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

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  • 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
    International Max Planck Research School for Neural Circuits)

  • Jarrod Robert Dowdall

    (Ernst Strüngmann Institute (ESI) for Neuroscience in Cooperation with Max Planck Society
    International Max Planck Research School for Neural Circuits)

  • Marieke Louise Schölvinck

    (Ernst Strüngmann Institute (ESI) for Neuroscience in Cooperation with Max Planck Society)

  • Conrado Arturo Bosman

    (Radboud University
    Faculty of Science, University of Amsterdam)

  • Bruss Lima

    (Max Planck Institute for Brain Research
    Federal University of Rio de Janeiro)

  • Alina Peter

    (Ernst Strüngmann Institute (ESI) for Neuroscience in Cooperation with Max Planck Society
    International Max Planck Research School for Neural Circuits)

  • Irene Onorato

    (Ernst Strüngmann Institute (ESI) for Neuroscience in Cooperation with Max Planck Society
    International Max Planck Research School for Neural Circuits)

  • Johanna Klon-Lipok

    (Ernst Strüngmann Institute (ESI) for Neuroscience in Cooperation with Max Planck Society
    Max Planck Institute for Brain Research)

  • Rasmus Roese

    (Ernst Strüngmann Institute (ESI) for Neuroscience in Cooperation with Max Planck Society)

  • Sergio Neuenschwander

    (Max Planck Institute for Brain Research
    Federal University of Rio Grande do Norte)

  • Pascal Fries

    (Ernst Strüngmann Institute (ESI) for Neuroscience in Cooperation with Max Planck Society
    Radboud University)

  • Martin Vinck

    (Ernst Strüngmann Institute (ESI) for Neuroscience in Cooperation with Max Planck Society
    Radboud University)

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.

Suggested Citation

  • Georgios Spyropoulos & Matteo Saponati & Jarrod Robert Dowdall & Marieke Louise Schölvinck & Conrado Arturo Bosman & Bruss Lima & Alina Peter & Irene Onorato & Johanna Klon-Lipok & Rasmus Roese & Serg, 2022. "Spontaneous variability in gamma dynamics described by a damped harmonic oscillator driven by noise," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-29674-x
    DOI: 10.1038/s41467-022-29674-x
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    References listed on IDEAS

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    1. Lyle Muller & Alexandre Reynaud & Frédéric Chavane & Alain Destexhe, 2014. "The stimulus-evoked population response in visual cortex of awake monkey is a propagating wave," Nature Communications, Nature, vol. 5(1), pages 1-14, May.
    2. Zachary W. Davis & Lyle Muller & Julio Martinez-Trujillo & Terrence Sejnowski & John H. Reynolds, 2020. "Spontaneous travelling cortical waves gate perception in behaving primates," Nature, Nature, vol. 587(7834), pages 432-436, November.
    3. Michael Wehr & Anthony M. Zador, 2003. "Balanced inhibition underlies tuning and sharpens spike timing in auditory cortex," Nature, Nature, vol. 426(6965), pages 442-446, November.
    4. Thilo Womelsdorf & Pascal Fries & Partha P. Mitra & Robert Desimone, 2006. "Gamma-band synchronization in visual cortex predicts speed of change detection," Nature, Nature, vol. 439(7077), pages 733-736, February.
    5. Jean-Sébastien Jouhanneau & Jens Kremkow & James F. A. Poulet, 2018. "Single synaptic inputs drive high-precision action potentials in parvalbumin expressing GABA-ergic cortical neurons in vivo," Nature Communications, Nature, vol. 9(1), pages 1-11, December.
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