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Lévy walk dynamics explain gamma burst patterns in primate cerebral cortex

Lévy walks describe patterns of intermittent motion with variable step sizes. In complex biological systems, Lévy walks (non-Brownian, superdiffusive random walks) are associated with behaviors such as search patterns of animals foraging for food. Here we show that Lévy walks also describe patterns...

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Autores principales: Liu, Yuxi, Long, Xian, Martin, Paul R., Solomon, Samuel G., Gong, Pulin
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8206356/
https://www.ncbi.nlm.nih.gov/pubmed/34131276
http://dx.doi.org/10.1038/s42003-021-02256-1
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author Liu, Yuxi
Long, Xian
Martin, Paul R.
Solomon, Samuel G.
Gong, Pulin
author_facet Liu, Yuxi
Long, Xian
Martin, Paul R.
Solomon, Samuel G.
Gong, Pulin
author_sort Liu, Yuxi
collection PubMed
description Lévy walks describe patterns of intermittent motion with variable step sizes. In complex biological systems, Lévy walks (non-Brownian, superdiffusive random walks) are associated with behaviors such as search patterns of animals foraging for food. Here we show that Lévy walks also describe patterns of oscillatory activity in primate cerebral cortex. We used a combination of empirical observation and modeling to investigate high-frequency (gamma band) local field potential activity in visual motion-processing cortical area MT of marmoset monkeys. We found that gamma activity is organized as localized burst patterns that propagate across the cortical surface with Lévy walk dynamics. Lévy walks are fundamentally different from either global synchronization, or regular propagating waves, because they include large steps that enable activity patterns to move rapidly over cortical modules. The presence of Lévy walk dynamics therefore represents a previously undiscovered mode of brain activity, and implies a novel way for the cortex to compute. We apply a biophysically realistic circuit model to explain that the Lévy walk dynamics arise from critical-state transitions between asynchronous and localized propagating wave states, and that these dynamics yield optimal spatial sampling of the cortical sheet. We hypothesise that Lévy walk dynamics could help the cortex to efficiently process variable inputs, and to find links in patterns of activity among sparsely spiking populations of neurons.
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spelling pubmed-82063562021-07-01 Lévy walk dynamics explain gamma burst patterns in primate cerebral cortex Liu, Yuxi Long, Xian Martin, Paul R. Solomon, Samuel G. Gong, Pulin Commun Biol Article Lévy walks describe patterns of intermittent motion with variable step sizes. In complex biological systems, Lévy walks (non-Brownian, superdiffusive random walks) are associated with behaviors such as search patterns of animals foraging for food. Here we show that Lévy walks also describe patterns of oscillatory activity in primate cerebral cortex. We used a combination of empirical observation and modeling to investigate high-frequency (gamma band) local field potential activity in visual motion-processing cortical area MT of marmoset monkeys. We found that gamma activity is organized as localized burst patterns that propagate across the cortical surface with Lévy walk dynamics. Lévy walks are fundamentally different from either global synchronization, or regular propagating waves, because they include large steps that enable activity patterns to move rapidly over cortical modules. The presence of Lévy walk dynamics therefore represents a previously undiscovered mode of brain activity, and implies a novel way for the cortex to compute. We apply a biophysically realistic circuit model to explain that the Lévy walk dynamics arise from critical-state transitions between asynchronous and localized propagating wave states, and that these dynamics yield optimal spatial sampling of the cortical sheet. We hypothesise that Lévy walk dynamics could help the cortex to efficiently process variable inputs, and to find links in patterns of activity among sparsely spiking populations of neurons. Nature Publishing Group UK 2021-06-15 /pmc/articles/PMC8206356/ /pubmed/34131276 http://dx.doi.org/10.1038/s42003-021-02256-1 Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open Access This 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 license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license 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 license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Liu, Yuxi
Long, Xian
Martin, Paul R.
Solomon, Samuel G.
Gong, Pulin
Lévy walk dynamics explain gamma burst patterns in primate cerebral cortex
title Lévy walk dynamics explain gamma burst patterns in primate cerebral cortex
title_full Lévy walk dynamics explain gamma burst patterns in primate cerebral cortex
title_fullStr Lévy walk dynamics explain gamma burst patterns in primate cerebral cortex
title_full_unstemmed Lévy walk dynamics explain gamma burst patterns in primate cerebral cortex
title_short Lévy walk dynamics explain gamma burst patterns in primate cerebral cortex
title_sort lévy walk dynamics explain gamma burst patterns in primate cerebral cortex
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8206356/
https://www.ncbi.nlm.nih.gov/pubmed/34131276
http://dx.doi.org/10.1038/s42003-021-02256-1
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