Atypical developmental trajectories of white matter microstructure in prenatal alcohol exposure: Preliminary evidence from neurite orientation dispersion and density imaging

IntroductionFetal alcohol spectrum disorder (FASD), a life-long condition resulting from prenatal alcohol exposure (PAE), is associated with structural brain anomalies and neurobehavioral differences. Evidence from longitudinal neuroimaging suggest trajectories of white matter microstructure maturat...

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Main Authors: Blake A. Gimbel, Donovan J. Roediger, Abigail M. Ernst, Mary E. Anthony, Erik de Water, Madeline N. Rockhold, Bryon A. Mueller, Sarah N. Mattson, Kenneth L. Jones, Edward P. Riley, Kelvin O. Lim, CIFASD, Jeffrey R. Wozniak
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Language:English
Published: Frontiers Media S.A. 2023-04-01
Series:Frontiers in Neuroscience
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Online Access:https://www.frontiersin.org/articles/10.3389/fnins.2023.1172010/full
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author Blake A. Gimbel
Donovan J. Roediger
Abigail M. Ernst
Mary E. Anthony
Erik de Water
Madeline N. Rockhold
Bryon A. Mueller
Sarah N. Mattson
Kenneth L. Jones
Edward P. Riley
Kelvin O. Lim
CIFASD
Jeffrey R. Wozniak
author_facet Blake A. Gimbel
Donovan J. Roediger
Abigail M. Ernst
Mary E. Anthony
Erik de Water
Madeline N. Rockhold
Bryon A. Mueller
Sarah N. Mattson
Kenneth L. Jones
Edward P. Riley
Kelvin O. Lim
CIFASD
Jeffrey R. Wozniak
author_sort Blake A. Gimbel
collection DOAJ
description IntroductionFetal alcohol spectrum disorder (FASD), a life-long condition resulting from prenatal alcohol exposure (PAE), is associated with structural brain anomalies and neurobehavioral differences. Evidence from longitudinal neuroimaging suggest trajectories of white matter microstructure maturation are atypical in PAE. We aimed to further characterize longitudinal trajectories of developmental white matter microstructure change in children and adolescents with PAE compared to typically-developing Controls using diffusion-weighted Neurite Orientation Dispersion and Density Imaging (NODDI).Materials and methodsParticipants: Youth with PAE (n = 34) and typically-developing Controls (n = 31) ages 8–17 years at enrollment. Participants underwent formal evaluation of growth and facial dysmorphology. Participants also completed two study visits (17 months apart on average), both of which involved cognitive testing and an MRI scan (data collected on a Siemens Prisma 3 T scanner). Age-related changes in the orientation dispersion index (ODI) and the neurite density index (NDI) were examined across five corpus callosum (CC) regions defined by tractography.ResultsWhile linear trajectories suggested similar overall microstructural integrity in PAE and Controls, analyses of symmetrized percent change (SPC) indicated group differences in the timing and magnitude of age-related increases in ODI (indexing the bending and fanning of axons) in the central region of the CC, with PAE participants demonstrating atypically steep increases in dispersion with age compared to Controls. Participants with PAE also demonstrated greater increases in ODI in the mid posterior CC (trend-level group difference). In addition, SPC in ODI and NDI was differentially correlated with executive function performance for PAE participants and Controls, suggesting an atypical relationship between white matter microstructure maturation and cognitive function in PAE.DiscussionPreliminary findings suggest subtle atypicality in the timing and magnitude of age-related white matter microstructure maturation in PAE compared to typically-developing Controls. These findings add to the existing literature on neurodevelopmental trajectories in PAE and suggest that advanced biophysical diffusion modeling (NODDI) may be sensitive to biologically-meaningful microstructural changes in the CC that are disrupted by PAE. Findings of atypical brain maturation-behavior relationships in PAE highlight the need for further study. Further longitudinal research aimed at characterizing white matter neurodevelopmental trajectories in PAE will be important.
