Long-range functional connections mirror and link microarchitectural and cognitive hierarchies in the human brain.

Humans Magnetic Resonance Imaging / methods Brain Mapping / methods Neocortex Cognition Emotions Neural Pathways Connectome / methods
connectome cortical gradients cortical microstructure functional connectivity neuroimaging

Journal

Cerebral cortex (New York, N.Y. : 1991)
ISSN: 1460-2199
Titre abrégé: Cereb Cortex
Pays: United States
ID NLM: 9110718

Informations de publication

Date de publication:
20 02 2023
Historique:
received: 16 11 2021
revised: 30 03 2022
accepted: 01 04 2022
pubmed: 22 5 2022
medline: 4 3 2023
entrez: 21 5 2022
Statut: ppublish

Résumé

Higher-order cognition is hypothesized to be implemented via distributed cortical networks that are linked via long-range connections. However, it is unknown how computational advantages of long-range connections reflect cortical microstructure and microcircuitry. We investigated this question by (i) profiling long-range cortical connectivity using resting-state functional magnetic resonance imaging (MRI) and cortico-cortical geodesic distance mapping, (ii) assessing how long-range connections reflect local brain microarchitecture, and (iii) examining the microarchitectural similarity of regions connected through long-range connections. Analysis of 2 independent datasets indicated that sensory/motor areas had more clustered short-range connections, while transmodal association systems hosted distributed, long-range connections. Meta-analytical decoding suggested that this topographical difference mirrored shifts in cognitive function, from perception/action towards emotional/social processing. Analysis of myelin-sensitive in vivo MRI as well as postmortem histology and transcriptomics datasets established that gradients in functional connectivity distance are paralleled by those present in cortical microarchitecture. Notably, long-range connections were found to link spatially remote regions of association cortex with an unexpectedly similar microarchitecture. By mapping covarying topographies of long-range functional connections and cortical microcircuits, the current work provides insights into structure-function relations in human neocortex.

Sections du résumé

BACKGROUND
Higher-order cognition is hypothesized to be implemented via distributed cortical networks that are linked via long-range connections. However, it is unknown how computational advantages of long-range connections reflect cortical microstructure and microcircuitry.
METHODS
We investigated this question by (i) profiling long-range cortical connectivity using resting-state functional magnetic resonance imaging (MRI) and cortico-cortical geodesic distance mapping, (ii) assessing how long-range connections reflect local brain microarchitecture, and (iii) examining the microarchitectural similarity of regions connected through long-range connections.
RESULTS
Analysis of 2 independent datasets indicated that sensory/motor areas had more clustered short-range connections, while transmodal association systems hosted distributed, long-range connections. Meta-analytical decoding suggested that this topographical difference mirrored shifts in cognitive function, from perception/action towards emotional/social processing. Analysis of myelin-sensitive in vivo MRI as well as postmortem histology and transcriptomics datasets established that gradients in functional connectivity distance are paralleled by those present in cortical microarchitecture. Notably, long-range connections were found to link spatially remote regions of association cortex with an unexpectedly similar microarchitecture.
CONCLUSIONS
By mapping covarying topographies of long-range functional connections and cortical microcircuits, the current work provides insights into structure-function relations in human neocortex.

Identifiants

DOI: 10.1093/cercor/bhac172 PMID: 35596951 PMC: PMC9977370
pubmed: 35596951
pii: 6590368
doi: 10.1093/cercor/bhac172
pmc: PMC9977370
doi:

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

1782-1798

Subventions

Organisme : CIHR
ID : FDN-154298
Pays : Canada

Informations de copyright

© The Author(s) 2022. Published by Oxford University Press. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.

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Auteurs

Yezhou Wang (Y)

Multimodal Imaging and Connectome Analysis Laboratory, McConnell Brain Imaging Centre, Department of Neurology and Neurosurgery and Montreal Neurological Institute and Hospital, McGill University, 3801 University Street, Montreal, Quebec H3A2B4, Canada.

Jessica Royer (J)

Multimodal Imaging and Connectome Analysis Laboratory, McConnell Brain Imaging Centre, Department of Neurology and Neurosurgery and Montreal Neurological Institute and Hospital, McGill University, 3801 University Street, Montreal, Quebec H3A2B4, Canada.

Bo-Yong Park (BY)

Multimodal Imaging and Connectome Analysis Laboratory, McConnell Brain Imaging Centre, Department of Neurology and Neurosurgery and Montreal Neurological Institute and Hospital, McGill University, 3801 University Street, Montreal, Quebec H3A2B4, Canada.
Department of Data Science, Inha University, 100 Inha-ro, Michuhol-gu, Incheon 22212, South Korea.
Center for Neuroscience Imaging Research, Institute for Basic Science, Sungkyunkwan University, Seobu-ro 2066, Jangan-gu, Suwon 16419, South Korea.
ORCID: 0000-0001-7096-337X

Reinder Vos de Wael (R)

Multimodal Imaging and Connectome Analysis Laboratory, McConnell Brain Imaging Centre, Department of Neurology and Neurosurgery and Montreal Neurological Institute and Hospital, McGill University, 3801 University Street, Montreal, Quebec H3A2B4, Canada.

