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Nonoptimal component placement of the human connectome supports variable brain dynamics

Neural systems are shaped by multiple constraints, balancing region communication with the cost of establishing and maintaining physical connections. It has been suggested that the lengths of neural projections be minimized, reducing their spatial and metabolic impact on the organism. However, long-...

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Autores principales: Hayward, Christopher James, Huo, Siyu, Chen, Xue, Kaiser, Marcus
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MIT Press 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10270717/
https://www.ncbi.nlm.nih.gov/pubmed/37334003
http://dx.doi.org/10.1162/netn_a_00282
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author Hayward, Christopher James
Huo, Siyu
Chen, Xue
Kaiser, Marcus
author_facet Hayward, Christopher James
Huo, Siyu
Chen, Xue
Kaiser, Marcus
author_sort Hayward, Christopher James
collection PubMed
description Neural systems are shaped by multiple constraints, balancing region communication with the cost of establishing and maintaining physical connections. It has been suggested that the lengths of neural projections be minimized, reducing their spatial and metabolic impact on the organism. However, long-range connections are prevalent in the connectomes across various species, and thus, rather than rewiring connections to reduce length, an alternative theory proposes that the brain minimizes total wiring length through a suitable positioning of regions, termed component placement optimization. Previous studies in nonhuman primates have refuted this idea by identifying a nonoptimal component placement, where a spatial rearrangement of brain regions in silico leads to a reduced total wiring length. Here, for the first time in humans, we test for component placement optimization. We show a nonoptimal component placement for all subjects in our sample from the Human Connectome Project (N = 280; aged 22–30 years; 138 females), suggesting the presence of constraints—such as the reduction of processing steps between regions—that compete with the elevated spatial and metabolic costs. Additionally, by simulating communication between brain regions, we argue that this suboptimal component placement supports dynamics that benefit cognition.
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spelling pubmed-102707172023-06-16 Nonoptimal component placement of the human connectome supports variable brain dynamics Hayward, Christopher James Huo, Siyu Chen, Xue Kaiser, Marcus Netw Neurosci Research Article Neural systems are shaped by multiple constraints, balancing region communication with the cost of establishing and maintaining physical connections. It has been suggested that the lengths of neural projections be minimized, reducing their spatial and metabolic impact on the organism. However, long-range connections are prevalent in the connectomes across various species, and thus, rather than rewiring connections to reduce length, an alternative theory proposes that the brain minimizes total wiring length through a suitable positioning of regions, termed component placement optimization. Previous studies in nonhuman primates have refuted this idea by identifying a nonoptimal component placement, where a spatial rearrangement of brain regions in silico leads to a reduced total wiring length. Here, for the first time in humans, we test for component placement optimization. We show a nonoptimal component placement for all subjects in our sample from the Human Connectome Project (N = 280; aged 22–30 years; 138 females), suggesting the presence of constraints—such as the reduction of processing steps between regions—that compete with the elevated spatial and metabolic costs. Additionally, by simulating communication between brain regions, we argue that this suboptimal component placement supports dynamics that benefit cognition. MIT Press 2023-01-01 /pmc/articles/PMC10270717/ /pubmed/37334003 http://dx.doi.org/10.1162/netn_a_00282 Text en © 2022 Massachusetts Institute of Technology https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. For a full description of the license, please visit https://creativecommons.org/licenses/by/4.0/.
spellingShingle Research Article
Hayward, Christopher James
Huo, Siyu
Chen, Xue
Kaiser, Marcus
Nonoptimal component placement of the human connectome supports variable brain dynamics
title Nonoptimal component placement of the human connectome supports variable brain dynamics
title_full Nonoptimal component placement of the human connectome supports variable brain dynamics
title_fullStr Nonoptimal component placement of the human connectome supports variable brain dynamics
title_full_unstemmed Nonoptimal component placement of the human connectome supports variable brain dynamics
title_short Nonoptimal component placement of the human connectome supports variable brain dynamics
title_sort nonoptimal component placement of the human connectome supports variable brain dynamics
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10270717/
https://www.ncbi.nlm.nih.gov/pubmed/37334003
http://dx.doi.org/10.1162/netn_a_00282
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