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Language network lateralization is reflected throughout the macroscale functional organization of cortex

Author

Listed:
  • Loïc Labache

    (Yale University)

  • Tian Ge

    (Massachusetts General Hospital
    Massachusetts General Hospital
    Broad Institute)

  • B. T. Thomas Yeo

    (National University of Singapore
    National University of Singapore
    National University of Singapore
    Massachusetts General Hospital)

  • Avram J. Holmes

    (Yale University
    Yale University
    Yale University
    Rutgers University)

Abstract

Hemispheric specialization is a fundamental feature of human brain organization. However, it is not yet clear to what extent the lateralization of specific cognitive processes may be evident throughout the broad functional architecture of cortex. While the majority of people exhibit left-hemispheric language dominance, a substantial minority of the population shows reverse lateralization. Using twin and family data from the Human Connectome Project, we provide evidence that atypical language dominance is associated with global shifts in cortical organization. Individuals with atypical language organization exhibit corresponding hemispheric differences in the macroscale functional gradients that situate discrete large-scale networks along a continuous spectrum, extending from unimodal through association territories. Analyses reveal that both language lateralization and gradient asymmetries are, in part, driven by genetic factors. These findings pave the way for a deeper understanding of the origins and relationships linking population-level variability in hemispheric specialization and global properties of cortical organization.

Suggested Citation

  • Loïc Labache & Tian Ge & B. T. Thomas Yeo & Avram J. Holmes, 2023. "Language network lateralization is reflected throughout the macroscale functional organization of cortex," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-39131-y
    DOI: 10.1038/s41467-023-39131-y
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    1. Zijin Gu & Keith Wakefield Jamison & Mert Rory Sabuncu & Amy Kuceyeski, 2021. "Heritability and interindividual variability of regional structure-function coupling," Nature Communications, Nature, vol. 12(1), pages 1-12, December.
    2. Whitcher, Brandon & Schmid, Volker J. & Thorton, Andrew, 2011. "Working with the DICOM and NIfTI Data Standards in R," Journal of Statistical Software, Foundation for Open Access Statistics, vol. 44(i06).
    3. Bernard Mazoyer & Laure Zago & Gaël Jobard & Fabrice Crivello & Marc Joliot & Guy Perchey & Emmanuel Mellet & Laurent Petit & Nathalie Tzourio-Mazoyer, 2014. "Gaussian Mixture Modeling of Hemispheric Lateralization for Language in a Large Sample of Healthy Individuals Balanced for Handedness," PLOS ONE, Public Library of Science, vol. 9(6), pages 1-14, June.
    4. Vyacheslav R. Karolis & Maurizio Corbetta & Michel Thiebaut de Schotten, 2019. "The architecture of functional lateralisation and its relationship to callosal connectivity in the human brain," Nature Communications, Nature, vol. 10(1), pages 1-9, December.
    5. Sofie L. Valk & Ting Xu & Casey Paquola & Bo-yong Park & Richard A. I. Bethlehem & Reinder Vos de Wael & Jessica Royer & Shahrzad Kharabian Masouleh & Şeyma Bayrak & Peter Kochunov & B. T. Thomas Yeo , 2022. "Genetic and phylogenetic uncoupling of structure and function in human transmodal cortex," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    6. Matthew F. Glasser & Timothy S. Coalson & Emma C. Robinson & Carl D. Hacker & John Harwell & Essa Yacoub & Kamil Ugurbil & Jesper Andersson & Christian F. Beckmann & Mark Jenkinson & Stephen M. Smith , 2016. "A multi-modal parcellation of human cerebral cortex," Nature, Nature, vol. 536(7615), pages 171-178, August.
    7. Charrad, Malika & Ghazzali, Nadia & Boiteau, Véronique & Niknafs, Azam, 2014. "NbClust: An R Package for Determining the Relevant Number of Clusters in a Data Set," Journal of Statistical Software, Foundation for Open Access Statistics, vol. 61(i06).
    8. Kevin M. Anderson & Meghan A. Collins & Rowena Chin & Tian Ge & Monica D. Rosenberg & Avram J. Holmes, 2020. "Transcriptional and imaging-genetic association of cortical interneurons, brain function, and schizophrenia risk," Nature Communications, Nature, vol. 11(1), pages 1-15, December.
    9. Gabriel Cuellar-Partida & Joyce Y. Tung & Nicholas Eriksson & Eva Albrecht & Fazil Aliev & Ole A. Andreassen & Inês Barroso & Jacques S. Beckmann & Marco P. Boks & Dorret I. Boomsma & Heather A. Boyd , 2021. "Genome-wide association study identifies 48 common genetic variants associated with handedness," Nature Human Behaviour, Nature, vol. 5(1), pages 59-70, January.
    10. Zhiqiang Sha & Dick Schijven & Amaia Carrion-Castillo & Marc Joliot & Bernard Mazoyer & Simon E. Fisher & Fabrice Crivello & Clyde Francks, 2021. "The genetic architecture of structural left–right asymmetry of the human brain," Nature Human Behaviour, Nature, vol. 5(9), pages 1226-1239, September.
    11. Xi-Nian Zuo & Ting Xu & Michael Peter Milham, 2019. "Harnessing reliability for neuroscience research," Nature Human Behaviour, Nature, vol. 3(8), pages 768-771, August.
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    Cited by:

    1. Dardo Tomasi & Nora D. Volkow, 2024. "Associations between handedness and brain functional connectivity patterns in children," Nature Communications, Nature, vol. 15(1), pages 1-12, December.

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