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

Georgios Spyropoulos (), Matteo Saponati, Jarrod Robert Dowdall, Marieke Louise Schölvinck, Conrado Arturo Bosman, Bruss Lima, Alina Peter, Irene Onorato, Johanna Klon-Lipok, Rasmus Roese, Sergio Neuenschwander, Pascal Fries () and Martin Vinck ()
Additional contact information
Georgios Spyropoulos: Ernst Strüngmann Institute (ESI) for Neuroscience in Cooperation with Max Planck Society
Matteo Saponati: Ernst Strüngmann Institute (ESI) for Neuroscience in Cooperation with Max Planck Society
Jarrod Robert Dowdall: Ernst Strüngmann Institute (ESI) for Neuroscience in Cooperation with Max Planck Society
Marieke Louise Schölvinck: Ernst Strüngmann Institute (ESI) for Neuroscience in Cooperation with Max Planck Society
Conrado Arturo Bosman: Radboud University
Bruss Lima: Max Planck Institute for Brain Research
Alina Peter: Ernst Strüngmann Institute (ESI) for Neuroscience in Cooperation with Max Planck Society
Irene Onorato: Ernst Strüngmann Institute (ESI) for Neuroscience in Cooperation with Max Planck Society
Johanna Klon-Lipok: Ernst Strüngmann Institute (ESI) for Neuroscience in Cooperation with Max Planck Society
Rasmus Roese: Ernst Strüngmann Institute (ESI) for Neuroscience in Cooperation with Max Planck Society
Sergio Neuenschwander: Max Planck Institute for Brain Research
Pascal Fries: Ernst Strüngmann Institute (ESI) for Neuroscience in Cooperation with Max Planck Society
Martin Vinck: Ernst Strüngmann Institute (ESI) for Neuroscience in Cooperation with Max Planck Society

Nature Communications, 2022, vol. 13, issue 1, 1-18

Abstract: Abstract 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.

Date: 2022
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DOI: 10.1038/s41467-022-29674-x

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