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Left-handedness and its genetic influences are associated with structural asymmetries mapped across the cerebral cortex in 31,864 individuals

Zhiqiang Sha, Antonietta Pepe, Dick Schijven, Amaia Carrion Castillo, James M. Roe, René Westerhausen, Marc Joliot, View ORCID ProfileSimon E. Fisher, View ORCID ProfileFabrice Crivello, View ORCID ProfileClyde Francks
doi: https://doi.org/10.1101/2021.07.16.452594
Zhiqiang Sha
1Language and Genetics Department, Max Planck Institute for Psycholinguistics, Nijmegen, The Netherlands
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Antonietta Pepe
2Institut des Maladies Neurodégénératives, UMR5293, Groupe d’Imagerie Neurofonctionnelle, Commissariat à l’énergie atomique et aux énergies alternatives, CNRS, Université de Bordeaux, Bordeaux cedex 33076, France
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Dick Schijven
1Language and Genetics Department, Max Planck Institute for Psycholinguistics, Nijmegen, The Netherlands
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Amaia Carrion Castillo
1Language and Genetics Department, Max Planck Institute for Psycholinguistics, Nijmegen, The Netherlands
3Basque Center on Cognition, Brain and Language, San Sebastian, Spain
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James M. Roe
4Center for Lifespan Changes in Brain and Cognition, Department of Psychology, University of Oslo, Oslo, Norway
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René Westerhausen
5Section for Cognitive and Clinical Neuroscience, Department of Psychology, University of Oslo, Oslo, Norway
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Marc Joliot
2Institut des Maladies Neurodégénératives, UMR5293, Groupe d’Imagerie Neurofonctionnelle, Commissariat à l’énergie atomique et aux énergies alternatives, CNRS, Université de Bordeaux, Bordeaux cedex 33076, France
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Simon E. Fisher
1Language and Genetics Department, Max Planck Institute for Psycholinguistics, Nijmegen, The Netherlands
6Donders Institute for Brain, Cognition and Behaviour, Radboud University, Nijmegen, The Netherlands
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Fabrice Crivello
2Institut des Maladies Neurodégénératives, UMR5293, Groupe d’Imagerie Neurofonctionnelle, Commissariat à l’énergie atomique et aux énergies alternatives, CNRS, Université de Bordeaux, Bordeaux cedex 33076, France
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Clyde Francks
1Language and Genetics Department, Max Planck Institute for Psycholinguistics, Nijmegen, The Netherlands
6Donders Institute for Brain, Cognition and Behaviour, Radboud University, Nijmegen, The Netherlands
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  • For correspondence: Clyde.Francks@mpi.nl
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Abstract

Roughly 10% of the human population is left-handed, and this rate is increased in some brain-related disorders. The neuroanatomical correlates of hand preference have remained equivocal. We re-sampled structural brain image data from 28,802 right-handers and 3,062 left-handers (UK Biobank population dataset) to a symmetrical surface template, and mapped asymmetries for each of 8,681 vertices across the cerebral cortex in each individual. Left-handers and right-handers showed average differences of surface area asymmetry within fusiform, anterior insular, anterior-middle-cingulate and precentral cortex. Meta-analyzed functional imaging data implicated these regions in executive functions and language. Polygenic disposition to left-handedness was associated with two of these regional asymmetries, and 18 loci previously linked with left-handedness by genome-wide screening showed associations with one or more of these asymmetries. Implicated genes included six encoding microtubule-related proteins: TUBB, TUBA1B, TUBB3, TUBB4A, MAP2 and NME7 – the latter is mutated in left-right reversal of the visceral organs. There were also two cortical regions where average thickness asymmetry was altered in left-handedness: on the postcentral gyrus and inferior occipital cortex, functionally annotated with hand sensorimotor and visual roles. These cortical thickness asymmetries were not heritable. Heritable surface area asymmetries of language-related regions may link the etiologies of hand preference and language, whereas non-heritable asymmetries of sensorimotor cortex may manifest as consequences of hand preference.

Competing Interest Statement

The authors have declared no competing interest.

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Posted July 16, 2021.
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Left-handedness and its genetic influences are associated with structural asymmetries mapped across the cerebral cortex in 31,864 individuals
Zhiqiang Sha, Antonietta Pepe, Dick Schijven, Amaia Carrion Castillo, James M. Roe, René Westerhausen, Marc Joliot, Simon E. Fisher, Fabrice Crivello, Clyde Francks
bioRxiv 2021.07.16.452594; doi: https://doi.org/10.1101/2021.07.16.452594
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Left-handedness and its genetic influences are associated with structural asymmetries mapped across the cerebral cortex in 31,864 individuals
Zhiqiang Sha, Antonietta Pepe, Dick Schijven, Amaia Carrion Castillo, James M. Roe, René Westerhausen, Marc Joliot, Simon E. Fisher, Fabrice Crivello, Clyde Francks
bioRxiv 2021.07.16.452594; doi: https://doi.org/10.1101/2021.07.16.452594

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