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Kuramoto model simulation of neural hubs and dynamic synchrony in the human cerebral connectome

BACKGROUND: The topological structure of the wiring of the mammalian brain cortex plays an important role in shaping the functional dynamics of large-scale neural activity. Due to their central embedding in the network, high degree hub regions and their connections (often referred to as the ‘rich cl...

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Autores principales: Schmidt, Ruben, LaFleur, Karl J. R., de Reus, Marcel A., van den Berg, Leonard H., van den Heuvel, Martijn P.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4556019/
https://www.ncbi.nlm.nih.gov/pubmed/26329640
http://dx.doi.org/10.1186/s12868-015-0193-z
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author Schmidt, Ruben
LaFleur, Karl J. R.
de Reus, Marcel A.
van den Berg, Leonard H.
van den Heuvel, Martijn P.
author_facet Schmidt, Ruben
LaFleur, Karl J. R.
de Reus, Marcel A.
van den Berg, Leonard H.
van den Heuvel, Martijn P.
author_sort Schmidt, Ruben
collection PubMed
description BACKGROUND: The topological structure of the wiring of the mammalian brain cortex plays an important role in shaping the functional dynamics of large-scale neural activity. Due to their central embedding in the network, high degree hub regions and their connections (often referred to as the ‘rich club’) have been hypothesized to facilitate intermodular neural communication and global integration of information by means of synchronization. Here, we examined the theoretical role of anatomical hubs and their wiring in brain dynamics. The Kuramoto model was used to simulate interaction of cortical brain areas by means of coupled phase oscillators—with anatomical connections between regions derived from diffusion weighted imaging and module assignment of brain regions based on empirically determined resting-state data. RESULTS: Our findings show that synchrony among hub nodes was higher than any module’s intramodular synchrony (p < 10(−4), for cortical coupling strengths, λ, in the range 0.02 < λ < 0.05), suggesting that hub nodes lead the functional modules in the process of synchronization. Furthermore, suppressing structural connectivity among hub nodes resulted in an elevated modular state (p < 4.1 × l0(−3), 0.015 < λ < 0.04), indicating that hub-to-hub connections are critical in intermodular synchronization. Finally, perturbing the oscillatory behavior of hub nodes prevented functional modules from synchronizing, implying that synchronization of functional modules is dependent on the hub nodes’ behavior. CONCLUSION: Our results converge on anatomical hubs having a leading role in intermodular synchronization and integration in the human brain. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12868-015-0193-z) contains supplementary material, which is available to authorized users.
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spelling pubmed-45560192015-09-02 Kuramoto model simulation of neural hubs and dynamic synchrony in the human cerebral connectome Schmidt, Ruben LaFleur, Karl J. R. de Reus, Marcel A. van den Berg, Leonard H. van den Heuvel, Martijn P. BMC Neurosci Research Article BACKGROUND: The topological structure of the wiring of the mammalian brain cortex plays an important role in shaping the functional dynamics of large-scale neural activity. Due to their central embedding in the network, high degree hub regions and their connections (often referred to as the ‘rich club’) have been hypothesized to facilitate intermodular neural communication and global integration of information by means of synchronization. Here, we examined the theoretical role of anatomical hubs and their wiring in brain dynamics. The Kuramoto model was used to simulate interaction of cortical brain areas by means of coupled phase oscillators—with anatomical connections between regions derived from diffusion weighted imaging and module assignment of brain regions based on empirically determined resting-state data. RESULTS: Our findings show that synchrony among hub nodes was higher than any module’s intramodular synchrony (p < 10(−4), for cortical coupling strengths, λ, in the range 0.02 < λ < 0.05), suggesting that hub nodes lead the functional modules in the process of synchronization. Furthermore, suppressing structural connectivity among hub nodes resulted in an elevated modular state (p < 4.1 × l0(−3), 0.015 < λ < 0.04), indicating that hub-to-hub connections are critical in intermodular synchronization. Finally, perturbing the oscillatory behavior of hub nodes prevented functional modules from synchronizing, implying that synchronization of functional modules is dependent on the hub nodes’ behavior. CONCLUSION: Our results converge on anatomical hubs having a leading role in intermodular synchronization and integration in the human brain. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12868-015-0193-z) contains supplementary material, which is available to authorized users. BioMed Central 2015-09-02 /pmc/articles/PMC4556019/ /pubmed/26329640 http://dx.doi.org/10.1186/s12868-015-0193-z Text en © Schmidt et al. 2015 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Schmidt, Ruben
LaFleur, Karl J. R.
de Reus, Marcel A.
van den Berg, Leonard H.
van den Heuvel, Martijn P.
Kuramoto model simulation of neural hubs and dynamic synchrony in the human cerebral connectome
title Kuramoto model simulation of neural hubs and dynamic synchrony in the human cerebral connectome
title_full Kuramoto model simulation of neural hubs and dynamic synchrony in the human cerebral connectome
title_fullStr Kuramoto model simulation of neural hubs and dynamic synchrony in the human cerebral connectome
title_full_unstemmed Kuramoto model simulation of neural hubs and dynamic synchrony in the human cerebral connectome
title_short Kuramoto model simulation of neural hubs and dynamic synchrony in the human cerebral connectome
title_sort kuramoto model simulation of neural hubs and dynamic synchrony in the human cerebral connectome
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4556019/
https://www.ncbi.nlm.nih.gov/pubmed/26329640
http://dx.doi.org/10.1186/s12868-015-0193-z
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