Fiber-specific structural properties relate to reading skills in children and adolescents
Abstract
Recent studies suggest that the cross-sectional relationship between reading skills and white matter microstructure, as indexed by fractional anisotropy, is not as robust as previously thought. Fixel-based analyses yield fiber-specific micro- and macrostructural measures, overcoming several shortcomings of the traditional diffusion tensor model. We ran a whole-brain analysis investigating whether the product of fiber density and cross-section (FDC) related to single-word reading skills in a large, open, quality-controlled data set of 983 children and adolescents ages 6-18. We also compared FDC between participants with (n = 102) and without (n = 570) reading disabilities. We found that FDC positively related to reading skills throughout the brain, especially in left temporoparietal and cerebellar white matter, but did not differ between reading proficiency groups. Exploratory analyses revealed that among metrics from other diffusion models - DTI, DKI, and NODDI - only the orientation dispersion and neurite density indexes from NODDI were associated (inversely) with reading skills. The present findings further support the importance of left-hemisphere dorsal temporoparietal white matter tracts in reading. Additionally, these results suggest future DWI studies of reading and dyslexia should be designed to benefit from advanced diffusion models, include cerebellar coverage, and consider continuous analyses that account for individual differences in reading skill.
Data availability
Raw and preprocessed neuroimaging data from the Healthy Brain Network are publicly available without restriction, and can be downloaded from Amazon Simple Storage Service (S3) following directions from the HBN-POD2 manuscript (Richie-Halford et al., 2022).Access to full phenotypic and behavioral data, which are stored at https://data.healthybrainnetwork.org/main.php, is restricted. For this reason, we cannot make our full study outputs publicly available. These data can be collected by any entity following directions on the Healthy Brain Network data portal (http://fcon_1000.projects.nitrc.org/indi/cmi_healthy_brain_network/index.html) after signing a data use agreement.Study-specific code and instructions for processing data and running the statistical models can be found at https://github.com/smeisler/Meisler_Reading_FBA. We share the population FOD template, tract segmentations, and model outputs (which only report data in the aggregate) at https://osf.io/3ady4/. These can all be viewed using MRview from MRtrix3.
-
HBN-POD2s3://fcp-indi/data/Projects/HBN/BIDS_curated/derivatives/qsiprep/.
-
Healthy Brain Networks3://fcp-indi/data/Projects/HBN/BIDS_curated/.
Article and author information
Author details
Funding
National Institute on Deafness and Other Communication Disorders (T32 Training Grant,5T32DC000038)
- Steven Lee Meisler
Chan Zuckerberg Initiative
- John Gabrieli
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Birte U Forstmann, University of Amsterdam, Netherlands
Ethics
Human subjects: The Healthy Brain Network project was approved by the Chesapeake Institutional Review Board (now called Advarra, Inc.; https://www.advarra.com/; protocol number: Pro00012309). Informed consent was obtained from all participants ages 18 or older. For younger participants, written informed consent was collected from their legal guardians, and written assent was obtained from the participants.
Version history
- Preprint posted: July 22, 2022 (view preprint)
- Received: July 22, 2022
- Accepted: December 21, 2022
- Accepted Manuscript published: December 28, 2022 (version 1)
- Version of Record published: January 5, 2023 (version 2)
Copyright
© 2022, Meisler & Gabrieli
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
Metrics
-
- 982
- views
-
- 157
- downloads
-
- 2
- citations
Views, downloads and citations are aggregated across all versions of this paper published by eLife.
Download links
Downloads (link to download the article as PDF)
Open citations (links to open the citations from this article in various online reference manager services)
Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)
Further reading
-
- Neuroscience
Cortical folding is an important feature of primate brains that plays a crucial role in various cognitive and behavioral processes. Extensive research has revealed both similarities and differences in folding morphology and brain function among primates including macaque and human. The folding morphology is the basis of brain function, making cross-species studies on folding morphology important for understanding brain function and species evolution. However, prior studies on cross-species folding morphology mainly focused on partial regions of the cortex instead of the entire brain. Previously, our research defined a whole-brain landmark based on folding morphology: the gyral peak. It was found to exist stably across individuals and ages in both human and macaque brains. Shared and unique gyral peaks in human and macaque are identified in this study, and their similarities and differences in spatial distribution, anatomical morphology, and functional connectivity were also dicussed.
-
- Neuroscience
Complex skills like speech and dance are composed of ordered sequences of simpler elements, but the neuronal basis for the syntactic ordering of actions is poorly understood. Birdsong is a learned vocal behavior composed of syntactically ordered syllables, controlled in part by the songbird premotor nucleus HVC (proper name). Here, we test whether one of HVC’s recurrent inputs, mMAN (medial magnocellular nucleus of the anterior nidopallium), contributes to sequencing in adult male Bengalese finches (Lonchura striata domestica). Bengalese finch song includes several patterns: (1) chunks, comprising stereotyped syllable sequences; (2) branch points, where a given syllable can be followed probabilistically by multiple syllables; and (3) repeat phrases, where individual syllables are repeated variable numbers of times. We found that following bilateral lesions of mMAN, acoustic structure of syllables remained largely intact, but sequencing became more variable, as evidenced by ‘breaks’ in previously stereotyped chunks, increased uncertainty at branch points, and increased variability in repeat numbers. Our results show that mMAN contributes to the variable sequencing of vocal elements in Bengalese finch song and demonstrate the influence of recurrent projections to HVC. Furthermore, they highlight the utility of species with complex syntax in investigating neuronal control of ordered sequences.