The individuality of shape asymmetries of the human cerebral cortex
Abstract
Asymmetries of the cerebral cortex are found across diverse phyla and are particularly pronounced in humans, with important implications for brain function and disease. However, many prior studies have confounded asymmetries due to size with those due to shape. Here, we introduce a novel approach to characterize asymmetries of the whole cortical shape, independent of size, across different spatial frequencies using magnetic resonance imaging data in three independent datasets. We find that cortical shape asymmetry is highly individualized and robust, akin to a cortical fingerprint, and identifies individuals more accurately than size-based descriptors, such as cortical thickness and surface area, or measures of inter-regional functional coupling of brain activity. Individual identifiability is optimal at coarse spatial scales (~37 mm wavelength), and shape asymmetries show scale-specific associations with sex and cognition, but not handedness. While unihemispheric cortical shape shows significant heritability at coarse scales (~65 mm wavelength), shape asymmetries are determined primarily by subject-specific environmental effects. Thus, coarse-scale shape asymmetries are highly personalized, sexually dimorphic, linked to individual differences in cognition, and are primarily driven by stochastic environmental influences.
Data availability
All data generated or analysed during this study are included in the manuscript. All code and dependent toolboxes used in this study can be found at: https://github.com/cyctbdbw/Shape-Asymmetry-Signature. The code of shape-DNA can be found at: http://reuter.mit.edu/software/shapedna/. The OASIS-3 dataset is available under https://www.oasis-brains.org/. The ADNI dataset is available under https://adni.loni.usc.edu. The HCP dataset is available under https://db.humanconnectome.org/.
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OASIS-3: Longitudinal Neuroimaging, Clinical, and Cognitive Dataset for Normal Aging and Alzheimer Disease.https://doi.org/10.1101/2019.12.13.19014902.
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The WU-Minn Human Connectome Project: an overview.https://doi.org/10.1016/j.neuroimage.2013.05.041.
Article and author information
Author details
Funding
Sylvia and Charles Viertel Charitable Foundation (Senior Medical Research Fellowship)
- Alex Fornito
National Health and Medical Research Council (1197431)
- Alex Fornito
National Health and Medical Research Council (1146292)
- Alex Fornito
Australian Research Council (DP200103509)
- Alex Fornito
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Ingrid S Johnsrude, University of Western Ontario, Canada
Ethics
Human subjects: This study only involved subjects from the open-sourced datasets, and all subjects were de-identified by the datasets. Each dataset was approved by its relevant ethics committee and obtained written informed consent from each participant.
Version history
- Preprint posted: September 15, 2021 (view preprint)
- Received: October 28, 2021
- Accepted: October 4, 2022
- Accepted Manuscript published: October 5, 2022 (version 1)
- Accepted Manuscript updated: October 6, 2022 (version 2)
- Version of Record published: November 16, 2022 (version 3)
Copyright
© 2022, Chen 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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