1. Neuroscience

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
https://doi.org/10.7554/eLife.82088
Share this article
Cite this article
  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
  2. Download BibTeX
  3. Download .RIS

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/.
    https://www.nature.com/articles/s41597-022-01695-7

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.

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.

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

  • 1,311
    views
  • 182
    downloads
  • 5
    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

Categories and tags

Research organism

Further reading

    1. Neuroscience

    Parabrachial CGRP neurons modulate active defensive behavior under a naturalistic threat

    Gyeong Hee Pyeon, Hyewon Cho ... Yong Sang Jo
    Research Article Updated

    Recent studies suggest that calcitonin gene-related peptide (CGRP) neurons in the parabrachial nucleus (PBN) represent aversive information and signal a general alarm to the forebrain. If CGRP neurons serve as a true general alarm, their activation would modulate both passive nad active defensive behaviors depending on the magnitude and context of the threat. However, most prior research has focused on the role of CGRP neurons in passive freezing responses, with limited exploration of their involvement in active defensive behaviors. To address this, we examined the role of CGRP neurons in active defensive behavior using a predator-like robot programmed to chase mice. Our electrophysiological results revealed that CGRP neurons encode the intensity of aversive stimuli through variations in firing durations and amplitudes. Optogenetic activation of CGRP neurons during robot chasing elevated flight responses in both conditioning and retention tests, presumably by amplifying the perception of the threat as more imminent and dangerous. In contrast, animals with inactivated CGRP neurons exhibited reduced flight responses, even when the robot was programmed to appear highly threatening during conditioning. These findings expand the understanding of CGRP neurons in the PBN as a critical alarm system, capable of dynamically regulating active defensive behaviors by amplifying threat perception, and ensuring adaptive responses to varying levels of danger.

    1. Evolutionary Biology
    2. Neuroscience

    Vision: The inner workings of a miniature eye

    Gregor Belušič
    Insight

    The first complete 3D reconstruction of the compound eye of a minute wasp species sheds light on the nuts and bolts of size reduction.

    1. Neuroscience

    Cortical tracking of hierarchical rhythms orchestrates the multisensory processing of biological motion

    Li Shen, Shuo Li ... Yi Jiang
    Research Article

    When observing others’ behaviors, we continuously integrate their movements with the corresponding sounds to enhance perception and develop adaptive responses. However, how the human brain integrates these complex audiovisual cues based on their natural temporal correspondence remains unclear. Using electroencephalogram (EEG), we demonstrated that rhythmic cortical activity tracked the hierarchical rhythmic structures in audiovisually congruent human walking movements and footstep sounds. Remarkably, the cortical tracking effects exhibit distinct multisensory integration modes at two temporal scales: an additive mode in a lower-order, narrower temporal integration window (step cycle) and a super-additive enhancement in a higher-order, broader temporal window (gait cycle). Furthermore, while neural responses at the lower-order timescale reflect a domain-general audiovisual integration process, cortical tracking at the higher-order timescale is exclusively engaged in the integration of biological motion cues. In addition, only this higher-order, domain-specific cortical tracking effect correlates with individuals’ autistic traits, highlighting its potential as a neural marker for autism spectrum disorder. These findings unveil the multifaceted mechanism whereby rhythmic cortical activity supports the multisensory integration of human motion, shedding light on how neural coding of hierarchical temporal structures orchestrates the processing of complex, natural stimuli across multiple timescales.