Heritability and cross-species comparisons of human cortical functional organization asymmetry
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.
Article and author information
Author details
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
- 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
- Preprint posted: November 4, 2021 (view preprint)
- Received: January 20, 2022
- Accepted: July 28, 2022
- Accepted Manuscript published: July 29, 2022 (version 1)
- Accepted Manuscript updated: August 11, 2022 (version 2)
- 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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