Adaptive spike-artifact removal from local field potentials uncovers prominent beta and gamma band neuronal synchronization

Kianoush Banaie Boroujeni; Paul Tiesinga; Thilo Womelsdorf

doi:10.1016/j.jneumeth.2019.108485

Adaptive spike-artifact removal from local field potentials uncovers prominent beta and gamma band neuronal synchronization

J Neurosci Methods. 2020 Jan 15:330:108485. doi: 10.1016/j.jneumeth.2019.108485. Epub 2019 Nov 6.

Authors

Kianoush Banaie Boroujeni¹, Paul Tiesinga², Thilo Womelsdorf³

Affiliations

¹ Department of Psychology, Vanderbilt University, Nashville, TN 37240, United States.
² Donders Institute for Brain, Cognition and Behaviour Radboud University Nijmegen, 6525 EN Nijmegen, Netherlands.
³ Department of Psychology, Vanderbilt University, Nashville, TN 37240, United States; Department of Biology, Centre for Vision Research, York University, 4700 Keele Street, Toronto, Ontario M6J 1P3, Canada. Electronic address: thilo.womelsdorf@vanderbilt.edu.

Abstract

Background: Many neurons synchronize their action potentials to the phase of local field potential (LFP) fluctuations in one or more frequency bands. Analyzing this spike-to-LFP synchronization is challenging, however, when neural spikes and LFP are generated in the same local circuit, because the spike's action potential waveform leak into the LFP and distort phase synchrony estimates. Existing approaches to address this spike bleed-through artifact relied on removing the average action potential waveforms of neurons, but this leaves artifacts in the LFP and distorts synchrony estimates.

New method: We describe a spike-removal method that surpasses these limitations by decomposing individual action potentials into their frequency components before their removal from the LFP. The adaptively estimated frequency components allow for variable spread, strength and temporal variation of the spike artifact.

Results: This adaptive approach effectively removes spike bleed-through artifacts in synthetic data with known ground truth, and in single neuron and LFP recordings in nonhuman primate striatum. For a large population of neurons with both narrow and broad action potential waveforms, the use of adaptive artifact removal uncovered 20-35 Hz beta and 35-45 Hz gamma band spike-LFP synchronization that would have remained contaminated otherwise.

Comparison with existing methods: We demonstrate that adaptive spike-artifact removal cleans LFP data that remained contaminated when applying existing Bayesian and non-Bayesian methods of average spike-artifact removal.

Conclusions: Applying adaptive spike-removal from field potentials allows to estimate the phase at which neurons synchronize and the consistency of their phase-locked firing for both beta and low gamma frequencies. These metrics may prove essential to understand cell-to-circuit neuronal interactions in multiple brain systems.

Keywords: Local field potential; Spike-related transient; Synchronization; Time frequency analysis.

Publication types

Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't

MeSH terms

Action Potentials / physiology*
Animals
Artifacts
Beta Rhythm / physiology*
Corpus Striatum / physiology*
Electroencephalography Phase Synchronization / physiology*
Gamma Rhythm / physiology*
Macaca mulatta
Male
Neurons / physiology*
Signal Processing, Computer-Assisted*

Abstract

Publication types

MeSH terms

Grants and funding