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Do Vascular Networks Branch Optimally or Randomly across Spatial Scales?
Modern models that derive allometric relationships between metabolic rate and body mass are based on the architectural design of the cardiovascular system and presume sibling vessels are symmetric in terms of radius, length, flow rate, and pressure. Here, we study the cardiovascular structure of the...
Autores principales: | , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Public Library of Science
2016
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5130167/ https://www.ncbi.nlm.nih.gov/pubmed/27902691 http://dx.doi.org/10.1371/journal.pcbi.1005223 |
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author | Tekin, Elif Hunt, David Newberry, Mitchell G. Savage, Van M. |
author_facet | Tekin, Elif Hunt, David Newberry, Mitchell G. Savage, Van M. |
author_sort | Tekin, Elif |
collection | PubMed |
description | Modern models that derive allometric relationships between metabolic rate and body mass are based on the architectural design of the cardiovascular system and presume sibling vessels are symmetric in terms of radius, length, flow rate, and pressure. Here, we study the cardiovascular structure of the human head and torso and of a mouse lung based on three-dimensional images processed via our software Angicart. In contrast to modern allometric theories, we find systematic patterns of asymmetry in vascular branching, potentially explaining previously documented mismatches between predictions (power-law or concave curvature) and observed empirical data (convex curvature) for the allometric scaling of metabolic rate. To examine why these systematic asymmetries in vascular branching might arise, we construct a mathematical framework to derive predictions based on local, junction-level optimality principles that have been proposed to be favored in the course of natural selection and development. The two most commonly used principles are material-cost optimizations (construction materials or blood volume) and optimization of efficient flow via minimization of power loss. We show that material-cost optimization solutions match with distributions for asymmetric branching across the whole network but do not match well for individual junctions. Consequently, we also explore random branching that is constrained at scales that range from local (junction-level) to global (whole network). We find that material-cost optimizations are the strongest predictor of vascular branching in the human head and torso, whereas locally or intermediately constrained random branching is comparable to material-cost optimizations for the mouse lung. These differences could be attributable to developmentally-programmed local branching for larger vessels and constrained random branching for smaller vessels. |
format | Online Article Text |
id | pubmed-5130167 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2016 |
publisher | Public Library of Science |
record_format | MEDLINE/PubMed |
spelling | pubmed-51301672016-12-15 Do Vascular Networks Branch Optimally or Randomly across Spatial Scales? Tekin, Elif Hunt, David Newberry, Mitchell G. Savage, Van M. PLoS Comput Biol Research Article Modern models that derive allometric relationships between metabolic rate and body mass are based on the architectural design of the cardiovascular system and presume sibling vessels are symmetric in terms of radius, length, flow rate, and pressure. Here, we study the cardiovascular structure of the human head and torso and of a mouse lung based on three-dimensional images processed via our software Angicart. In contrast to modern allometric theories, we find systematic patterns of asymmetry in vascular branching, potentially explaining previously documented mismatches between predictions (power-law or concave curvature) and observed empirical data (convex curvature) for the allometric scaling of metabolic rate. To examine why these systematic asymmetries in vascular branching might arise, we construct a mathematical framework to derive predictions based on local, junction-level optimality principles that have been proposed to be favored in the course of natural selection and development. The two most commonly used principles are material-cost optimizations (construction materials or blood volume) and optimization of efficient flow via minimization of power loss. We show that material-cost optimization solutions match with distributions for asymmetric branching across the whole network but do not match well for individual junctions. Consequently, we also explore random branching that is constrained at scales that range from local (junction-level) to global (whole network). We find that material-cost optimizations are the strongest predictor of vascular branching in the human head and torso, whereas locally or intermediately constrained random branching is comparable to material-cost optimizations for the mouse lung. These differences could be attributable to developmentally-programmed local branching for larger vessels and constrained random branching for smaller vessels. Public Library of Science 2016-11-30 /pmc/articles/PMC5130167/ /pubmed/27902691 http://dx.doi.org/10.1371/journal.pcbi.1005223 Text en © 2016 Tekin et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. |
spellingShingle | Research Article Tekin, Elif Hunt, David Newberry, Mitchell G. Savage, Van M. Do Vascular Networks Branch Optimally or Randomly across Spatial Scales? |
title | Do Vascular Networks Branch Optimally or Randomly across Spatial Scales? |
title_full | Do Vascular Networks Branch Optimally or Randomly across Spatial Scales? |
title_fullStr | Do Vascular Networks Branch Optimally or Randomly across Spatial Scales? |
title_full_unstemmed | Do Vascular Networks Branch Optimally or Randomly across Spatial Scales? |
title_short | Do Vascular Networks Branch Optimally or Randomly across Spatial Scales? |
title_sort | do vascular networks branch optimally or randomly across spatial scales? |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5130167/ https://www.ncbi.nlm.nih.gov/pubmed/27902691 http://dx.doi.org/10.1371/journal.pcbi.1005223 |
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