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Spontaneous variability in gamma dynamics described by a damped harmonic oscillator driven by noise

Circuits of excitatory and inhibitory neurons generate gamma-rhythmic activity (30–80 Hz). Gamma-cycles show spontaneous variability in amplitude and duration. To investigate the mechanisms underlying this variability, we recorded local-field-potentials (LFPs) and spikes from awake macaque V1. We de...

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Autores principales: Spyropoulos, Georgios, Saponati, Matteo, Dowdall, Jarrod Robert, Schölvinck, Marieke Louise, Bosman, Conrado Arturo, Lima, Bruss, Peter, Alina, Onorato, Irene, Klon-Lipok, Johanna, Roese, Rasmus, Neuenschwander, Sergio, Fries, Pascal, Vinck, Martin
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9018758/
https://www.ncbi.nlm.nih.gov/pubmed/35440540
http://dx.doi.org/10.1038/s41467-022-29674-x
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author Spyropoulos, Georgios
Saponati, Matteo
Dowdall, Jarrod Robert
Schölvinck, Marieke Louise
Bosman, Conrado Arturo
Lima, Bruss
Peter, Alina
Onorato, Irene
Klon-Lipok, Johanna
Roese, Rasmus
Neuenschwander, Sergio
Fries, Pascal
Vinck, Martin
author_facet Spyropoulos, Georgios
Saponati, Matteo
Dowdall, Jarrod Robert
Schölvinck, Marieke Louise
Bosman, Conrado Arturo
Lima, Bruss
Peter, Alina
Onorato, Irene
Klon-Lipok, Johanna
Roese, Rasmus
Neuenschwander, Sergio
Fries, Pascal
Vinck, Martin
author_sort Spyropoulos, Georgios
collection PubMed
description Circuits of excitatory and inhibitory neurons generate gamma-rhythmic activity (30–80 Hz). Gamma-cycles show spontaneous variability in amplitude and duration. To investigate the mechanisms underlying this variability, we recorded local-field-potentials (LFPs) and spikes from awake macaque V1. We developed a noise-robust method to detect gamma-cycle amplitudes and durations, which showed a weak but positive correlation. This correlation, and the joint amplitude-duration distribution, is well reproduced by a noise-driven damped harmonic oscillator. This model accurately fits LFP power-spectra, is equivalent to a linear, noise-driven E-I circuit, and recapitulates two additional features of gamma: (1) Amplitude-duration correlations decrease with oscillation strength; (2) amplitudes and durations exhibit strong and weak autocorrelations, respectively, depending on oscillation strength. Finally, longer gamma-cycles are associated with stronger spike-synchrony, but lower spike-rates in both (putative) excitatory and inhibitory neurons. In sum, V1 gamma-dynamics are well described by the simplest possible model of gamma: A damped harmonic oscillator driven by noise.
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spelling pubmed-90187582022-04-28 Spontaneous variability in gamma dynamics described by a damped harmonic oscillator driven by noise Spyropoulos, Georgios Saponati, Matteo Dowdall, Jarrod Robert Schölvinck, Marieke Louise Bosman, Conrado Arturo Lima, Bruss Peter, Alina Onorato, Irene Klon-Lipok, Johanna Roese, Rasmus Neuenschwander, Sergio Fries, Pascal Vinck, Martin Nat Commun Article Circuits of excitatory and inhibitory neurons generate gamma-rhythmic activity (30–80 Hz). Gamma-cycles show spontaneous variability in amplitude and duration. To investigate the mechanisms underlying this variability, we recorded local-field-potentials (LFPs) and spikes from awake macaque V1. We developed a noise-robust method to detect gamma-cycle amplitudes and durations, which showed a weak but positive correlation. This correlation, and the joint amplitude-duration distribution, is well reproduced by a noise-driven damped harmonic oscillator. This model accurately fits LFP power-spectra, is equivalent to a linear, noise-driven E-I circuit, and recapitulates two additional features of gamma: (1) Amplitude-duration correlations decrease with oscillation strength; (2) amplitudes and durations exhibit strong and weak autocorrelations, respectively, depending on oscillation strength. Finally, longer gamma-cycles are associated with stronger spike-synchrony, but lower spike-rates in both (putative) excitatory and inhibitory neurons. In sum, V1 gamma-dynamics are well described by the simplest possible model of gamma: A damped harmonic oscillator driven by noise. Nature Publishing Group UK 2022-04-19 /pmc/articles/PMC9018758/ /pubmed/35440540 http://dx.doi.org/10.1038/s41467-022-29674-x Text en © The Author(s) 2022 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
Spyropoulos, Georgios
Saponati, Matteo
Dowdall, Jarrod Robert
Schölvinck, Marieke Louise
Bosman, Conrado Arturo
Lima, Bruss
Peter, Alina
Onorato, Irene
Klon-Lipok, Johanna
Roese, Rasmus
Neuenschwander, Sergio
Fries, Pascal
Vinck, Martin
Spontaneous variability in gamma dynamics described by a damped harmonic oscillator driven by noise
title Spontaneous variability in gamma dynamics described by a damped harmonic oscillator driven by noise
title_full Spontaneous variability in gamma dynamics described by a damped harmonic oscillator driven by noise
title_fullStr Spontaneous variability in gamma dynamics described by a damped harmonic oscillator driven by noise
title_full_unstemmed Spontaneous variability in gamma dynamics described by a damped harmonic oscillator driven by noise
title_short Spontaneous variability in gamma dynamics described by a damped harmonic oscillator driven by noise
title_sort spontaneous variability in gamma dynamics described by a damped harmonic oscillator driven by noise
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9018758/
https://www.ncbi.nlm.nih.gov/pubmed/35440540
http://dx.doi.org/10.1038/s41467-022-29674-x
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