A Longitudinal Study of White Matter Development in Relation to Changes in Autism Severity Across Early Childhood

Andrews, Derek Sayre; Lee, Joshua K.; Harvey, Danielle; Waizbard-Bartov, Einat; Solomon, Marjorie; Rogers, Sally J.; Nordahl, Christine Wu; Amaral, David G.

doi:10.1016/j.biopsych.2020.10.013

Cited by 47 publications

(60 citation statements)

References 56 publications

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“…This notion is further supported by the improved estimates of AFD-age relationships in the data processed with the TiDi-Fused pipeline compared to the data processed with the conventional pipeline. AFD values from TiDi-Fused data also show more biologically plausible (positive) age trajectories that are corroborated by previous accounts of AFD development of large white matter tracts in non-autistic youth (Dimond et al, 2020 ) and align with previous work done to assess diagnostic differences in white matter development in various white matter tracts throughout the brain (Andrews et al, 2021 ). The TiDi-Fused processing pipeline, therefore, appears to allow for more reliable estimates of white matter microstructure (less variability) and improved biological plausibility, which can, in turn, enhance the validity of in vivo assessments of brainstem-behavior relationships in autistic and non-autistic youth.…”

Section: Discussionsupporting

confidence: 87%

Improving Imaging of the Brainstem and Cerebellum in Autistic Children: Transformation-Based High-Resolution Diffusion MRI (TiDi-Fused) in the Human Brainstem

Guerrero-González

Surgent

Adluru

et al. 2022

Front. Integr. Neurosci.

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Diffusion-weighted magnetic resonance imaging (dMRI) of the brainstem is technically challenging, especially in young autistic children as nearby tissue-air interfaces and motion (voluntary and physiological) can lead to artifacts. This limits the availability of high-resolution images, which are desirable for improving the ability to study brainstem structures. Furthermore, inherently low signal-to-noise ratios, geometric distortions, and sensitivity to motion not related to molecular diffusion have resulted in limited techniques for high-resolution data acquisition compared to other modalities such as T1-weighted imaging. Here, we implement a method for achieving increased apparent spatial resolution in pediatric dMRI that hinges on accurate geometric distortion correction and on high fidelity within subject image registration between dMRI and magnetization prepared rapid acquisition gradient echo (MPnRAGE) images. We call this post-processing pipeline T1 weighted-diffusion fused, or “TiDi-Fused”. Data used in this work consists of dMRI data (2.4 mm resolution, corrected using FSL’s Topup) and T1-weighted (T1w) MPnRAGE anatomical data (1 mm resolution) acquired from 128 autistic and non-autistic children (ages 6–10 years old). Accurate correction of geometric distortion permitted for a further increase in apparent resolution of the dMRI scan via boundary-based registration to the MPnRAGE T1w. Estimation of fiber orientation distributions and further analyses were carried out in the T1w space. Data processed with the TiDi-Fused method were qualitatively and quantitatively compared to data processed with conventional dMRI processing methods. Results show the advantages of the TiDi-Fused pipeline including sharper brainstem gray-white matter tissue contrast, improved inter-subject spatial alignment for group analyses of dMRI based measures, accurate spatial alignment with histology-based imaging of the brainstem, reduced variability in brainstem-cerebellar white matter tracts, and more robust biologically plausible relationships between age and brainstem-cerebellar white matter tracts. Overall, this work identifies a promising pipeline for achieving high-resolution imaging of brainstem structures in pediatric and clinical populations who may not be able to endure long scan times. This pipeline may serve as a gateway for feasibly elucidating brainstem contributions to autism and other conditions.

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Section: Discussionsupporting

confidence: 87%

Improving Imaging of the Brainstem and Cerebellum in Autistic Children: Transformation-Based High-Resolution Diffusion MRI (TiDi-Fused) in the Human Brainstem

Guerrero-González

Surgent

Adluru

et al. 2022

Front. Integr. Neurosci.

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“…This hypothesis would be consistent with previous reports of decreased myelin in superficial WM in adolescent and adults with ASD (Hong et al, 2019). Furthermore, this hypothesis would converge with previous studies who showed an early developmental pattern that could be indicative of increased myelin content in various WM tracts during infancy followed by a delayed myelination process after the age of 12 months in ASD compared to TD (Wolff et al, 2012;Solso et al, 2016;Andrews et al, 2021). Thus, decreased myelin in superficial WM could be part of a more generalized alteration of the myelin as Ameis and Catani (2015) concluded that adults with ASD present a globally decreased connectivity after a review of diffusion imaging literature.…”

