Spatial neuronal synchronization and the waveform of oscillations: Implications for EEG and MEG

Neuronal oscillations are ubiquitous in the human brain and are implicated in virtually all brain functions. Although they can be described by a prominent peak in the power spectrum, their waveform is not necessarily sinusoidal and shows rather complex morphology. Both frequency and temporal descrip...

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Published inPLoS computational biology Vol. 15; no. 5; p. e1007055
Main Authors Schaworonkow, Natalie, Nikulin, Vadim V
Format Journal Article
LanguageEnglish
Published United States Public Library of Science 01.05.2019
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Abstract Neuronal oscillations are ubiquitous in the human brain and are implicated in virtually all brain functions. Although they can be described by a prominent peak in the power spectrum, their waveform is not necessarily sinusoidal and shows rather complex morphology. Both frequency and temporal descriptions of such non-sinusoidal neuronal oscillations can be utilized. However, in non-invasive EEG/MEG recordings the waveform of oscillations often takes a sinusoidal shape which in turn leads to a rather oversimplified view on oscillatory processes. In this study, we show in simulations how spatial synchronization can mask non-sinusoidal features of the underlying rhythmic neuronal processes. Consequently, the degree of non-sinusoidality can serve as a measure of spatial synchronization. To confirm this empirically, we show that a mixture of EEG components is indeed associated with more sinusoidal oscillations compared to the waveform of oscillations in each constituent component. Using simulations, we also show that the spatial mixing of the non-sinusoidal neuronal signals strongly affects the amplitude ratio of the spectral harmonics constituting the waveform. Finally, our simulations show how spatial mixing can affect the strength and even the direction of the amplitude coupling between constituent neuronal harmonics at different frequencies. Validating these simulations, we also demonstrate these effects in real EEG recordings. Our findings have far reaching implications for the neurophysiological interpretation of spectral profiles, cross-frequency interactions, as well as for the unequivocal determination of oscillatory phase.
AbstractList Neuronal oscillations are ubiquitous in the human brain and are implicated in virtually all brain functions. Although they can be described by a prominent peak in the power spectrum, their waveform is not necessarily sinusoidal and shows rather complex morphology. Both frequency and temporal descriptions of such non-sinusoidal neuronal oscillations can be utilized. However, in non-invasive EEG/MEG recordings the waveform of oscillations often takes a sinusoidal shape which in turn leads to a rather oversimplified view on oscillatory processes. In this study, we show in simulations how spatial synchronization can mask non-sinusoidal features of the underlying rhythmic neuronal processes. Consequently, the degree of non-sinusoidality can serve as a measure of spatial synchronization. To confirm this empirically, we show that a mixture of EEG components is indeed associated with more sinusoidal oscillations compared to the waveform of oscillations in each constituent component. Using simulations, we also show that the spatial mixing of the non-sinusoidal neuronal signals strongly affects the amplitude ratio of the spectral harmonics constituting the waveform. Finally, our simulations show how spatial mixing can affect the strength and even the direction of the amplitude coupling between constituent neuronal harmonics at different frequencies. Validating these simulations, we also demonstrate these effects in real EEG recordings. Our findings have far reaching implications for the neurophysiological interpretation of spectral profiles, cross-frequency interactions, as well as for the unequivocal determination of oscillatory phase. The electrical activity in the human brain demonstrates oscillations of intricate complexity. Interestingly, such complex waveforms are primarily visible in invasive recordings but not so much when neuronal activity is recorded with non-invasive methods such as electroencephalography. Yet a specific waveform is informative about the postsynaptic processes which are at the core of our understanding of cortical excitability and information transfer in neuronal networks. In our study, we show with simulations and real EEG data, how temporal delays between different cortical sources can contribute to a more sinusoidal or non-sinusoidal shape of neuronal oscillations. We illustrate how, depending on the temporal delays, low- and high-frequency components of oscillations can be enhanced or attenuated to a different degree thus affecting the shape of oscillations and corresponding spectra which are often associated with specific functional consequences. We further show how this phenomenon can challenge our understanding of the link between neuronal oscillations and motor function, cognition and perception.
