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Network Path Convergence Shapes Low-Level Processing in the Visual Cortex

Hierarchical counterstream via feedforward and feedback interactions is a major organizing principle of the cerebral cortex. The counterstream, as a topological feature of the network of cortical areas, is captured by the convergence and divergence of paths through directed links. So defined, the co...

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Autores principales: Varga, Bálint, Soós, Bettina, Jákli, Balázs, Bálint, Eszter, Somogyvári, Zoltán, Négyessy, László
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8181740/
https://www.ncbi.nlm.nih.gov/pubmed/34108867
http://dx.doi.org/10.3389/fnsys.2021.645709
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author Varga, Bálint
Soós, Bettina
Jákli, Balázs
Bálint, Eszter
Somogyvári, Zoltán
Négyessy, László
author_facet Varga, Bálint
Soós, Bettina
Jákli, Balázs
Bálint, Eszter
Somogyvári, Zoltán
Négyessy, László
author_sort Varga, Bálint
collection PubMed
description Hierarchical counterstream via feedforward and feedback interactions is a major organizing principle of the cerebral cortex. The counterstream, as a topological feature of the network of cortical areas, is captured by the convergence and divergence of paths through directed links. So defined, the convergence degree (CD) reveals the reciprocal nature of forward and backward connections, and also hierarchically relevant integrative properties of areas through their inward and outward connections. We asked if topology shapes large-scale cortical functioning by studying the role of CD in network resilience and Granger causal coupling in a model of hierarchical network dynamics. Our results indicate that topological synchronizability is highly vulnerable to attacking edges based on CD, while global network efficiency depends mostly on edge betweenness, a measure of the connectedness of a link. Furthermore, similar to anatomical hierarchy determined by the laminar distribution of connections, CD highly correlated with causal coupling in feedforward gamma, and feedback alpha-beta band synchronizations in a well-studied subnetwork, including low-level visual cortical areas. In contrast, causal coupling did not correlate with edge betweenness. Considering the entire network, the CD-based hierarchy correlated well with both the anatomical and functional hierarchy for low-level areas that are far apart in the hierarchy. Conversely, in a large part of the anatomical network where hierarchical distances are small between the areas, the correlations were not significant. These findings suggest that CD-based and functional hierarchies are interrelated in low-level processing in the visual cortex. Our results are consistent with the idea that the interplay of multiple hierarchical features forms the basis of flexible functional cortical interactions.
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spelling pubmed-81817402021-06-08 Network Path Convergence Shapes Low-Level Processing in the Visual Cortex Varga, Bálint Soós, Bettina Jákli, Balázs Bálint, Eszter Somogyvári, Zoltán Négyessy, László Front Syst Neurosci Neuroscience Hierarchical counterstream via feedforward and feedback interactions is a major organizing principle of the cerebral cortex. The counterstream, as a topological feature of the network of cortical areas, is captured by the convergence and divergence of paths through directed links. So defined, the convergence degree (CD) reveals the reciprocal nature of forward and backward connections, and also hierarchically relevant integrative properties of areas through their inward and outward connections. We asked if topology shapes large-scale cortical functioning by studying the role of CD in network resilience and Granger causal coupling in a model of hierarchical network dynamics. Our results indicate that topological synchronizability is highly vulnerable to attacking edges based on CD, while global network efficiency depends mostly on edge betweenness, a measure of the connectedness of a link. Furthermore, similar to anatomical hierarchy determined by the laminar distribution of connections, CD highly correlated with causal coupling in feedforward gamma, and feedback alpha-beta band synchronizations in a well-studied subnetwork, including low-level visual cortical areas. In contrast, causal coupling did not correlate with edge betweenness. Considering the entire network, the CD-based hierarchy correlated well with both the anatomical and functional hierarchy for low-level areas that are far apart in the hierarchy. Conversely, in a large part of the anatomical network where hierarchical distances are small between the areas, the correlations were not significant. These findings suggest that CD-based and functional hierarchies are interrelated in low-level processing in the visual cortex. Our results are consistent with the idea that the interplay of multiple hierarchical features forms the basis of flexible functional cortical interactions. Frontiers Media S.A. 2021-05-24 /pmc/articles/PMC8181740/ /pubmed/34108867 http://dx.doi.org/10.3389/fnsys.2021.645709 Text en Copyright © 2021 Varga, Soós, Jákli, Bálint, Somogyvári and Négyessy. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Neuroscience
Varga, Bálint
Soós, Bettina
Jákli, Balázs
Bálint, Eszter
Somogyvári, Zoltán
Négyessy, László
Network Path Convergence Shapes Low-Level Processing in the Visual Cortex
title Network Path Convergence Shapes Low-Level Processing in the Visual Cortex
title_full Network Path Convergence Shapes Low-Level Processing in the Visual Cortex
title_fullStr Network Path Convergence Shapes Low-Level Processing in the Visual Cortex
title_full_unstemmed Network Path Convergence Shapes Low-Level Processing in the Visual Cortex
title_short Network Path Convergence Shapes Low-Level Processing in the Visual Cortex
title_sort network path convergence shapes low-level processing in the visual cortex
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8181740/
https://www.ncbi.nlm.nih.gov/pubmed/34108867
http://dx.doi.org/10.3389/fnsys.2021.645709
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