Fiber-specific structural properties relate to reading skills in children and adolescents

  1. Steven Lee Meisler  Is a corresponding author
  2. John Gabrieli
  1. Harvard University, United States
  2. Massachusetts Institute of Technology, United States

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.

The following previously published data sets were used
    1. Richie-Halford A
    2. et al
    (2022) HBN-POD2
    s3://fcp-indi/data/Projects/HBN/BIDS_curated/derivatives/qsiprep/.

Article and author information

Author details

  1. Steven Lee Meisler

    Program in Speech and Hearing Bioscience and Technology, Harvard University, Cambridge, United States
    For correspondence
    smeisler@g.harvard.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8888-1572
  2. John Gabrieli

    Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.

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

  1. 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

  1. Preprint posted: July 22, 2022 (view preprint)
  2. Received: July 22, 2022
  3. Accepted: December 21, 2022
  4. Accepted Manuscript published: December 28, 2022 (version 1)
  5. 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

A two-part list of links to download the article, or parts of the article, in various formats.

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)

  1. Steven Lee Meisler
  2. John Gabrieli
(2022)
Fiber-specific structural properties relate to reading skills in children and adolescents
eLife 11:e82088.
https://doi.org/10.7554/eLife.82088

Share this article

https://doi.org/10.7554/eLife.82088

Further reading

    1. Neuroscience
    Songyao Zhang, Tuo Zhang ... Tianming Liu
    Research Article

    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.

    1. Neuroscience
    Avani Koparkar, Timothy L Warren ... Lena Veit
    Research Article

    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.