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      The shaky ground truth of real-time phase estimation

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          Abstract

          Instantaneous phase of brain oscillations in electroencephalography (EEG) is a measure of brain state that is relevant to neuronal processing and modulates evoked responses. However, determining phase at the time of a stimulus with standard signal processing methods is not possible due to the stimulus artifact masking the future part of the signal. Here, we quantify the degree to which signal-to-noise ratio and instantaneous amplitude of the signal affect the variance of phase estimation error and the precision with which “ground truth” phase is even defined, using both the variance of equivalent estimators and realistic simulated EEG data with known synthetic phase. Necessary experimental conditions are specified in which pre-stimulus phase estimation is meaningfully possible based on instantaneous amplitude and signal-to-noise ratio of the oscillation of interest. An open source toolbox is made available for causal (using pre-stimulus signal only) phase estimation along with a EEG dataset consisting of recordings from 140 participants and a best practices workflow for algorithm optimization and benchmarking. As an illustration, post-hoc sorting of open-loop transcranial magnetic stimulation (TMS) trials according to pre-stimulus sensorimotor μ-rhythm phase is performed to demonstrate modulation of corticospinal excitability, as indexed by the amplitude of motor evoked potentials.

          Highlights

          • The accuracy of causal and non-causal phase estimation methods is quantified using real and synthetic EEG data.

          • Sensorimotor rhythm EEG data from 140 participants is made available for algorithm calibration and benchmarking.

          • A causal phase estimation algorithm using autoregressive forward-prediction is made available as an open source toolbox.

          • Phase estimability is decreased for data with low signal-to-noise ratio is and during periods of low oscillatory amplitude.

          • Best practices for ​ post-hoc ​phase sorting are proposed and illustrated using EEG modulation of motor evoked potentials.

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          Most cited references30

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          α-Oscillations in the monkey sensorimotor network influence discrimination performance by rhythmical inhibition of neuronal spiking.

          Extensive work in humans using magneto- and electroencephalography strongly suggests that decreased oscillatory α-activity (8-14 Hz) facilitates processing in a given region, whereas increased α-activity serves to actively suppress irrelevant or interfering processing. However, little work has been done to understand how α-activity is linked to neuronal firing. Here, we simultaneously recorded local field potentials and spikes from somatosensory, premotor, and motor regions while a trained monkey performed a vibrotactile discrimination task. In the local field potentials we observed strong activity in the α-band, which decreased in the sensorimotor regions during the discrimination task. This α-power decrease predicted better discrimination performance. Furthermore, the α-oscillations demonstrated a rhythmic relation with the spiking, such that firing was highest at the trough of the α-cycle. Firing rates increased with a decrease in α-power. These findings suggest that α-oscillations exercise a strong inhibitory influence on both spike timing and firing rate. Thus, the pulsed inhibition by α-oscillations plays an important functional role in the extended sensorimotor system.
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            An on-line transformation of EEG scalp potentials into orthogonal source derivations.

            Bo Hjorth (1975)
            A new type of EEG derivation has been investigated. This derivation, constituting a practical implementation of the Laplace operator, detects source activity as it appears at the surface level of the scalp. It is realized in the 10-20 system of electrode placement basically as an analogue superposition of four bipolar derivations, forming a star-like configuration around each electrode. Visual estimation of the topographical origins of a pattern, is thus replaced by a more efficient on-line process, which derives the source activity at the position of each individual electrode. Practical correlation tests have shown that the separation of adjacent derivations is improved by a factor of between two and four, compared to the corresponding bipolar and common reference derivations. Any feature of local origin will therefore have a correspondingly increased signal-to-noise ratio prior to the stage of visual or automatic interpretation. As a consequence of the partition of the scalp field into 19 source zreas, instead of utilizing an arbitrary number of potential differences, one fixed montage with 19 recorder channels is sufficient to present the total surface activity, within the limits of resolution of the electrode system.
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              Real-time EEG-defined excitability states determine efficacy of TMS-induced plasticity in human motor cortex.

              Rapidly changing excitability states in an oscillating neuronal network can explain response variability to external stimulation, but if repetitive stimulation of always the same high- or low-excitability state results in long-term plasticity of opposite direction has never been explored in vivo.
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                Author and article information

                Contributors
                Journal
                Neuroimage
                Neuroimage
                Neuroimage
                Academic Press
                1053-8119
                1095-9572
                01 July 2020
                01 July 2020
                : 214
                : 116761
                Affiliations
                [a ]Department of Neurology & Stroke, And Hertie Institute for Clinical Brain Research, University of Tübingen, Tübingen, Germany
                [b ]Department of Neuroscience and Biomedical Engineering, Aalto University School of Science, Espoo, Finland
                Author notes
                []Corresponding author. ulf.ziemann@ 123456uni-tuebingen.de
                Article
                S1053-8119(20)30248-2 116761
                10.1016/j.neuroimage.2020.116761
                7284312
                32198050
                b95a0290-c0ed-43fa-9a69-a2f190e009d1
                © 2020 The Authors

                This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

                History
                : 31 December 2019
                : 9 March 2020
                : 16 March 2020
                Categories
                Article

                Neurosciences
                eeg,oscillation,phase,real-time,tms,eeg–tms,brain state,estimator
                Neurosciences
                eeg, oscillation, phase, real-time, tms, eeg–tms, brain state, estimator

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