Neuronal oscillations are ubiquitous in the human brain and are implicated in virtually all brain functions. Although they can be described by a prominent peak in the power spectrum, their waveform is not necessarily sinusoidal and shows rather complex morphology. Both frequency and temporal descriptions of such non-sinusoidal neuronal oscillations can be utilized. However, in non-invasive EEG/MEG recordings the waveform of oscillations often takes a sinusoidal shape which in turn leads to a rather oversimplified view on oscillatory processes. In this study, we show in simulations how spatial synchronization can mask non-sinusoidal features of the underlying rhythmic neuronal processes. Consequently, the degree of non-sinusoidality can serve as a measure of spatial synchronization. To confirm this empirically, we show that a mixture of EEG components is indeed associated with more sinusoidal oscillations compared to the waveform of oscillations in each constituent component. Using simulations, we also show that the spatial mixing of the non-sinusoidal neuronal signals strongly affects the amplitude ratio of the spectral harmonics constituting the waveform. Finally, our simulations show how spatial mixing can affect the strength and even the direction of the amplitude coupling between constituent neuronal harmonics at different frequencies. Validating these simulations, we also demonstrate these effects in real EEG recordings. Our findings have far reaching implications for the neurophysiological interpretation of spectral profiles, cross-frequency interactions, as well as for the unequivocal determination of oscillatory phase.
Audience Academic
Author Schaworonkow, Natalie
Nikulin, Vadim V
AuthorAffiliation 6 Bernstein Center for Computational Neuroscience Berlin, Berlin, Germany
Radboud Universiteit Nijmegen, NETHERLANDS
4 Centre for Cognition and Decision Making, National Research University Higher School of Economics, Moscow, Russian Federation
3 Department of Neurology, Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig, Germany
5 Neurophysics Group, Department of Neurology, Charité-University Medicine Berlin – Campus Benjamin Franklin, Berlin, Germany
1 Frankfurt Institute for Advanced Studies, Johann Wolfgang Goethe University, Frankfurt am Main, Germany
2 Department of Neurology & Stroke, and Hertie Institute for Clinical Brain Research, University of Tübingen, Tübingen, Germany
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/31086368$$D View this record in MEDLINE/PubMed
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2019 Schaworonkow, Nikulin. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
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Snippet Neuronal oscillations are ubiquitous in the human brain and are implicated in virtually all brain functions. Although they can be described by a prominent peak...
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StartPage e1007055
SubjectTerms Adult
Aged
Amplitudes
Biology and Life Sciences
Brain
Brain - physiology
Brain Mapping - statistics & numerical data
Brain research
Brain Waves - physiology
Computational Biology
Computer Simulation
Constituents
EEG
Electrodes
Electroencephalography
Electroencephalography - statistics & numerical data
Electroencephalography Phase Synchronization
Engineering and Technology
Female
Harmonics
Humans
Magnetoencephalography
Magnetoencephalography - statistics & numerical data
Male
Medicine and Health Sciences
Methods
Middle Aged
Models, Neurological
Morphology
Neural oscillations
Neurology
Neurons
Neurons - physiology
Neurophysiology
Neurosciences
Observations
Oscillations
Physiological aspects
Research and Analysis Methods
Rhythms
Signal processing
Signal Processing, Computer-Assisted
Signal-To-Noise Ratio
Simulation
Synchronism
Synchronization
Young Adult
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Title Spatial neuronal synchronization and the waveform of oscillations: Implications for EEG and MEG
URI https://www.ncbi.nlm.nih.gov/pubmed/31086368
https://www.proquest.com/docview/2250647365
https://search.proquest.com/docview/2232025002
https://pubmed.ncbi.nlm.nih.gov/PMC6534335
https://doaj.org/article/9b4deb03eb73499fbda059683e5e4322
http://dx.doi.org/10.1371/journal.pcbi.1007055
Volume 15
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