
Parekh, Shalin A.
Wren-Jarvis, Jamie
Lazerwitz, Maia
Rowe, Mikaela A.
Powers, Rachel
Bourla, Ioanna
Cai, Lanya T.
Chu, Robyn
Trimarchi, Kaitlyn
Garcia, Rafael
Marco, Elysa J.
Mukherjee, Pratik
Hemispheric lateralization of white matter microstructure in children and its potential role in sensory processing dysfunction
title Hemispheric lateralization of white matter microstructure in children and its potential role in sensory processing dysfunction
title_full Hemispheric lateralization of white matter microstructure in children and its potential role in sensory processing dysfunction
title_fullStr Hemispheric lateralization of white matter microstructure in children and its potential role in sensory processing dysfunction
title_full_unstemmed Hemispheric lateralization of white matter microstructure in children and its potential role in sensory processing dysfunction
title_short Hemispheric lateralization of white matter microstructure in children and its potential role in sensory processing dysfunction
title_sort hemispheric lateralization of white matter microstructure in children and its potential role in sensory processing dysfunction
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10149818/
https://www.ncbi.nlm.nih.gov/pubmed/37139524
http://dx.doi.org/10.3389/fnins.2023.1088052
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