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Microstructural and functional gradients are increasingly dissociated in transmodal cortices

Author

Listed:
  • Casey Paquola
  • Reinder Vos De Wael
  • Konrad Wagstyl
  • Richard A I Bethlehem
  • Seok-Jun Hong
  • Jakob Seidlitz
  • Edward T Bullmore
  • Alan C Evans
  • Bratislav Misic
  • Daniel S Margulies
  • Jonathan Smallwood
  • Boris C Bernhardt

Abstract

While the role of cortical microstructure in organising neural function is well established, it remains unclear how structural constraints can give rise to more flexible elements of cognition. While nonhuman primate research has demonstrated a close structure–function correspondence, the relationship between microstructure and function remains poorly understood in humans, in part because of the reliance on post mortem analyses, which cannot be directly related to functional data. To overcome this barrier, we developed a novel approach to model the similarity of microstructural profiles sampled in the direction of cortical columns. Our approach was initially formulated based on an ultra-high–resolution 3D histological reconstruction of an entire human brain and then translated to myelin-sensitive magnetic resonance imaging (MRI) data in a large cohort of healthy adults. This novel method identified a system-level gradient of microstructural differentiation traversing from primary sensory to limbic regions that followed shifts in laminar differentiation and cytoarchitectural complexity. Importantly, while microstructural and functional gradients described a similar hierarchy, they became increasingly dissociated in transmodal default mode and fronto–parietal networks. Meta-analytic decoding of these topographic dissociations highlighted involvement in higher-level aspects of cognition, such as cognitive control and social cognition. Our findings demonstrate a relative decoupling of macroscale functional from microstructural gradients in transmodal regions, which likely contributes to the flexible role these regions play in human cognition.Modelling cortico-cortical networks of microstructural similarity in post mortem and in vivo brains reveals consistent gradients of microstructural differentiation running from sensory to transmodal cortices, and allows single-subject investigation of structure-function correspondence.

Suggested Citation

  • Casey Paquola & Reinder Vos De Wael & Konrad Wagstyl & Richard A I Bethlehem & Seok-Jun Hong & Jakob Seidlitz & Edward T Bullmore & Alan C Evans & Bratislav Misic & Daniel S Margulies & Jonathan Small, 2019. "Microstructural and functional gradients are increasingly dissociated in transmodal cortices," PLOS Biology, Public Library of Science, vol. 17(5), pages 1-28, May.
  • Handle: RePEc:plo:pbio00:3000284
    DOI: 10.1371/journal.pbio.3000284
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    1. 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.
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    11. Evan Collins & Omar Chishti & Sami Obaid & Hari McGrath & Alex King & Xilin Shen & Jagriti Arora & Xenophon Papademetris & R. Todd Constable & Dennis D. Spencer & Hitten P. Zaveri, 2024. "Mapping the structure-function relationship along macroscale gradients in the human brain," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
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    16. Xiaolu Kong & Ru Kong & Csaba Orban & Peng Wang & Shaoshi Zhang & Kevin Anderson & Avram Holmes & John D. Murray & Gustavo Deco & Martijn Heuvel & B. T. Thomas Yeo, 2021. "Sensory-motor cortices shape functional connectivity dynamics in the human brain," Nature Communications, Nature, vol. 12(1), pages 1-15, December.
    17. Vincent Bazinet & Justine Y. Hansen & Reinder Vos de Wael & Boris C. Bernhardt & Martijn P. Heuvel & Bratislav Misic, 2023. "Assortative mixing in micro-architecturally annotated brain connectomes," Nature Communications, Nature, vol. 14(1), pages 1-16, December.

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