Cargando…

Asymmetric signaling across the hierarchy of cytoarchitecture within the human connectome

Cortical variations in cytoarchitecture form a sensory-fugal axis that shapes regional profiles of extrinsic connectivity and is thought to guide signal propagation and integration across the cortical hierarchy. While neuroimaging work has shown that this axis constrains local properties of the huma...

Descripción completa

Detalles Bibliográficos
Autores principales: Parkes, Linden, Kim, Jason Z., Stiso, Jennifer, Calkins, Monica E., Cieslak, Matthew, Gur, Raquel E., Gur, Ruben C., Moore, Tyler M., Ouellet, Mathieu, Roalf, David R., Shinohara, Russell T., Wolf, Daniel H., Satterthwaite, Theodore D., Bassett, Dani S.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Association for the Advancement of Science 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9750154/
https://www.ncbi.nlm.nih.gov/pubmed/36516263
http://dx.doi.org/10.1126/sciadv.add2185
_version_ 1784850191313010688
author Parkes, Linden
Kim, Jason Z.
Stiso, Jennifer
Calkins, Monica E.
Cieslak, Matthew
Gur, Raquel E.
Gur, Ruben C.
Moore, Tyler M.
Ouellet, Mathieu
Roalf, David R.
Shinohara, Russell T.
Wolf, Daniel H.
Satterthwaite, Theodore D.
Bassett, Dani S.
author_facet Parkes, Linden
Kim, Jason Z.
Stiso, Jennifer
Calkins, Monica E.
Cieslak, Matthew
Gur, Raquel E.
Gur, Ruben C.
Moore, Tyler M.
Ouellet, Mathieu
Roalf, David R.
Shinohara, Russell T.
Wolf, Daniel H.
Satterthwaite, Theodore D.
Bassett, Dani S.
author_sort Parkes, Linden
collection PubMed
description Cortical variations in cytoarchitecture form a sensory-fugal axis that shapes regional profiles of extrinsic connectivity and is thought to guide signal propagation and integration across the cortical hierarchy. While neuroimaging work has shown that this axis constrains local properties of the human connectome, it remains unclear whether it also shapes the asymmetric signaling that arises from higher-order topology. Here, we used network control theory to examine the amount of energy required to propagate dynamics across the sensory-fugal axis. Our results revealed an asymmetry in this energy, indicating that bottom-up transitions were easier to complete compared to top-down. Supporting analyses demonstrated that asymmetries were underpinned by a connectome topology that is wired to support efficient bottom-up signaling. Lastly, we found that asymmetries correlated with differences in communicability and intrinsic neuronal time scales and lessened throughout youth. Our results show that cortical variation in cytoarchitecture may guide the formation of macroscopic connectome topology.
format Online
Article
Text
id pubmed-9750154
institution National Center for Biotechnology Information
language English
publishDate 2022
publisher American Association for the Advancement of Science
record_format MEDLINE/PubMed
spelling pubmed-97501542022-12-21 Asymmetric signaling across the hierarchy of cytoarchitecture within the human connectome Parkes, Linden Kim, Jason Z. Stiso, Jennifer Calkins, Monica E. Cieslak, Matthew Gur, Raquel E. Gur, Ruben C. Moore, Tyler M. Ouellet, Mathieu Roalf, David R. Shinohara, Russell T. Wolf, Daniel H. Satterthwaite, Theodore D. Bassett, Dani S. Sci Adv Neuroscience Cortical variations in cytoarchitecture form a sensory-fugal axis that shapes regional profiles of extrinsic connectivity and is thought to guide signal propagation and integration across the cortical hierarchy. While neuroimaging work has shown that this axis constrains local properties of the human connectome, it remains unclear whether it also shapes the asymmetric signaling that arises from higher-order topology. Here, we used network control theory to examine the amount of energy required