Applying microstructural models to understand the role of white matter in cognitive development

Huber, Elizabeth; Henriques, Rafael Neto; Owen, Julia P.; Rokem, Ariel; Yeatman, Jason D.

doi:10.1016/j.dcn.2019.100624

Cited by 40 publications

(51 citation statements)

References 67 publications

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“…These structural abnormalities have been associated with decreased IQ and visuomotor function in children born VPT (Kelly et al, 2016; Young et al, 2019), and greater symptoms of social impairment in individuals with ASD (Dimond 2019). These findings, alongside NDI-cognitive associations in healthy individuals (Chung et al, 2018; Collins et al, 2019; Huber et al, 2019; Merluzzi et al, 2016), suggest that neurite density plays an important role in cognitive function, likely mediated by influences on network connectivity. Age-related increases in NDI have been shown to be associated with increased structural network properties (Batalle et al, 2017) and greater functional network connectivity (Deligianni et al, 2016), which is believed to enable faster communication across brain regions in support of various cognitive processes (Zimmermann et al, 2018).…”

Section: Discussionmentioning

confidence: 80%

“…Utilizing NODDI (Zhang et al, 2012), several studies have demonstrated substantial white matter microstructural changes across the lifespan, characterized by approximately logarithmic increases in NDI from birth to adulthood (Batalle et al, 2017; Chang et al, 2015; Dean et al, 2017; Genc et al, 2017a; Huber et al, 2019; Jelescu et al, 2015; Mah et al, 2017; Young et al, 2019), and delayed exponential increases in ODI (Chang et al, 2015), with marginal increases in ODI during early infancy (0-1 years) (Batalle et al, 2017; Dean et al, 2017), no change during childhood and adolescence (Mah et al, 2017; Young et al, 2019), and more rapid increases in mid-late adulthood (Billiet et al, 2015; Chang et al, 2015; Kodiweera et al, 2016; Ota et al, 2017).…”

Section: Discussionmentioning

confidence: 99%

“…Since its introduction, NODDI (Zhang et al, 2012) has become a popular tool for assessing white matter microstructure, though other biophysical diffusion models have been developed in recent years to estimate neurite or axonal density in-vivo. White matter tract integrity (WMTI; Fieremans et al, 2011) is a two-component model that has been utilized to show developmental increases in axonal water fraction (AWF; the fraction of diffusion signal that is attributed to intra-cellular, as opposed to extra-cellular diffusion, which approximates axonal volume or density) during infancy (Jelescu et al, 2015) and late childhood-adolescence (Huber et al, 2019). Similar to our findings with NDI, Huber et al (2019) found that AWF increases with age in almost all white matter tracts, with a stronger effect in the arcuate fasciculi where we found NDI changes to be most rapid.…”

Section: Discussionmentioning

confidence: 99%

“…During early childhood, cognitive maturation is rapid, with developmental improvements in working memory (Burnett Heyes et al, 2012), math (Garon-Carrier et al, 2018), self-regulation (Montroy et al, 2016), reading (Ferretti et al, 2008), and attention (Breckenridge et al, 2013; Mullane et al, 2016), among other traits. Individual differences in axonal/neurite density have been linked to each of these cognitive traits (Chung et al, 2018; Collins et al, 2019; Genc et al, 2019; Huber et al, 2019; Kelly et al, 2016; Merluzzi et al, 2016), suggesting developmental increases in neurite density may contribute to cognitive-behavioral maturation in early childhood. Considering growth patterns in infancy and late childhood (Batalle et al, 2017; Dean et al, 2017; Jelescu et al, 2015), we interpret our NDI results to suggest maturation during early childhood in association fibers is becoming more rapid, commissural and projection fibers are approaching maturity, and maturation in limbic and frontal tracts remains modest.…”

Section: Discussionmentioning

confidence: 99%

“…More recently, advanced biophysical diffusion models capable of estimating specific white matter properties (see Jelescu and Budde, 2017 for review) have been applied to study white matter development (Dean et al, 2017; Dimond et al, 2019a; Huber et al, 2019). One such model, called neurite orientation dispersion and density imaging (NODDI; Zhang et al, 2012), provides metrics sensitive to neurite/axonal density (neurite density index (NDI)) and the extent of orientational incoherence/dispersion amongst axonal projections within a voxel (orientation dispersion index (ODI)).…”

Section: Introductionmentioning

confidence: 99%

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Maturation and interhemispheric asymmetry in neurite density and orientation dispersion in early childhood

