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The impact of a closed-loop thalamocortical model on the spatiotemporal dynamics of cortical and thalamic traveling waves

Propagation of activity in spatially structured neuronal networks has been observed in awake, anesthetized, and sleeping brains. How these wave patterns emerge and organize across brain structures, and how network connectivity affects spatiotemporal neural activity remains unclear. Here, we develop...

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Autores principales: Bhattacharya, Sayak, Cauchois, Matthieu B. L., Iglesias, Pablo A., Chen, Zhe Sage
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8277909/
https://www.ncbi.nlm.nih.gov/pubmed/34257333
http://dx.doi.org/10.1038/s41598-021-93618-6
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author Bhattacharya, Sayak
Cauchois, Matthieu B. L.
Iglesias, Pablo A.
Chen, Zhe Sage
author_facet Bhattacharya, Sayak
Cauchois, Matthieu B. L.
Iglesias, Pablo A.
Chen, Zhe Sage
author_sort Bhattacharya, Sayak
collection PubMed
description Propagation of activity in spatially structured neuronal networks has been observed in awake, anesthetized, and sleeping brains. How these wave patterns emerge and organize across brain structures, and how network connectivity affects spatiotemporal neural activity remains unclear. Here, we develop a computational model of a two-dimensional thalamocortical network, which gives rise to emergent traveling waves similar to those observed experimentally. We illustrate how spontaneous and evoked oscillatory activity in space and time emerge using a closed-loop thalamocortical architecture, sustaining smooth waves in the cortex and staggered waves in the thalamus. We further show that intracortical and thalamocortical network connectivity, cortical excitation/inhibition balance, and thalamocortical or corticothalamic delay can independently or jointly change the spatiotemporal patterns (radial, planar and rotating waves) and characteristics (speed, direction, and frequency) of cortical and thalamic traveling waves. Computer simulations predict that increased thalamic inhibition induces slower cortical frequencies and that enhanced cortical excitation increases traveling wave speed and frequency. Overall, our results provide insight into the genesis and sustainability of thalamocortical spatiotemporal patterns, showing how simple synaptic alterations cause varied spontaneous and evoked wave patterns. Our model and simulations highlight the need for spatially spread neural recordings to uncover critical circuit mechanisms for brain functions.
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spelling pubmed-82779092021-07-15 The impact of a closed-loop thalamocortical model on the spatiotemporal dynamics of cortical and thalamic traveling waves Bhattacharya, Sayak Cauchois, Matthieu B. L. Iglesias, Pablo A. Chen, Zhe Sage Sci Rep Article Propagation of activity in spatially structured neuronal networks has been observed in awake, anesthetized, and sleeping brains. How these wave patterns emerge and organize across brain structures, and how network connectivity affects spatiotemporal neural activity remains unclear. Here, we develop a computational model of a two-dimensional thalamocortical network, which gives rise to emergent traveling waves similar to those observed experimentally. We illustrate how spontaneous and evoked oscillatory activity in space and time emerge using a closed-loop thalamocortical architecture, sustaining smooth waves in the cortex and staggered waves in the thalamus. We further show that intracortical and thalamocortical network connectivity, cortical excitation/inhibition balance, and thalamocortical or corticothalamic delay can independently or jointly change the spatiotemporal patterns (radial, planar and rotating waves) and characteristics (speed, direction, and frequency) of cortical and thalamic traveling waves. Computer simulations predict that increased thalamic inhibition induces slower cortical frequencies and that enhanced cortical excitation increases traveling wave speed and frequency. Overall, our results provide insight into the genesis and sustainability of thalamocortical spatiotemporal patterns, showing how simple synaptic alterations cause varied spontaneous and evoked wave patterns. Our model and simulations highlight the need for spatially spread neural recordings to uncover critical circuit mechanisms for brain functions. Nature Publishing Group UK 2021-07-13 /pmc/articles/PMC8277909/ /pubmed/34257333 http://dx.doi.org/10.1038/s41598-021-93618-6 Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Bhattacharya, Sayak
Cauchois, Matthieu B. L.
Iglesias, Pablo A.
Chen, Zhe Sage
The impact of a closed-loop thalamocortical model on the spatiotemporal dynamics of cortical and thalamic traveling waves
title The impact of a closed-loop thalamocortical model on the spatiotemporal dynamics of cortical and thalamic traveling waves
title_full The impact of a closed-loop thalamocortical model on the spatiotemporal dynamics of cortical and thalamic traveling waves
title_fullStr The impact of a closed-loop thalamocortical model on the spatiotemporal dynamics of cortical and thalamic traveling waves
title_full_unstemmed The impact of a closed-loop thalamocortical model on the spatiotemporal dynamics of cortical and thalamic traveling waves
title_short The impact of a closed-loop thalamocortical model on the spatiotemporal dynamics of cortical and thalamic traveling waves
title_sort impact of a closed-loop thalamocortical model on the spatiotemporal dynamics of cortical and thalamic traveling waves
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8277909/
https://www.ncbi.nlm.nih.gov/pubmed/34257333
http://dx.doi.org/10.1038/s41598-021-93618-6
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