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Dynamic reconfiguration of macaque brain networks during natural vision

Lookup NU author(s): Michael Ortiz Rios, Dr Fabien BalezeauORCiD, Dr Marcus Haag, Professor Michael Schmid, Professor Marcus Kaiser

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This work is licensed under a Creative Commons Attribution 4.0 International License (CC BY 4.0).


Abstract

© 2021 The AuthorsNatural 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.


Publication metadata

Author(s): Ortiz-Rios M, Balezeau F, Haag M, Schmid MC, Kaiser M

Publication type: Article

Publication status: Published

Journal: NeuroImage

Year: 2021

Volume: 244

Print publication date: 01/12/2021

Online publication date: 23/09/2021

Acceptance date: 22/09/2021

Date deposited: 05/10/2023

ISSN (print): 1053-8119

ISSN (electronic): 1095-9572

Publisher: Academic Press Inc.

URL: https://doi.org/10.1016/j.neuroimage.2021.118615

DOI: 10.1016/j.neuroimage.2021.118615


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Funding

Funder referenceFunder name
102037
637638Commission of the European Communities
EP/N031962/1EPSRC
Guangci Professorship Program of Rui Jin Hospital
NS/A000026/1
Wellcome Trust

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