Dimond

Heo

et al. 2019

Preprint

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BackgroundThe brain’s white matter undergoes profound changes during early childhood, which are believed to underlie the rapid development of cognitive and behavioral skills during this period. Neurite density, and complexity of axonal projections, have been shown to change across the life span, though changes during early childhood are poorly characterized. Here, we utilize neurite orientation dispersion and density imaging (NODDI) to investigate maturational changes in tract-wise neurite density index (NDI) and orientation dispersion index (ODI) during early childhood. Additionally, we assess hemispheric asymmetry of tract-wise NDI and ODI values, and longitudinal changes.MethodsTwo sets of diffusion weighted images (DWI) with different diffusion-weighting were collected from 125 typically developing children scanned at baseline (N=125; age range=4.14-7.29; F/M=73/52), 6-month (N=8; F/M=8/0), and 12-month (N=52; F/M=39/13) timepoints. NODDI and template-based tractography using constrained spherical deconvolution were utilized to calculate NDI and ODI values for major white matter tracts. Mixed-effects models controlling for sex, handedness, and in-scanner head motion were utilized to assess developmental changes in tract-wise NDI and ODI. Paired t-tests were used to assess interhemispheric differences in tract-wise NDI and ODI values and longitudinal changes in cross-sectional and 12-month longitudinal analyses, respectively.ResultsMaturational increases in NDI were seen in all major white matter tracts, though we did not observe the expected tract-wise pattern of maturational rates (e.g. fast commissural/projection and slow frontal/temporal tract change). ODI did not change significantly with age in any tract. We observed higher cross-sectional NDI and ODI values in the right as compared to the left hemisphere for most tracts, but no hemispheric asymmetry for longitudinal changes.ConclusionsThese findings suggest that neurite density, but not orientation dispersion, increases with age during early childhood. In relation to NDI growth trends reported in infancy and late-childhood, our results suggest that early childhood may be a transitional period for neurite density maturation wherein commissural/projection fibers are approaching maturity, maturation in long range association fibers is increasing, and changes in limbic/frontal fibers remain modest. Rightward asymmetry in NDI and ODI values, but not longitudinal changes, suggests that rightward asymmetry of neurite density and orientation dispersion is established prior to age 4.

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Section: Discussionmentioning

confidence: 80%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Maturation and interhemispheric asymmetry in neurite density and orientation dispersion in early childhood

Dimond

Heo

et al. 2019

Preprint

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Maturation of cortical microstructure and cognitive development in childhood and adolescence: A T1w/T2w ratio MRI study

Norbom

Rokicki

Alnæs

et al. 2020

Human Brain Mapping

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The restructuring and optimization of the cerebral cortex from early childhood and through adolescence is an essential feature of human brain development, underlying immense cognitive improvements. Beyond established morphometric cortical assessments, the T1w/T2w ratio quantifies partly separate biological processes, and might inform models of typical neurocognitive development and developmental psychopathology. In the present study, we computed vertex-wise T1w/T2w ratio across the cortical surface in 621 youths (3-21 years) sampled from the Pediatric Imaging, Neurocognition, and Genetics (PING) study and tested for associations with individual differences in age, sex, and both general and specific cognitive abilities. The results showed a near global linear age-related increase in T1w/T2w ratio across the brain surface, with a general posterior to anterior increasing gradient in association strength. Moreover, results indicated that boys in late adolescence had regionally higher T1w/T2w ratio as compared to girls. Across individuals, T1w/T2w ratio was negatively associated with general and several specific cognitive abilities mainly within anterior cortical regions. Our study indicates age-related differences in T1w/T2w ratio throughout childhood, adolescence, and young adulthood, in line with the known protracted myelination of the cortex. Moreover, the study supports T1w/T2w ratio as a promising surrogate measure of individual differences in intracortical brain structure in neurodevelopment.

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Development of the visual white matter pathways mediates development of electrophysiological responses in visual cortex

Caffarra

Joo

Bloom

et al. 2021

Human Brain Mapping

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The latency of neural responses in the visual cortex changes systematically across the lifespan. Here, we test the hypothesis that development of visual white matter pathways mediates maturational changes in the latency of visual signals. Thirty-eight children participated in a cross-sectional study including diffusion magnetic resonance imaging (MRI) and magnetoencephalography (MEG) sessions. During the MEG acquisition, participants performed a lexical decision and a fixation task on words presented at varying levels of contrast and noise. For all stimuli and tasks, early evoked fields were observed around 100 ms after stimulus onset (M100), with slower and lower amplitude responses for low as compared to high contrast stimuli. The optic radiations and optic tracts were identified in each individual's brain based on diffusion MRI tractography. The diffusion properties of the optic radiations predicted M100 responses, especially for high contrast stimuli. Higher optic radiation fractional anisotropy (FA) values were associated with faster and larger M100 responses. Over this developmental window, the M100 responses to high contrast stimuli became faster with age and the optic radiation FA mediated this effect. These findings suggest that the maturation of the optic radiations over childhood accounts for individual variations observed in the developmental trajectory of visual cortex responses.

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Applying microstructural models to understand the role of white matter in cognitive development

Cited by 40 publications

References 67 publications

Maturation and interhemispheric asymmetry in neurite density and orientation dispersion in early childhood

Maturation and interhemispheric asymmetry in neurite density and orientation dispersion in early childhood

Maturation of cortical microstructure and cognitive development in childhood and adolescence: A T1w/T2w ratio MRI study

Development of the visual white matter pathways mediates development of electrophysiological responses in visual cortex

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