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Detecting Spontaneous Neural Oscillation Events in Primate Auditory Cortex

Electrophysiological oscillations in the brain have been shown to occur as multicycle events, with onset and offset dependent on behavioral and cognitive state. To provide a baseline for state-related and task-related events, we quantified oscillation features in resting-state recordings. We develop...

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Autores principales: Neymotin, Samuel A., Tal, Idan, Barczak, Annamaria, O’Connell, Monica N., McGinnis, Tammy, Markowitz, Noah, Espinal, Elizabeth, Griffith, Erica, Anwar, Haroon, Dura-Bernal, Salvador, Schroeder, Charles E., Lytton, William W., Jones, Stephanie R., Bickel, Stephan, Lakatos, Peter
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Society for Neuroscience 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9395248/
https://www.ncbi.nlm.nih.gov/pubmed/35906065
http://dx.doi.org/10.1523/ENEURO.0281-21.2022
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author Neymotin, Samuel A.
Tal, Idan
Barczak, Annamaria
O’Connell, Monica N.
McGinnis, Tammy
Markowitz, Noah
Espinal, Elizabeth
Griffith, Erica
Anwar, Haroon
Dura-Bernal, Salvador
Schroeder, Charles E.
Lytton, William W.
Jones, Stephanie R.
Bickel, Stephan
Lakatos, Peter
author_facet Neymotin, Samuel A.
Tal, Idan
Barczak, Annamaria
O’Connell, Monica N.
McGinnis, Tammy
Markowitz, Noah
Espinal, Elizabeth
Griffith, Erica
Anwar, Haroon
Dura-Bernal, Salvador
Schroeder, Charles E.
Lytton, William W.
Jones, Stephanie R.
Bickel, Stephan
Lakatos, Peter
author_sort Neymotin, Samuel A.
collection PubMed
description Electrophysiological oscillations in the brain have been shown to occur as multicycle events, with onset and offset dependent on behavioral and cognitive state. To provide a baseline for state-related and task-related events, we quantified oscillation features in resting-state recordings. We developed an open-source wavelet-based tool to detect and characterize such oscillation events (OEvents) and exemplify the use of this tool in both simulations and two invasively-recorded electrophysiology datasets: one from human, and one from nonhuman primate (NHP) auditory system. After removing incidentally occurring event-related potentials (ERPs), we used OEvents to quantify oscillation features. We identified ∼2 million oscillation events, classified within traditional frequency bands: δ, θ, α, β, low γ, γ, and high γ. Oscillation events of 1–44 cycles could be identified in at least one frequency band 90% of the time in human and NHP recordings. Individual oscillation events were characterized by nonconstant frequency and amplitude. This result necessarily contrasts with prior studies which assumed frequency constancy, but is consistent with evidence from event-associated oscillations. We measured oscillation event duration, frequency span, and waveform shape. Oscillations tended to exhibit multiple cycles per event, verifiable by comparing filtered to unfiltered waveforms. In addition to the clear intraevent rhythmicity, there was also evidence of interevent rhythmicity within bands, demonstrated by finding that coefficient of variation of interval distributions and Fano factor (FF) measures differed significantly from a Poisson distribution assumption. Overall, our study provides an easy-to-use tool to study oscillation events at the single-trial level or in ongoing recordings, and demonstrates that rhythmic, multicycle oscillation events dominate auditory cortical dynamics.
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spelling pubmed-93952482022-08-23 Detecting Spontaneous Neural Oscillation Events in Primate Auditory Cortex Neymotin, Samuel A. Tal, Idan Barczak, Annamaria O’Connell, Monica N. McGinnis, Tammy Markowitz, Noah Espinal, Elizabeth Griffith, Erica Anwar, Haroon Dura-Bernal, Salvador Schroeder, Charles E. Lytton, William W. Jones, Stephanie R. Bickel, Stephan Lakatos, Peter eNeuro Research Article: New Research Electrophysiological oscillations in the brain have been shown to occur as multicycle events, with onset and offset dependent on behavioral and cognitive state. To provide a baseline for state-related and task-related events, we quantified oscillation features in resting-state recordings. We developed an open-source wavelet-based tool to detect and characterize such oscillation events (OEvents) and exemplify the use of this tool in both simulations and two invasively-recorded electrophysiology datasets: one from human, and one from nonhuman primate (NHP) auditory system. After removing incidentally occurring event-related potentials (ERPs), we used OEvents to quantify oscillation features. We identified ∼2 million oscillation events, classified within traditional frequency bands: δ, θ, α, β, low γ, γ, and high γ. Oscillation events of 1–44 cycles could be identified in at least one frequency band 90% of the time in human and NHP recordings. Individual oscillation events were characterized by nonconstant frequency and amplitude. This result necessarily contrasts with prior studies which assumed frequency constancy, but is consistent with evidence from event-associated oscillations. We measured oscillation event duration, frequency span, and waveform shape. Oscillations tended to exhibit multiple cycles per event, verifiable by comparing filtered to unfiltered waveforms. In addition to the clear intraevent rhythmicity, there was also evidence of interevent rhythmicity within bands, demonstrated by finding that coefficient of variation of interval distributions and Fano factor (FF) measures differed significantly from a Poisson distribution assumption. Overall, our study provides an easy-to-use tool to study oscillation events at the single-trial level or in ongoing recordings, and demonstrates that rhythmic, multicycle oscillation events dominate auditory cortical dynamics. Society for Neuroscience 2022-08-18 /pmc/articles/PMC9395248/ /pubmed/35906065 http://dx.doi.org/10.1523/ENEURO.0281-21.2022 Text en Copyright © 2022 Neymotin et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.
spellingShingle Research Article: New Research
Neymotin, Samuel A.
Tal, Idan
Barczak, Annamaria
O’Connell, Monica N.
McGinnis, Tammy
Markowitz, Noah
Espinal, Elizabeth
Griffith, Erica
Anwar, Haroon
Dura-Bernal, Salvador
Schroeder, Charles E.
Lytton, William W.
Jones, Stephanie R.
Bickel, Stephan
Lakatos, Peter
Detecting Spontaneous Neural Oscillation Events in Primate Auditory Cortex
title Detecting Spontaneous Neural Oscillation Events in Primate Auditory Cortex
title_full Detecting Spontaneous Neural Oscillation Events in Primate Auditory Cortex
title_fullStr Detecting Spontaneous Neural Oscillation Events in Primate Auditory Cortex
title_full_unstemmed Detecting Spontaneous Neural Oscillation Events in Primate Auditory Cortex
title_short Detecting Spontaneous Neural Oscillation Events in Primate Auditory Cortex
title_sort detecting spontaneous neural oscillation events in primate auditory cortex
topic Research Article: New Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9395248/
https://www.ncbi.nlm.nih.gov/pubmed/35906065
http://dx.doi.org/10.1523/ENEURO.0281-21.2022
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