to propagate dynamics across the sensory-fugal axis. Our results revealed an asymmetry in this energy, indicating that bottom-up transitions were easier to complete compared to top-down. Supporting analyses demonstrated that asymmetries were underpinned by a connectome topology that is wired to support efficient bottom-up signaling. Lastly, we found that asymmetries correlated with differences in communicability and intrinsic neuronal time scales and lessened throughout youth. Our results show that cortical variation in cytoarchitecture may guide the formation of macroscopic connectome topology. American Association for the Advancement of Science 2022-12-14 /pmc/articles/PMC9750154/ /pubmed/36516263 http://dx.doi.org/10.1126/sciadv.add2185 Text en Copyright © 2022 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works. Distributed under a Creative Commons Attribution NonCommercial License 4.0 (CC BY-NC). https://creativecommons.org/licenses/by-nc/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution-NonCommercial license (https://creativecommons.org/licenses/by-nc/4.0/) , which permits use, distribution, and reproduction in any medium, so long as the resultant use is not for commercial advantage and provided the original work is properly cited.
spellingShingle Neuroscience
Parkes, Linden
Kim, Jason Z.
Stiso, Jennifer
Calkins, Monica E.
Cieslak, Matthew
Gur, Raquel E.
Gur, Ruben C.
Moore, Tyler M.
Ouellet, Mathieu
Roalf, David R.
Shinohara, Russell T.
Wolf, Daniel H.
Satterthwaite, Theodore D.
Bassett, Dani S.
Asymmetric signaling across the hierarchy of cytoarchitecture within the human connectome
title Asymmetric signaling across the hierarchy of cytoarchitecture within the human connectome
title_full Asymmetric signaling across the hierarchy of cytoarchitecture within the human connectome
title_fullStr Asymmetric signaling across the hierarchy of cytoarchitecture within the human connectome
title_full_unstemmed Asymmetric signaling across the hierarchy of cytoarchitecture within the human connectome
title_short Asymmetric signaling across the hierarchy of cytoarchitecture within the human connectome
title_sort asymmetric signaling across the hierarchy of cytoarchitecture within the human connectome
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9750154/
https://www.ncbi.nlm.nih.gov/pubmed/36516263
http://dx.doi.org/10.1126/sciadv.add2185
work_keys_str_mv AT parkeslinden asymmetricsignalingacrossthehierarchyofcytoarchitecturewithinthehumanconnectome
AT kimjasonz asymmetricsignalingacrossthehierarchyofcytoarchitecturewithinthehumanconnectome
AT stisojennifer asymmetricsignalingacrossthehierarchyofcytoarchitecturewithinthehumanconnectome
AT calkinsmonicae asymmetricsignalingacrossthehierarchyofcytoarchitecturewithinthehumanconnectome
AT cieslakmatthew asymmetricsignalingacrossthehierarchyofcytoarchitecturewithinthehumanconnectome
AT gurraquele asymmetricsignalingacrossthehierarchyofcytoarchitecturewithinthehumanconnectome
AT gurrubenc asymmetricsignalingacrossthehierarchyofcytoarchitecturewithinthehumanconnectome
AT mooretylerm asymmetricsignalingacrossthehierarchyofcytoarchitecturewithinthehumanconnectome
AT ouelletmathieu asymmetricsignalingacrossthehierarchyofcytoarchitecturewithinthehumanconnectome
AT roalfdavidr asymmetricsignalingacrossthehierarchyofcytoarchitecturewithinthehumanconnectome
AT shinohararussellt asymmetricsignalingacrossthehierarchyofcytoarchitecturewithinthehumanconnectome
AT wolfdanielh asymmetricsignalingacrossthehierarchyofcytoarchitecturewithinthehumanconnectome
AT satterthwaitetheodored asymmetricsignalingacrossthehierarchyofcytoarchitecturewithinthehumanconnectome
AT bassettdanis asymmetricsignalingacrossthehierarchyofcytoarchitecturewithinthehumanconnectome