Tracing the development and lifespan change of population-level structural asymmetry in the cerebral cortex

  1. James M Roe  Is a corresponding author
  2. Didac Vidal-Pineiro
  3. Inge K Amlien
  4. Mengyu Pan
  5. Markus H Sneve
  6. Michel Thiebaut de Schotten
  7. Patrick Friedrich
  8. Zhiqiang Sha
  9. Clyde Francks
  10. Espen M Eilertsen
  11. Yunpeng Wang
  12. Kristine B Walhovd
  13. Anders M Fjell
  14. René Westerhausen
  1. University of Oslo, Norway
  2. University of Bordeaux, France
  3. Research Centre Jülich, Germany
  4. Max Planck Institute for Psycholinguistics, Netherlands

Abstract

Cortical asymmetry is a ubiquitous feature of brain organization that is subtly altered in some neurodevelopmental disorders, yet we lack knowledge of how its development proceeds across life in health. Achieving consensus on the precise cortical asymmetries in humans is necessary to uncover the developmental timing of asymmetry and extent to which it arises through genetic and later influences in childhood. Here, we delineate population-level asymmetry in cortical thickness and surface area vertex-wise in 7 datasets and chart asymmetry trajectories longitudinally across life (4-89 years; observations = 3937; 70% longitudinal). We find replicable asymmetry interrelationships, heritability maps, and test asymmetry associations in large-scale data. Cortical asymmetry was robust across datasets. Whereas areal asymmetry is predominantly stable across life, thickness asymmetry grows in childhood and peaks in early adulthood. Areal asymmetry is low-moderately heritable (max h2SNP ~19%) and correlates phenotypically and genetically in specific regions, indicating coordinated development of asymmetries partly through genes. In contrast, thickness asymmetry is globally interrelated across the cortex in a pattern suggesting highly left-lateralized individuals tend towards left-lateralization also in population-level right-asymmetric regions (and vice versa), and exhibits low or absent heritability. We find less areal asymmetry in the most consistently lateralized region in humans associates with subtly lower cognitive ability, and confirm small handedness and sex effects. Results suggest areal asymmetry is developmentally stable and arises early in life through genetic but mainly subject-specific stochastic effects, whereas childhood developmental growth shapes thickness asymmetry and may lead to directional variability of global thickness lateralization in the population.

Data availability

All summary-level maps are available in Supplementary file 2. All code underlying the main analyses is available at https://github.com/jamesmroe/PopAsym and on the Open Science Framework (OSF; https://osf.io/dv9um/). Derived source data underlying figures is also available on the OSF. All datasets used in this work are openly available, with the exception of LCBC where participants, which include many children, have not consented to share their data publicly online. Other datasets used in this work are available without restrictions and are not subject to application approval (DLBS; https://fcon_1000.projects.nitrc.org/indi/retro/dlbs.html; CC BY-NC; SALD; http://fcon_1000.projects.nitrc.org/indi/retro/sald.html; CC BY-NC; IXI; https://brain-development.org/ixi-dataset; CC BY-SA 3.0). Accordingly, we have made the individual-level data for these samples available and our code can be used to reproduce vertex-wise analyses in these samples. Individual-level data for the remaining samples (LCBC; Cam-CAN, HCP; UKB) may be available upon reasonable request, given appropriate ethical, data protection, and data-sharing agreements where applicable. Requests must be submitted and approved via the relevant channel (details are provided in Supplementary File 1).

The following previously published data sets were used
    1. Tyler LK
    (2017) Cam-CAN
    https://doi.org/10.1016/j.neuroimage.2015.09.018.
    1. Park DC
    (2012) DLBS
    https://fcon_1000.projects.nitrc.org/indi/retro/dlbs.html.
    1. Wei D
    2. Zhuang K
    3. Chen Q
    4. Yang W
    5. Liu W
    6. Wang K
    7. ... & Qiu J
    (2018) SALD
    http://fcon_1000.projects.nitrc.org/indi/retro/sald.html.

