Dynamic reconfiguration of macaque brain networks during natural vision

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 anatomi...

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Main Authors: Michael Ortiz-Rios, Fabien Balezeau, Marcus Haag, Michael C. Schmid, Marcus Kaiser
Format: Article
Language:English
Published: Elsevier 2021-12-01
Series:NeuroImage
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S1053811921008880
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spelling doaj-c2207311287f4d7bbcf6fd3a252121142021-09-27T04:24:29ZengElsevierNeuroImage1095-95722021-12-01244118615Dynamic reconfiguration of macaque brain networks during natural visionMichael Ortiz-Rios0Fabien Balezeau1Marcus Haag2Michael C. Schmid3Marcus Kaiser4Bioscience Institute, Henry Welcome Building, Medical School, Framlington Place, Newcastle upon Tyne NE2 4HH, UK; Functional Imaging Laboratory, Deutsches Primatenzentrum (DPZ), Leibniz-Institut für Primatenforschung, Göttingen, Germany; Corresponding author.Bioscience Institute, Henry Welcome Building, Medical School, Framlington Place, Newcastle upon Tyne NE2 4HH, UKBioscience Institute, Henry Welcome Building, Medical School, Framlington Place, Newcastle upon Tyne NE2 4HH, UK; Shanghai Jiao Tong University, Rui Jin Hospital, Department of Functional Neurosurgery, ChinaBioscience Institute, Henry Welcome Building, Medical School, Framlington Place, Newcastle upon Tyne NE2 4HH, UK; Faculty of Science and Medicine, University of Fribourg, Chemin du Musée 5, 1700 Fribourg, SwitzerlandSchool of Computing, Urban Sciences Building, Newcastle University, Science Central, Newcastle upon Tyne NE4 5TG, UK; Precision Imaging Beacon, School of Medicine, University of Nottingham, UK; Shanghai Jiao Tong University, Rui Jin Hospital, Department of Functional Neurosurgery, ChinaNatural 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.http://www.sciencedirect.com/science/article/pii/S1053811921008880Macaque monkeyfMRIBOLDFree-viewing networksStructural networks
collection DOAJ
language English
format Article
sources DOAJ
author Michael Ortiz-Rios
Fabien Balezeau
Marcus Haag
Michael C. Schmid
Marcus Kaiser
spellingShingle Michael Ortiz-Rios
Fabien Balezeau
Marcus Haag
Michael C. Schmid
Marcus Kaiser
Dynamic reconfiguration of macaque brain networks during natural vision
NeuroImage
Macaque monkey
fMRI
BOLD
Free-viewing networks
Structural networks
author_facet Michael Ortiz-Rios
Fabien Balezeau
Marcus Haag
Michael C. Schmid
Marcus Kaiser
author_sort Michael Ortiz-Rios
title Dynamic reconfiguration of macaque brain networks during natural vision
title_short Dynamic reconfiguration of macaque brain networks during natural vision
title_full Dynamic reconfiguration of macaque brain networks during natural vision
title_fullStr Dynamic reconfiguration of macaque brain networks during natural vision
title_full_unstemmed Dynamic reconfiguration of macaque brain networks during natural vision
title_sort dynamic reconfiguration of macaque brain networks during natural vision
publisher Elsevier
series NeuroImage
issn 1095-9572
publishDate 2021-12-01
description 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.
topic Macaque monkey
fMRI
BOLD
Free-viewing networks
Structural networks
url http://www.sciencedirect.com/science/article/pii/S1053811921008880
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