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spelling doaj.art-5c7532a3c4d44ffeaba0b592feacd3922023-04-24T04:21:53ZengFrontiers Media S.A.Frontiers in Neuroscience1662-453X2023-04-011710.3389/fnins.2023.11720101172010Atypical developmental trajectories of white matter microstructure in prenatal alcohol exposure: Preliminary evidence from neurite orientation dispersion and density imagingBlake A. Gimbel0Donovan J. Roediger1Abigail M. Ernst2Mary E. Anthony3Erik de Water4Madeline N. Rockhold5Bryon A. Mueller6Sarah N. Mattson7Kenneth L. Jones8Edward P. Riley9Kelvin O. Lim10CIFASDJeffrey R. Wozniak11Department of Psychiatry and Behavioral Sciences, University of Minnesota Twin Cities, Minneapolis, MN, United StatesDepartment of Psychiatry and Behavioral Sciences, University of Minnesota Twin Cities, Minneapolis, MN, United StatesDepartment of Psychiatry and Behavioral Sciences, University of Minnesota Twin Cities, Minneapolis, MN, United StatesDepartment of Psychiatry and Behavioral Sciences, University of Minnesota Twin Cities, Minneapolis, MN, United StatesGreat Lakes Neurobehavioral Center, Edina, MN, United StatesDepartment of Psychology, University of Rochester, Rochester, NY, United StatesDepartment of Psychiatry and Behavioral Sciences, University of Minnesota Twin Cities, Minneapolis, MN, United StatesDepartment of Psychology, San Diego State University, San Diego, CA, United StatesDepartment of Pediatrics, University of California, San Diego, San Diego, CA, United StatesDepartment of Psychology, San Diego State University, San Diego, CA, United StatesDepartment of Psychiatry and Behavioral Sciences, University of Minnesota Twin Cities, Minneapolis, MN, United StatesDepartment of Psychiatry and Behavioral Sciences, University of Minnesota Twin Cities, Minneapolis, MN, United StatesIntroductionFetal alcohol spectrum disorder (FASD), a life-long condition resulting from prenatal alcohol exposure (PAE), is associated with structural brain anomalies and neurobehavioral differences. Evidence from longitudinal neuroimaging suggest trajectories of white matter microstructure maturation are atypical in PAE. We aimed to further characterize longitudinal trajectories of developmental white matter microstructure change in children and adolescents with PAE compared to typically-developing Controls using diffusion-weighted Neurite Orientation Dispersion and Density Imaging (NODDI).Materials and methodsParticipants: Youth with PAE (n = 34) and typically-developing Controls (n = 31) ages 8–17 years at enrollment. Participants underwent formal evaluation of growth and facial dysmorphology. Participants also completed two study visits (17 months apart on average), both of which involved cognitive testing and an MRI scan (data collected on a Siemens Prisma 3 T scanner). Age-related changes in the orientation dispersion index (ODI) and the neurite density index (NDI) were examined across five corpus callosum (CC) regions defined by tractography.ResultsWhile linear trajectories suggested similar overall microstructural integrity in PAE and Controls, analyses of symmetrized percent change (SPC) indicated group differences in the timing and magnitude of age-related increases in ODI (indexing the bending and fanning of axons) in the central region of the CC, with PAE participants demonstrating atypically steep increases in dispersion with age compared to Controls. Participants with PAE also demonstrated greater increases in ODI in the mid posterior CC (trend-level group difference). In addition, SPC in ODI and NDI was differentially correlated with executive function performance for PAE participants and Controls, suggesting an atypical relationship between white matter microstructure maturation and cognitive function in PAE.DiscussionPreliminary findings suggest subtle atypicality in the timing and magnitude of age-related white matter microstructure maturation in PAE compared to typically-developing Controls. These findings add to the existing literature on neurodevelopmental trajectories in PAE and suggest that advanced biophysical diffusion modeling (NODDI) may be sensitive to biologically-meaningful microstructural changes in the CC that are disrupted by PAE. Findings of atypical brain maturation-behavior relationships in PAE highlight the need for further study. Further longitudinal research aimed at characterizing white matter neurodevelopmental trajectories in PAE will be important.https://www.frontiersin.org/articles/10.3389/fnins.2023.1172010/fullFASDneurodevelopmentlongitudinalcorpus callosumNODDI
spellingShingle Blake A. Gimbel
Donovan J. Roediger
Abigail M. Ernst
Mary E. Anthony
Erik de Water
Madeline N. Rockhold
Bryon A. Mueller
Sarah N. Mattson
Kenneth L. Jones
Edward P. Riley
Kelvin O. Lim
CIFASD
Jeffrey R. Wozniak
Atypical developmental trajectories of white matter microstructure in prenatal alcohol exposure: Preliminary evidence from neurite orientation dispersion and density imaging
Frontiers in Neuroscience
FASD
neurodevelopment
longitudinal
corpus callosum
NODDI
title Atypical developmental trajectories of white matter microstructure in prenatal alcohol exposure: Preliminary evidence from neurite orientation dispersion and density imaging
title_full Atypical developmental trajectories of white matter microstructure in prenatal alcohol exposure: Preliminary evidence from neurite orientation dispersion and density imaging
title_fullStr Atypical developmental trajectories of white matter microstructure in prenatal alcohol exposure: Preliminary evidence from neurite orientation dispersion and density imaging
title_full_unstemmed Atypical developmental trajectories of white matter microstructure in prenatal alcohol exposure: Preliminary evidence from neurite orientation dispersion and density imaging
title_short Atypical developmental trajectories of white matter microstructure in prenatal alcohol exposure: Preliminary evidence from neurite orientation dispersion and density imaging
title_sort atypical developmental trajectories of white matter microstructure in prenatal alcohol exposure preliminary evidence from neurite orientation dispersion and density imaging
topic FASD
neurodevelopment
longitudinal
corpus callosum
NODDI
url https://www.frontiersin.org/articles/10.3389/fnins.2023.1172010/full
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