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Dynamic reconfiguration of macaque brain networks during natural vision

Ortiz-Rios, Michael; Balezeau, Fabien; Haag, Marcus; Schmid, Michael C.; Kaiser, Marcus

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Authors

Michael Ortiz-Rios

Fabien Balezeau

Marcus Haag

Michael C. Schmid

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MARCUS KAISER MARCUS.KAISER@NOTTINGHAM.AC.UK
Professor of Neuroinformatics



Abstract

Natural vision engages a wide range of higher-level regions that integrate visual information over the large-scale brain network. How interareal connectivity reconfigures during the processing of ongoing natural visual scenes and how these dynamic functional changes relate to the underlaying anatomical links between regions is not well understood. Here, we hypothesized that macaque visual brain regions are poly-functional sharing the capacity to change their configuration state depending on the nature of visual input. To address this hypothesis, we reconstructed networks from in-vivo diffusion-weighted imaging (DWI) and functional magnetic resonance imaging (fMRI) data obtained in four alert macaque monkeys viewing naturalistic movie scenes. At first, we characterized network properties and found greater interhemispheric density and greater inter-subject variability in free-viewing networks as compared to structural networks. From the structural connectivity, we then captured modules on which we identified hubs during free-viewing that formed a widespread visuo-saccadic network across frontal (FEF, 46v), parietal (LIP, Tpt), and occipitotemporal modules (MT, V4, TEm), and that excluded primary visual cortex. Inter-subject variability of well-connected hubs reflected subject-specific configurations that largely recruited occipito-parietal and frontal modules. Across the cerebral hemispheres, free-viewing networks showed higher correlations among long-distance brain regions as compared to structural networks. From these findings, we hypothesized that long-distance interareal connectivity could reconfigure depending on the ongoing changes in visual scenes. Testing this hypothesis by applying temporally resolved functional connectivity we observed that many structurally defined areas (such as areas V4, MT/MST and LIP) were poly-functional as they were recruited as hub members of multiple network states that changed during the presentation of scenes containing objects, motion, faces, and actions. We suggest that functional flexibility in macaque macroscale brain networks is required for the efficient interareal communication during active natural vision. To further promote the use of naturalistic free-viewing paradigms and increase the development of macaque neuroimaging resources, we share our datasets in the PRIME-DE consortium.

Citation

Ortiz-Rios, M., Balezeau, F., Haag, M., Schmid, M. C., & Kaiser, M. (2021). Dynamic reconfiguration of macaque brain networks during natural vision. NeuroImage, 244, Article 118615. https://doi.org/10.1016/j.neuroimage.2021.118615

Journal Article Type Article
Acceptance Date Sep 22, 2021
Online Publication Date Sep 25, 2021
Publication Date Dec 1, 2021
Deposit Date Oct 23, 2022
Publicly Available Date Mar 28, 2024
Journal NeuroImage
Print ISSN 1053-8119
Electronic ISSN 1095-9572
Publisher Elsevier
Peer Reviewed Peer Reviewed
Volume 244
Article Number 118615
DOI https://doi.org/10.1016/j.neuroimage.2021.118615
Public URL https://nottingham-repository.worktribe.com/output/9085273
Publisher URL https://www.sciencedirect.com/science/article/pii/S1053811921008880

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