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

Abstract 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...

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Main Authors: Sayak Bhattacharya, Matthieu B. L. Cauchois, Pablo A. Iglesias, Zhe Sage Chen
Format: Article
Language:English
Published: Nature Publishing Group 2021-07-01
Series:Scientific Reports
Online Access:https://doi.org/10.1038/s41598-021-93618-6
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spelling doaj-86a22cd2e9b042608d413a0baa296c162021-07-18T11:26:04ZengNature Publishing GroupScientific Reports2045-23222021-07-0111111910.1038/s41598-021-93618-6The impact of a closed-loop thalamocortical model on the spatiotemporal dynamics of cortical and thalamic traveling wavesSayak Bhattacharya0Matthieu B. L. Cauchois1Pablo A. Iglesias2Zhe Sage Chen3Department of Electrical and Computer Engineering, Whiting School of Engineering, Johns Hopkins UniversityDepartment of Mechanical Engineering, Whiting School of Engineering, Johns Hopkins UniversityDepartment of Electrical and Computer Engineering, Whiting School of Engineering, Johns Hopkins UniversityDepartment of Psychiatry, Department of Neuroscience and Physiology, Neuroscience Institute, New York University Grossman School of MedicineAbstract 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.https://doi.org/10.1038/s41598-021-93618-6
collection DOAJ
language English
format Article
sources DOAJ
author Sayak Bhattacharya
Matthieu B. L. Cauchois
Pablo A. Iglesias
Zhe Sage Chen
spellingShingle Sayak Bhattacharya
Matthieu B. L. Cauchois
Pablo A. Iglesias
Zhe Sage Chen
The impact of a closed-loop thalamocortical model on the spatiotemporal dynamics of cortical and thalamic traveling waves
Scientific Reports
author_facet Sayak Bhattacharya
Matthieu B. L. Cauchois
Pablo A. Iglesias
Zhe Sage Chen
author_sort Sayak Bhattacharya
title 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_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_sort impact of a closed-loop thalamocortical model on the spatiotemporal dynamics of cortical and thalamic traveling waves
publisher Nature Publishing Group
series Scientific Reports
issn 2045-2322
publishDate 2021-07-01
description Abstract 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.
url https://doi.org/10.1038/s41598-021-93618-6
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