A multi-scale cortical wiring space links cellular architecture and functional dynamics in the human brain.


Journal

PLoS biology
ISSN: 1545-7885
Titre abrégé: PLoS Biol
Pays: United States
ID NLM: 101183755

Informations de publication

Date de publication:
11 2020
Historique:
received: 26 03 2020
accepted: 02 11 2020
revised: 10 12 2020
pubmed: 1 12 2020
medline: 5 1 2021
entrez: 30 11 2020
Statut: epublish

Résumé

The vast net of fibres within and underneath the cortex is optimised to support the convergence of different levels of brain organisation. Here, we propose a novel coordinate system of the human cortex based on an advanced model of its connectivity. Our approach is inspired by seminal, but so far largely neglected models of cortico-cortical wiring established by postmortem anatomical studies and capitalises on cutting-edge in vivo neuroimaging and machine learning. The new model expands the currently prevailing diffusion magnetic resonance imaging (MRI) tractography approach by incorporation of additional features of cortical microstructure and cortico-cortical proximity. Studying several datasets and different parcellation schemes, we could show that our coordinate system robustly recapitulates established sensory-limbic and anterior-posterior dimensions of brain organisation. A series of validation experiments showed that the new wiring space reflects cortical microcircuit features (including pyramidal neuron depth and glial expression) and allowed for competitive simulations of functional connectivity and dynamics based on resting-state functional magnetic resonance imaging (rs-fMRI) and human intracranial electroencephalography (EEG) coherence. Our results advance our understanding of how cell-specific neurobiological gradients produce a hierarchical cortical wiring scheme that is concordant with increasing functional sophistication of human brain organisation. Our evaluations demonstrate the cortical wiring space bridges across scales of neural organisation and can be easily translated to single individuals.

Identifiants

pubmed: 33253185
doi: 10.1371/journal.pbio.3000979
pii: PBIOLOGY-D-20-00780
pmc: PMC7728398
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

e3000979

Subventions

Organisme : CIHR
ID : FDN-154298
Pays : Canada

Déclaration de conflit d'intérêts

The authors have declared that no competing interests exist.

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Auteurs

Casey Paquola (C)

Multimodal Imaging and Connectome Analysis Lab, McConnell Brain Imaging Centre, Montreal Neurological Institute and Hospital, McGill University, Montreal, Quebec, Canada.

Jakob Seidlitz (J)

Developmental Neurogenomics Unit, National Institute of Mental Health, Bethesda, Maryland, United States of America.

Oualid Benkarim (O)

Multimodal Imaging and Connectome Analysis Lab, McConnell Brain Imaging Centre, Montreal Neurological Institute and Hospital, McGill University, Montreal, Quebec, Canada.

Jessica Royer (J)

Multimodal Imaging and Connectome Analysis Lab, McConnell Brain Imaging Centre, Montreal Neurological Institute and Hospital, McGill University, Montreal, Quebec, Canada.

Petr Klimes (P)

Montreal Neurological Institute and Hospital, McGill University, Montreal, Quebec, Canada.

Richard A I Bethlehem (RAI)

Department of Psychiatry, University of Cambridge, Cambridge, United Kingdom.

Sara Larivière (S)

Multimodal Imaging and Connectome Analysis Lab, McConnell Brain Imaging Centre, Montreal Neurological Institute and Hospital, McGill University, Montreal, Quebec, Canada.

Reinder Vos de Wael (R)

Multimodal Imaging and Connectome Analysis Lab, McConnell Brain Imaging Centre, Montreal Neurological Institute and Hospital, McGill University, Montreal, Quebec, Canada.

Raul Rodríguez-Cruces (R)

Multimodal Imaging and Connectome Analysis Lab, McConnell Brain Imaging Centre, Montreal Neurological Institute and Hospital, McGill University, Montreal, Quebec, Canada.

Jeffery A Hall (JA)

Montreal Neurological Institute and Hospital, McGill University, Montreal, Quebec, Canada.

Birgit Frauscher (B)

Montreal Neurological Institute and Hospital, McGill University, Montreal, Quebec, Canada.

Jonathan Smallwood (J)

York Neuroimaging Center, University of York, York, United Kingdom.

Boris C Bernhardt (BC)

Multimodal Imaging and Connectome Analysis Lab, McConnell Brain Imaging Centre, Montreal Neurological Institute and Hospital, McGill University, Montreal, Quebec, Canada.

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