Subcortical influences on the topology of cortical networks align with functional processing hierarchies

fMRI of the human brain reveals spatiotemporal patterns of functional connectivity (FC), forming distinct cortical networks. Lately, subcortical contributions to these configurations are receiving renewed interest, but investigations rarely focus explicitly on their effects on cortico-cortical FC. H...

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Main Authors: Fabian Hirsch, Afra Wohlschlaeger
Format: Article
Language:English
Published: Elsevier 2023-12-01
Series:NeuroImage
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S1053811923005682
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author Fabian Hirsch
Afra Wohlschlaeger
author_facet Fabian Hirsch
Afra Wohlschlaeger
author_sort Fabian Hirsch
collection DOAJ
description fMRI of the human brain reveals spatiotemporal patterns of functional connectivity (FC), forming distinct cortical networks. Lately, subcortical contributions to these configurations are receiving renewed interest, but investigations rarely focus explicitly on their effects on cortico-cortical FC. Here, we employ a straightforward multivariable approach and graph-theoretic tools to assess subcortical impact on topological features of cortical networks. Given recent evidence showing that structures like the thalamus and basal ganglia integrate input from multiple networks, we expect increased segregation between cortical networks after removal of subcortical effects on their FC patterns. We analyze resting state data of young and healthy participants (male and female; N = 100) from the human connectome project. We find that overall, the cortical network architecture becomes less segregated, and more integrated, when subcortical influences are accounted for. Underlying these global effects are the following trends: ‘Transmodal’ systems become more integrated with the rest of the network, while ‘unimodal’ networks show the opposite effect. For single nodes this hierarchical organization is reflected by a close correspondence with the spatial layout of the principal gradient of FC (Margulies et al., 2016). Lastly, we show that the limbic system is significantly less coherent with subcortical influences removed. The findings are validated in a (split-sample) replication dataset. Our results provide new insight regarding the interplay between subcortex and cortical networks, by putting the integrative impact of subcortex in the context of macroscale patterns of cortical organization.
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spelling doaj.art-e27ece219fc54ea79ec390658ddf22ac2023-11-16T06:06:00ZengElsevierNeuroImage1095-95722023-12-01283120417Subcortical influences on the topology of cortical networks align with functional processing hierarchiesFabian Hirsch0Afra Wohlschlaeger1Corresponding author.; Department of Diagnostic and Interventional Neuroradiology, Klinikum R.d.Isar, Technical University Munich, Ismaninger Str. 22, Munich 81675, GermanyDepartment of Diagnostic and Interventional Neuroradiology, Klinikum R.d.Isar, Technical University Munich, Ismaninger Str. 22, Munich 81675, GermanyfMRI of the human brain reveals spatiotemporal patterns of functional connectivity (FC), forming distinct cortical networks. Lately, subcortical contributions to these configurations are receiving renewed interest, but investigations rarely focus explicitly on their effects on cortico-cortical FC. Here, we employ a straightforward multivariable approach and graph-theoretic tools to assess subcortical impact on topological features of cortical networks. Given recent evidence showing that structures like the thalamus and basal ganglia integrate input from multiple networks, we expect increased segregation between cortical networks after removal of subcortical effects on their FC patterns. We analyze resting state data of young and healthy participants (male and female; N = 100) from the human connectome project. We find that overall, the cortical network architecture becomes less segregated, and more integrated, when subcortical influences are accounted for. Underlying these global effects are the following trends: ‘Transmodal’ systems become more integrated with the rest of the network, while ‘unimodal’ networks show the opposite effect. For single nodes this hierarchical organization is reflected by a close correspondence with the spatial layout of the principal gradient of FC (Margulies et al., 2016). Lastly, we show that the limbic system is significantly less coherent with subcortical influences removed. The findings are validated in a (split-sample) replication dataset. Our results provide new insight regarding the interplay between subcortex and cortical networks, by putting the integrative impact of subcortex in the context of macroscale patterns of cortical organization.http://www.sciencedirect.com/science/article/pii/S1053811923005682Functional connectivitySubcortexGradientGraph analysisLimbic systemThalamus
spellingShingle Fabian Hirsch
Afra Wohlschlaeger
Subcortical influences on the topology of cortical networks align with functional processing hierarchies
NeuroImage
Functional connectivity
Subcortex
Gradient
Graph analysis
Limbic system
Thalamus
title Subcortical influences on the topology of cortical networks align with functional processing hierarchies
title_full Subcortical influences on the topology of cortical networks align with functional processing hierarchies
title_fullStr Subcortical influences on the topology of cortical networks align with functional processing hierarchies
title_full_unstemmed Subcortical influences on the topology of cortical networks align with functional processing hierarchies
title_short Subcortical influences on the topology of cortical networks align with functional processing hierarchies
title_sort subcortical influences on the topology of cortical networks align with functional processing hierarchies
topic Functional connectivity
Subcortex
Gradient
Graph analysis
Limbic system
Thalamus
url http://www.sciencedirect.com/science/article/pii/S1053811923005682
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