Influence of wiring cost on the large-scale architecture of human cortical connectivity.

In the past two decades some fundamental properties of cortical connectivity have been discovered: small-world structure, pronounced hierarchical and modular organisation, and strong core and rich-club structures. A common assumption when interpreting results of this kind is that the observed struct...

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Main Authors: David Samu, Anil K Seth, Thomas Nowotny
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2014-04-01
Series:PLoS Computational Biology
Online Access:https://www.ncbi.nlm.nih.gov/pmc/articles/pmid/24699277/?tool=EBI
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spelling doaj-5f4f6766607a47d19fd6b85055dc323f2021-06-17T04:33:39ZengPublic Library of Science (PLoS)PLoS Computational Biology1553-734X1553-73582014-04-01104e100355710.1371/journal.pcbi.1003557Influence of wiring cost on the large-scale architecture of human cortical connectivity.David SamuAnil K SethThomas NowotnyIn the past two decades some fundamental properties of cortical connectivity have been discovered: small-world structure, pronounced hierarchical and modular organisation, and strong core and rich-club structures. A common assumption when interpreting results of this kind is that the observed structural properties are present to enable the brain's function. However, the brain is also embedded into the limited space of the skull and its wiring has associated developmental and metabolic costs. These basic physical and economic aspects place separate, often conflicting, constraints on the brain's connectivity, which must be characterized in order to understand the true relationship between brain structure and function. To address this challenge, here we ask which, and to what extent, aspects of the structural organisation of the brain are conserved if we preserve specific spatial and topological properties of the brain but otherwise randomise its connectivity. We perform a comparative analysis of a connectivity map of the cortical connectome both on high- and low-resolutions utilising three different types of surrogate networks: spatially unconstrained ('random'), connection length preserving ('spatial'), and connection length optimised ('reduced') surrogates. We find that unconstrained randomisation markedly diminishes all investigated architectural properties of cortical connectivity. By contrast, spatial and reduced surrogates largely preserve most properties and, interestingly, often more so in the reduced surrogates. Specifically, our results suggest that the cortical network is less tightly integrated than its spatial constraints would allow, but more strongly segregated than its spatial constraints would necessitate. We additionally find that hierarchical organisation and rich-club structure of the cortical connectivity are largely preserved in spatial and reduced surrogates and hence may be partially attributable to cortical wiring constraints. In contrast, the high modularity and strong s-core of the high-resolution cortical network are significantly stronger than in the surrogates, underlining their potential functional relevance in the brain.https://www.ncbi.nlm.nih.gov/pmc/articles/pmid/24699277/?tool=EBI
collection DOAJ
language English
format Article
sources DOAJ
author David Samu
Anil K Seth
Thomas Nowotny
spellingShingle David Samu
Anil K Seth
Thomas Nowotny
Influence of wiring cost on the large-scale architecture of human cortical connectivity.
PLoS Computational Biology
author_facet David Samu
Anil K Seth
Thomas Nowotny
author_sort David Samu
title Influence of wiring cost on the large-scale architecture of human cortical connectivity.
title_short Influence of wiring cost on the large-scale architecture of human cortical connectivity.
title_full Influence of wiring cost on the large-scale architecture of human cortical connectivity.
title_fullStr Influence of wiring cost on the large-scale architecture of human cortical connectivity.
title_full_unstemmed Influence of wiring cost on the large-scale architecture of human cortical connectivity.
title_sort influence of wiring cost on the large-scale architecture of human cortical connectivity.
publisher Public Library of Science (PLoS)
series PLoS Computational Biology
issn 1553-734X
1553-7358
publishDate 2014-04-01
description In the past two decades some fundamental properties of cortical connectivity have been discovered: small-world structure, pronounced hierarchical and modular organisation, and strong core and rich-club structures. A common assumption when interpreting results of this kind is that the observed structural properties are present to enable the brain's function. However, the brain is also embedded into the limited space of the skull and its wiring has associated developmental and metabolic costs. These basic physical and economic aspects place separate, often conflicting, constraints on the brain's connectivity, which must be characterized in order to understand the true relationship between brain structure and function. To address this challenge, here we ask which, and to what extent, aspects of the structural organisation of the brain are conserved if we preserve specific spatial and topological properties of the brain but otherwise randomise its connectivity. We perform a comparative analysis of a connectivity map of the cortical connectome both on high- and low-resolutions utilising three different types of surrogate networks: spatially unconstrained ('random'), connection length preserving ('spatial'), and connection length optimised ('reduced') surrogates. We find that unconstrained randomisation markedly diminishes all investigated architectural properties of cortical connectivity. By contrast, spatial and reduced surrogates largely preserve most properties and, interestingly, often more so in the reduced surrogates. Specifically, our results suggest that the cortical network is less tightly integrated than its spatial constraints would allow, but more strongly segregated than its spatial constraints would necessitate. We additionally find that hierarchical organisation and rich-club structure of the cortical connectivity are largely preserved in spatial and reduced surrogates and hence may be partially attributable to cortical wiring constraints. In contrast, the high modularity and strong s-core of the high-resolution cortical network are significantly stronger than in the surrogates, underlining their potential functional relevance in the brain.
url https://www.ncbi.nlm.nih.gov/pmc/articles/pmid/24699277/?tool=EBI
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