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

Author:

Roe James M1ORCID,Vidal-Pineiro Didac1ORCID,Amlien Inge K1,Pan Mengyu1,Sneve Markus H1,Thiebaut de Schotten Michel23ORCID,Friedrich Patrick4,Sha Zhiqiang5,Francks Clyde567ORCID,Eilertsen Espen M8,Wang Yunpeng1,Walhovd Kristine B19ORCID,Fjell Anders M19,Westerhausen René10ORCID

Affiliation:

1. Center for Lifespan Changes in Brain and Cognition (LCBC), Department of Psychology, University of Oslo

2. Groupe d'Imagerie Neurofonctionnelle, Institut des Maladies Neurodégénératives-UMR 5293, CNRS, CEA, University of Bordeaux

3. Brian Connectivity and Behaviour Laboratory, Sorbonne University

4. Institute of Neuroscience and Medicine, Research Centre Jülich

5. Language and Genetics Department, Max Planck Institute for Psycholinguistics

6. Donders Institute for Brain, Cognition and Behaviour, Radboud University

7. Department of Human Genetics, Radboud University Medical Center

8. PROMENTA Research Center, Department of Psychology, University of Oslo

9. Department of Radiology and Nuclear Medicine, Oslo University Hospital

10. Section for Cognitive and Clinical Neuroscience, Department of Psychology, University of Oslo

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 the 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 seven 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.

Funder

European Research Council

Norwegian Research Council

Publisher

eLife Sciences Publications, Ltd

Subject

General Immunology and Microbiology,General Biochemistry, Genetics and Molecular Biology,General Medicine,General Neuroscience

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