Section: Neurobiological Interpretations Of Altered Gwc Valuessupporting

confidence: 92%

Altered Gray-White Matter Boundary Contrast in Toddlers at Risk for Autism Relates to Later Diagnosis of Autism Spectrum Disorder

et al. 2021

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BackgroundRecent neuroimaging studies have highlighted differences in cerebral maturation in individuals with autism spectrum disorder (ASD) in comparison to typical development. For instance, the contrast of the gray-white matter boundary is decreased in adults with ASD. To determine how gray-white matter boundary integrity relates to early ASD phenotypes, we used a regional structural MRI index of gray-white matter contrast (GWC) on a sample of toddlers with a hereditary high risk for ASD.Materials and MethodsWe used a surface-based approach to compute vertex-wise GWC in a longitudinal cohort of toddlers at high-risk for ASD imaged twice between 12 and 24 months (n = 20). A full clinical assessment of ASD-related symptoms was performed in conjunction with imaging and again at 3 years of age for diagnostic outcome. Three outcome groups were defined (ASD, n = 9; typical development, n = 8; non-typical development, n = 3).ResultsASD diagnostic outcome at age 3 was associated with widespread increases in GWC between age 12 and 24 months. Many cortical regions were affected, including regions implicated in social processing and language acquisition. In parallel, we found that early onset of ASD symptoms (i.e., prior to 18-months) was specifically associated with slower GWC rates of change during the second year of life. These alterations were found in areas mainly belonging to the central executive network.LimitationsOur study is the first to measure maturational changes in GWC in toddlers who developed autism, but given the limited size of our sample results should be considered exploratory and warrant further replication in independent and larger samples.ConclusionThese preliminary results suggest that ASD is linked to early alterations of the gray-white matter boundary in widespread brain regions. Early onset of ASD diagnosis constitutes an independent clinical parameter associated with a specific corresponding neurobiological developmental trajectory. Altered neural migration and/or altered myelination processes potentially explain these findings.

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“…This hypothesis would be consistent with previous reports of decreased myelin in super cial WM in adolescent and adults with ASD (71). Furthermore, this hypothesis would converge with previous studies who showed an early developmental pattern that could be indicative of increased myelin content in various WM tracts during infancy followed by a delayed myelination process after the age of 12 months in ASD compared to TD (19,68,72). Thus, decreased myelin in super cial WM could be part of a more generalized alteration of the myelin as Ameis and Catani, 2015 concluded that adults with ASD present a globally decreased connectivity after a review of diffusion imaging literature (73).…”

Section: Neurobiological Interpretations Of Altered Gwc Valuessupporting

confidence: 90%

Altered Gray-White Matter Boundary Contrast in Toddlers at Risk for Autism Relates to Later Diagnosis of Autism Spectrum Disorder.

Godel

Andrews

Amaral

et al. 2021

Preprint

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Background: Recent neuroimaging studies have highlighted differences in cerebral maturation in individuals with autism spectrum disorder (ASD) in comparison to typical development. For instance, the contrast of the gray-white matter boundary is decreased in adults with ASD. To determine how gray-white matter boundary integrity relates to early ASD phenotypes, we used a regional structural MRI index of gray-white matter contrast (GWC) on a sample of toddlers with a hereditary high risk for ASD. Methods: We used a surface-based approach to compute vertex-wise GWC in a longitudinal cohort of toddlers at high-risk for ASD imaged twice between 12 and 24 months (n=20). A full clinical assessment of ASD-related symptoms was performed in conjunction with imaging and again at three years of age for diagnostic outcome. Three outcome groups were defined (ASD, n=9; typical development, n=8; non-typical development, n=3).Results: ASD diagnostic outcome at age 3 was associated with widespread increases in GWC between age 12 and 24 months. Many cortical regions were affected, including regions implicated in social processing and language acquisition. In parallel, we found that early onset of ASD symptoms (i.e. prior to 18-months) was specifically associated with slower GWC rates of change during the second year of life. These alterations were found in areas mainly belonging to the central executive network.Limitations: Our study is the first to measure maturational changes in GWC in toddlers who developed autism, but given the limited size of our sample results should be considered exploratory and warrant further replication in independent and larger samples. Conclusion: These preliminary results suggest that ASD is linked to early alterations of the gray-white matter boundary in widespread brain regions. Early onset of ASD diagnosis constitutes an independent clinical parameter associated with a specific corresponding neurobiological developmental trajectory. Altered neural migration and/or altered myelination processes potentially explain these findings.

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A Longitudinal Study of White Matter Development in Relation to Changes in Autism Severity Across Early Childhood

Cited by 47 publications

References 56 publications

Improving Imaging of the Brainstem and Cerebellum in Autistic Children: Transformation-Based High-Resolution Diffusion MRI (TiDi-Fused) in the Human Brainstem

Improving Imaging of the Brainstem and Cerebellum in Autistic Children: Transformation-Based High-Resolution Diffusion MRI (TiDi-Fused) in the Human Brainstem

Altered Gray-White Matter Boundary Contrast in Toddlers at Risk for Autism Relates to Later Diagnosis of Autism Spectrum Disorder

Altered Gray-White Matter Boundary Contrast in Toddlers at Risk for Autism Relates to Later Diagnosis of Autism Spectrum Disorder.

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