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Developmental trajectory of Caenorhabditis elegans nervous system governs its structural organization

A central problem of neuroscience involves uncovering the principles governing the organization of nervous systems which ensure robustness in brain development. The nematode Caenorhabditis elegans provides us with a model organism for studying this question. In this paper, we focus on the invariant...

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Autores principales: Pathak, Anand, Chatterjee, Nivedita, Sinha, Sitabhra
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6959611/
https://www.ncbi.nlm.nih.gov/pubmed/31895942
http://dx.doi.org/10.1371/journal.pcbi.1007602
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author Pathak, Anand
Chatterjee, Nivedita
Sinha, Sitabhra
author_facet Pathak, Anand
Chatterjee, Nivedita
Sinha, Sitabhra
author_sort Pathak, Anand
collection PubMed
description A central problem of neuroscience involves uncovering the principles governing the organization of nervous systems which ensure robustness in brain development. The nematode Caenorhabditis elegans provides us with a model organism for studying this question. In this paper, we focus on the invariant connection structure and spatial arrangement of the neurons comprising the somatic neuronal network of this organism to understand the key developmental constraints underlying its design. We observe that neurons with certain shared characteristics—such as, neural process lengths, birth time cohort, lineage and bilateral symmetry—exhibit a preference for connecting to each other. Recognizing the existence of such homophily and their relative degree of importance in determining connection probability within neurons (for example, in synapses, symmetric pairing is the most dominant factor followed by birth time cohort, process length and lineage) helps in connecting specific neuronal attributes to the topological organization of the network. Further, the functional identities of neurons appear to dictate the temporal hierarchy of their appearance during the course of development. Providing crucial insights into principles that may be common across many organisms, our study shows how the trajectory in the developmental landscape constrains the structural organization of a nervous system.
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spelling pubmed-69596112020-01-26 Developmental trajectory of Caenorhabditis elegans nervous system governs its structural organization Pathak, Anand Chatterjee, Nivedita Sinha, Sitabhra PLoS Comput Biol Research Article A central problem of neuroscience involves uncovering the principles governing the organization of nervous systems which ensure robustness in brain development. The nematode Caenorhabditis elegans provides us with a model organism for studying this question. In this paper, we focus on the invariant connection structure and spatial arrangement of the neurons comprising the somatic neuronal network of this organism to understand the key developmental constraints underlying its design. We observe that neurons with certain shared characteristics—such as, neural process lengths, birth time cohort, lineage and bilateral symmetry—exhibit a preference for connecting to each other. Recognizing the existence of such homophily and their relative degree of importance in determining connection probability within neurons (for example, in synapses, symmetric pairing is the most dominant factor followed by birth time cohort, process length and lineage) helps in connecting specific neuronal attributes to the topological organization of the network. Further, the functional identities of neurons appear to dictate the temporal hierarchy of their appearance during the course of development. Providing crucial insights into principles that may be common across many organisms, our study shows how the trajectory in the developmental landscape constrains the structural organization of a nervous system. Public Library of Science 2020-01-02 /pmc/articles/PMC6959611/ /pubmed/31895942 http://dx.doi.org/10.1371/journal.pcbi.1007602 Text en © 2020 Pathak 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
Pathak, Anand
Chatterjee, Nivedita
Sinha, Sitabhra
Developmental trajectory of Caenorhabditis elegans nervous system governs its structural organization
title Developmental trajectory of Caenorhabditis elegans nervous system governs its structural organization
title_full Developmental trajectory of Caenorhabditis elegans nervous system governs its structural organization
title_fullStr Developmental trajectory of Caenorhabditis elegans nervous system governs its structural organization
title_full_unstemmed Developmental trajectory of Caenorhabditis elegans nervous system governs its structural organization
title_short Developmental trajectory of Caenorhabditis elegans nervous system governs its structural organization
title_sort developmental trajectory of caenorhabditis elegans nervous system governs its structural organization
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6959611/
https://www.ncbi.nlm.nih.gov/pubmed/31895942
http://dx.doi.org/10.1371/journal.pcbi.1007602
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