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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Bibliographic Details
Published in:Nature communications 2022-04, Vol.13 (1), p.2019-18, Article 2019
Main Authors: 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
Format: Article
Language:English
Subjects:
631/378
631/378/116
631/378/2613
631/378/3917
Action Potentials - physiology
Amplitudes
Animals
Circuits
Correlation
Electrophysiological recording
Gamma Rhythm - physiology
Harmonic oscillators
Humanities and Social Sciences
Macaca
multidisciplinary
Neurogenesis
Neurons
Neurons - physiology
Noise
Oscillations
Power spectra
Rhythms
Science
Science (multidisciplinary)
Wakefulness
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Summary: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. It remains unclear how to best model local field potential gamma oscillations. Here, the authors show that gamma dynamics are well-captured by a damped harmonic oscillator model.
ISSN:2041-1723
2041-1723
DOI:10.1038/s41467-022-29674-x