Article and author information

Author details

  1. James M Roe

    Department of Psychology, University of Oslo, Oslo, Norway
    For correspondence
    j.m.roe@psykologi.uio.no
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8008-902X
  2. Didac Vidal-Pineiro

    Department of Psychology, University of Oslo, Oslo, Norway
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9997-9156
  3. Inge K Amlien

    Department of Psychology, University of Oslo, Oslo, Norway
    Competing interests
    The authors declare that no competing interests exist.
  4. Mengyu Pan

    Department of Psychology, University of Oslo, Oslo, Norway
    Competing interests
    The authors declare that no competing interests exist.
  5. Markus H Sneve

    Department of Psychology, University of Oslo, Oslo, Norway
    Competing interests
    The authors declare that no competing interests exist.
  6. Michel Thiebaut de Schotten

    Brian Connectivity and Behaviour Laboratory, University of Bordeaux, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0329-1814
  7. Patrick Friedrich

    Institute of Neuroscience and Medicine, Research Centre Jülich, Jülich, Germany
    Competing interests
    The authors declare that no competing interests exist.
  8. Zhiqiang Sha

    Language and Genetics Department, Max Planck Institute for Psycholinguistics, Nijmegen, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  9. Clyde Francks

    Language and Genetics Department, Max Planck Institute for Psycholinguistics, Nijmegen, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9098-890X
  10. Espen M Eilertsen

    Department of Psychology, University of Oslo, Oslo, Norway
    Competing interests
    The authors declare that no competing interests exist.
  11. Yunpeng Wang

    Department of Psychology, University of Oslo, Oslo, Norway
    Competing interests
    The authors declare that no competing interests exist.
  12. Kristine B Walhovd

    Department of Psychology, University of Oslo, Oslo, Norway
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1918-1123
  13. Anders M Fjell

    Department of Psychology, University of Oslo, Oslo, Norway
    Competing interests
    The authors declare that no competing interests exist.
  14. René Westerhausen

    Department of Psychology, University of Oslo, Oslo, Norway
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7107-2712

Funding

European Research Council (283634)

  • Anders M Fjell

European Research Council (725025)

  • Anders M Fjell

European Research Council (313440)

  • Kristine B Walhovd

Norwegian Research Council (249931)

  • Anders M Fjell

Norwegian Research Council (249931)

  • Kristine B Walhovd

Norwegian Research Council (302854)

  • Yunpeng Wang

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Jonas Obleser, University of Lübeck, Germany

Ethics

Human subjects: All studies were conducted in accordance with the Declaration of Helsinki. Ethical approval was obtained from the relevant authorities, and all participants provided informed consent. Studies conducted at the Center for Lifespan Changes in Brain and Cognition (LCBC) were approved by the Regional Ethical Committee of South-East Norway (2017/653) and complied with all relevant ethical regulations. Ethical approval for the other datasets was granted by the relevant authorities (Supplementary File 1M).

Version history

  1. Preprint posted: November 25, 2021 (view preprint)
  2. Received: November 3, 2022
  3. Accepted: June 16, 2023
  4. Accepted Manuscript published: June 19, 2023 (version 1)
  5. Version of Record published: July 25, 2023 (version 2)

Copyright

© 2023, Roe et al.

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.

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  1. James M Roe
  2. Didac Vidal-Pineiro
  3. Inge K Amlien
  4. Mengyu Pan
  5. Markus H Sneve
  6. Michel Thiebaut de Schotten
  7. Patrick Friedrich
  8. Zhiqiang Sha
  9. Clyde Francks
  10. Espen M Eilertsen
  11. Yunpeng Wang
  12. Kristine B Walhovd
  13. Anders M Fjell
  14. René Westerhausen
(2023)
Tracing the development and lifespan change of population-level structural asymmetry in the cerebral cortex
eLife 12:e84685.
https://doi.org/10.7554/eLife.84685

Share this article

https://doi.org/10.7554/eLife.84685

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