Detecting Spontaneous Neural Oscillation Events in Primate Auditory Cortex

Samuel A. Neymotin, Idan Tal, Annamaria Barczak, Monica N. O’connell, Tammy McGinnis, Noah Markowitz, Elizabeth Espinal, Erica Griffith, Haroon Anwar, Salvador Dura-Bernal, Charles E. Schroeder, William W. Lytton, Stephanie R. Jones, Stephan Bickel, Peter Lakatos

Research output: Contribution to journalArticlepeer-review

18 Scopus citations

Abstract

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,lowγ, γ, andhighγ. 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.

Original languageEnglish
Article numberENEURO.0281-21.2022
JournaleNeuro
Volume9
Issue number4
DOIs
StatePublished - 1 Jul 2022
Externally publishedYes

Bibliographical note

Publisher Copyright:
© 2022 Neymotin et al.

Funding

This work was supported by the National Institutes of Health (NIH) Grant R01DC012947 (to S.A.N., C.E.S., and P.L.); the Army Research Office Grant W911NF-19-1-0402 (to S.A.N.); the Army Research Office Undergraduate Research Apprenticeship Program (URAP) Supplement (S.A.N.); the New York State Empire Clinical Research Investigator Program (ECRIP) Fellowship (S.B.); Army Research Lab Cooperative Agreement W911NF-22-2-0139 (to S.A.N.); NIH Grants P50 MH109429 (to P.L. and C.E.S.), R01MH106174 (to S.R.J.), U24EB028998 (to S.-D.B.), and U01EB017695 (to W.W.L.); the New York State Spinal Cord Injury Research Board Grant DOH01-C32250GG-3450000 (to S.D.-B.); the National Science Foundation (NSF) Grant 1904444 (to S.D.-B.); the NIH Grant R01MH111439 (to C.E.S.); and a The James S. McDonnell Foundation grant (C.E.S.). This research is dedicated to the memory of Peter Lakatos (5/30/21). *S.A.N. and I.T. contributed equally to this work. This work was supported by the National Institutes of Health (NIH) Grant R01DC012947 (to S.A.N., C.E.S., and P.L.); the Army Research Office Grant W911NF-19-1-0402 (to S.A.N.); the Army Research Office Undergraduate Research Apprenticeship Program (URAP) Supplement (S.A.N.); the New York State Empire Clinical Research Investigator Program (ECRIP) Fellowship (S.B.); Army Research Lab Cooperative Agreement W911NF-22-2-0139 (to S.A.N.); NIH Grants P50 MH109429 (to P.L. and C.E.S.), R01MH106174 (to S.R.J.), U24EB028998 (to S.-D.B.), and U01EB017695 (to W.W.L.); the New York State Spinal Cord Injury Research Board Grant DOH01-C32250GG-3450000 (to S.D.-B.); the National Science Foundation (NSF) Grant 1904444 (to S.D.-B.); the NIH Grant R01MH111439 (to C.E.S.); and a The James S. McDonnell Foundation grant (C.E.S.).This research is dedicated to the memory of Peter Lakatos (5/30/21).

FundersFunder number
Army Research Lab Cooperative AgreementU01EB017695, R01MH106174, P50 MH109429, W911NF-22-2-0139, U24EB028998
New York State Spinal Cord Injury Research BoardDOH01-C32250GG-3450000
National Science FoundationR01MH111439, 1904444
National Institutes of HealthR01DC012947
Army Research OfficeW911NF-19-1-0402
James S. McDonnell Foundation5/30/21

    Keywords

    • auditory cortex
    • current-source density
    • electrophysiology
    • local field potential
    • oscillations
    • rhythms

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