Sara Larivière (S)

Multimodal Imaging and Connectome Analysis Laboratory, McConnell Brain Imaging Centre, Department of Neurology and Neurosurgery and Montreal Neurological Institute and Hospital, McGill University, 3801 University Street, Montreal, Quebec H3A2B4, Canada.

Shahin Tavakol (S)

Multimodal Imaging and Connectome Analysis Laboratory, McConnell Brain Imaging Centre, Department of Neurology and Neurosurgery and Montreal Neurological Institute and Hospital, McGill University, 3801 University Street, Montreal, Quebec H3A2B4, Canada.

Raul Rodriguez-Cruces (R)

Multimodal Imaging and Connectome Analysis Laboratory, McConnell Brain Imaging Centre, Department of Neurology and Neurosurgery and Montreal Neurological Institute and Hospital, McGill University, 3801 University Street, Montreal, Quebec H3A2B4, Canada.

Casey Paquola (C)

Multimodal Imaging and Connectome Analysis Laboratory, McConnell Brain Imaging Centre, Department of Neurology and Neurosurgery and Montreal Neurological Institute and Hospital, McGill University, 3801 University Street, Montreal, Quebec H3A2B4, Canada.
Institute of Neuroscience and Medicine, Brain & Behaviour (INM-7), Research Centre Jülich, Jülich, Germany.

Seok-Jun Hong (SJ)

Center for Neuroscience Imaging Research, Institute for Basic Science, Sungkyunkwan University, Seobu-ro 2066, Jangan-gu, Suwon 16419, South Korea.
Department of Biomedical Engineering, Sungkyunkwan University, Seobu-ro 2066, Jangan-gu, Suwon 16419, South Korea.
ORCID: 0000-0002-1847-578X

Daniel S Margulies (DS)

Cognitive Neuroanatomy Lab, Integrative Neuroscience and Cognition Centre, University of Paris and CRNS, INCC - UMR 8002, Rue des Saint-Pères 75006, Paris.

Jonathan Smallwood (J)

Department of Psychology, Queen's University, 62 Arch Street, Humphrey Hall, Room 232 Kingston, Ontario K7L 3N6, Canada.

Sofie L Valk (SL)

Institute of Neuroscience and Medicine, Brain & Behaviour (INM-7), Research Centre Jülich, Jülich, Germany.
Otto Hahn Group Cognitive Neurogenetics, Max Planck Institute for Human Cognitive and Brain Sciences, Stephanstraße 1A. Leipzig D-04103, Germany.
Institute of Systems Neuroscience, Heinrich Heine University, Moorenstr. 5, Düsseldorf 40225, Germany.
ORCID: 0000-0003-2998-6849

Alan C Evans (AC)

Multimodal Imaging and Connectome Analysis Laboratory, McConnell Brain Imaging Centre, Department of Neurology and Neurosurgery and Montreal Neurological Institute and Hospital, McGill University, 3801 University Street, Montreal, Quebec H3A2B4, Canada.

Boris C Bernhardt (BC)

Multimodal Imaging and Connectome Analysis Laboratory, McConnell Brain Imaging Centre, Department of Neurology and Neurosurgery and Montreal Neurological Institute and Hospital, McGill University, 3801 University Street, Montreal, Quebec H3A2B4, Canada.
ORCID: 0000-0001-9256-6041

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Classifications MeSH

questionsmedicales.fr › Eucaryotes › Animaux › Chordés › Vertébrés › Mammifères › Eutheria › Primates › Haplorhini › Catarrhini › Hominidae › Humains › Long-range functional connections mirror and...
questionsmedicales.fr › Diagnostic › Techniques et procédures diagnostiques › Imagerie diagnostique › Tomographie › Imagerie par résonance magnétique › Long-range functional connections mirror and...
questionsmedicales.fr › Techniques d'investigation › Neuroimagerie › Neuroimagerie fonctionnelle › Cartographie cérébrale › Long-range functional connections mirror and...
questionsmedicales.fr › Système nerveux › Système nerveux central › Encéphale › Prosencéphale › Télencéphale › Cerveau › Cortex cérébral › Néocortex › Long-range functional connections mirror and...
questionsmedicales.fr › Phénomènes psychologiques › Processus mentaux › Cognition › Long-range functional connections mirror and...
questionsmedicales.fr › Comportement et mécanismes comportementaux › Émotions › Long-range functional connections mirror and...
questionsmedicales.fr › Système nerveux › Voies nerveuses › Long-range functional connections mirror and...
questionsmedicales.fr › Techniques d'investigation › Neuroimagerie › Neuroimagerie fonctionnelle › Cartographie cérébrale › Connectome › Long-range functional connections mirror and...