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A blueprint of mammalian cortical connectomes

The cerebral cortex of mammals exhibits intricate interareal wiring. Moreover, mammalian cortices differ vastly in size, cytological composition, and phylogenetic distance. Given such complexity and pronounced species differences, it is a considerable challenge to decipher organizational principles...

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Autores principales: Goulas, Alexandros, Majka, Piotr, Rosa, Marcello G. P., Hilgetag, Claus C.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6456226/
https://www.ncbi.nlm.nih.gov/pubmed/30901324
http://dx.doi.org/10.1371/journal.pbio.2005346
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author Goulas, Alexandros
Majka, Piotr
Rosa, Marcello G. P.
Hilgetag, Claus C.
author_facet Goulas, Alexandros
Majka, Piotr
Rosa, Marcello G. P.
Hilgetag, Claus C.
author_sort Goulas, Alexandros
collection PubMed
description The cerebral cortex of mammals exhibits intricate interareal wiring. Moreover, mammalian cortices differ vastly in size, cytological composition, and phylogenetic distance. Given such complexity and pronounced species differences, it is a considerable challenge to decipher organizational principles of mammalian connectomes. Here, we demonstrate species-specific and species-general unifying principles linking the physical, cytological, and connectional dimensions of architecture in the mouse, cat, marmoset, and macaque monkey. The existence of connections is related to the cytology of cortical areas, in addition to the role of physical distance, but this relation is attenuated in mice and marmoset monkeys. The cytoarchitectonic cortical gradients, and not the rostrocaudal axis of the cortex, are closely linked to the laminar origin of connections, a principle that allows the extrapolation of this connectional feature to humans. Lastly, a network core, with a central role under different modes of network communication, characterizes all cortical connectomes. We observe a displacement of the network core in mammals, with a shift of the core of cats and macaque monkeys toward the less neuronally dense areas of the cerebral cortex. This displacement has functional ramifications but also entails a potential increased degree of vulnerability to pathology. In sum, our results sketch out a blueprint of mammalian connectomes consisting of species-specific and species-general links between the connectional, physical, and cytological dimensions of the cerebral cortex, possibly reflecting variations and persistence of evolutionarily conserved mechanisms and cellular phenomena. Our framework elucidates organizational principles that encompass but also extend beyond the wiring economy principle imposed by the physical embedding of the cerebral cortex.
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spelling pubmed-64562262019-05-03 A blueprint of mammalian cortical connectomes Goulas, Alexandros Majka, Piotr Rosa, Marcello G. P. Hilgetag, Claus C. PLoS Biol Research Article The cerebral cortex of mammals exhibits intricate interareal wiring. Moreover, mammalian cortices differ vastly in size, cytological composition, and phylogenetic distance. Given such complexity and pronounced species differences, it is a considerable challenge to decipher organizational principles of mammalian connectomes. Here, we demonstrate species-specific and species-general unifying principles linking the physical, cytological, and connectional dimensions of architecture in the mouse, cat, marmoset, and macaque monkey. The existence of connections is related to the cytology of cortical areas, in addition to the role of physical distance, but this relation is attenuated in mice and marmoset monkeys. The cytoarchitectonic cortical gradients, and not the rostrocaudal axis of the cortex, are closely linked to the laminar origin of connections, a principle that allows the extrapolation of this connectional feature to humans. Lastly, a network core, with a central role under different modes of network communication, characterizes all cortical connectomes. We observe a displacement of the network core in mammals, with a shift of the core of cats and macaque monkeys toward the less neuronally dense areas of the cerebral cortex. This displacement has functional ramifications but also entails a potential increased degree of vulnerability to pathology. In sum, our results sketch out a blueprint of mammalian connectomes consisting of species-specific and species-general links between the connectional, physical, and cytological dimensions of the cerebral cortex, possibly reflecting variations and persistence of evolutionarily conserved mechanisms and cellular phenomena. Our framework elucidates organizational principles that encompass but also extend beyond the wiring economy principle imposed by the physical embedding of the cerebral cortex. Public Library of Science 2019-03-22 /pmc/articles/PMC6456226/ /pubmed/30901324 http://dx.doi.org/10.1371/journal.pbio.2005346 Text en © 2019 Goulas 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
Goulas, Alexandros
Majka, Piotr
Rosa, Marcello G. P.
Hilgetag, Claus C.
A blueprint of mammalian cortical connectomes
title A blueprint of mammalian cortical connectomes
title_full A blueprint of mammalian cortical connectomes
title_fullStr A blueprint of mammalian cortical connectomes
title_full_unstemmed A blueprint of mammalian cortical connectomes
title_short A blueprint of mammalian cortical connectomes
title_sort blueprint of mammalian cortical connectomes
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6456226/
https://www.ncbi.nlm.nih.gov/pubmed/30901324
http://dx.doi.org/10.1371/journal.pbio.2005346
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