Heritability and cross-species comparisons of human cortical functional organization asymmetry

  1. Bin Wan  Is a corresponding author
  2. Şeyma Bayrak
  3. Ting Ting Xu
  4. H Lina Schaare
  5. Richard AI Bethlehem
  6. Boris C Bernhardt
  7. Sofie Louise Valk  Is a corresponding author
  1. Max Planck Institute for Human Cognitive and Brain Sciences, Germany
  2. Child Mind Institute, United States
  3. University of Cambridge, United Kingdom
  4. McGill University, Canada

Abstract

The human cerebral cortex is symmetrically organized along large-scale axes but also presents inter-hemispheric differences in structure and function. The quantified contralateral homologous difference, i.e., asymmetry, is a key feature of the human brain left-right axis supporting functional processes, such as language. Here, we assessed whether the asymmetry of cortical functional organization is heritable and phylogenetically conserved between humans and macaques. Our findings indicate asymmetric organization along an axis describing a functional trajectory from perceptual/action to abstract cognition. Whereas language network showed leftward asymmetric organization, frontoparietal network showed rightward asymmetric organization in humans. These asymmetries were heritable in humans and showed a similar spatial distribution with macaques, in the case of intra-hemispheric asymmetry of functional hierarchy. This suggests (phylo)genetic conservation. However, both language and frontoparietal networks showed a qualitatively larger asymmetry in humans relative to macaques. Overall, our findings suggest a genetic basis for asymmetry in intrinsic functional organization, linked to higher-order cognitive functions uniquely developed in humans.

Data availability

All human data analyzed in this manuscript were obtained from the open-access HCP youngadult sample (HCP; www.humanconnectome.org/), UK Biobank (UKB,https://www.ukbiobank.ac.uk/). Macaque data came from PRIME-DE(http://fcon_1000.projects.nitrc.org/indi/indiPRIME.html). Full statistical scripts can be found at https://bit.ly/3sAJ1bP.

The following previously published data sets were used

Article and author information

Author details

  1. Bin Wan

    Otto Hahn Group Cognitive Neurogenetics, Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig, Germany
    For correspondence
    wanb.psych@outlook.com
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9077-3354
  2. Şeyma Bayrak

    Otto Hahn Group Cognitive Neurogenetics, Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig, Germany
    Competing interests
    The authors declare that no competing interests exist.
  3. Ting Ting Xu

    Center for the Developing Brain, Child Mind Institute, New York, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. H Lina Schaare

    Otto Hahn Group Cognitive Neurogenetics, Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig, Germany
    Competing interests
    The authors declare that no competing interests exist.
  5. Richard AI Bethlehem

    Department of Psychiatry, University of Cambridge, Cambridge, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0714-0685
  6. Boris C Bernhardt

    McConnell Brain Imaging Centre, McGill University, Montreal, Canada
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9256-6041
  7. Sofie Louise Valk

    Otto Hahn Group Cognitive Neurogenetics, Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig, Germany
    For correspondence
    valk@cbs.mpg.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2998-6849

Funding

Max Planck Gesellschaft

  • Sofie Louise Valk

Sick Kids Foundation (NI17-039)

  • Boris C Bernhardt

National Sciences and Engineering Research Council of Canada (Discovery-1304413)

  • Boris C Bernhardt

Canadian Institute of Health Research (FDN154298)

  • Boris C Bernhardt

Azrieli Center for Autism Research

  • Boris C Bernhardt

Canada First Research Excellence Fund

  • Boris C Bernhardt
  • Sofie Louise Valk

International Max Planck Research School on Neuroscience of Communication: Function, Structure, and Plasticity

  • Bin Wan

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

Reviewing Editor

  1. Saad Jbabdi, University of Oxford, United Kingdom

Ethics

Human subjects: The current research complies with all relevant ethical regulations as set by The Independent Research Ethics Committee at the Medical Faculty of the Heinrich-Heine-University of Duesseldorf (study number 2018-317).

Version history

  1. Preprint posted: November 4, 2021 (view preprint)
  2. Received: January 20, 2022
  3. Accepted: July 28, 2022
  4. Accepted Manuscript published: July 29, 2022 (version 1)
  5. Accepted Manuscript updated: August 11, 2022 (version 2)
  6. Version of Record published: August 16, 2022 (version 3)

Copyright

© 2022, Wan 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. Bin Wan
  2. Şeyma Bayrak
  3. Ting Ting Xu
  4. H Lina Schaare
  5. Richard AI Bethlehem
  6. Boris C Bernhardt
  7. Sofie Louise Valk
(2022)
Heritability and cross-species comparisons of human cortical functional organization asymmetry
eLife 11:e77215.
https://doi.org/10.7554/eLife.77215

Share this article

https://doi.org/10.7554/eLife.77215

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