Multiple Midfrontal Thetas Revealed by Source Separation of Simultaneous MEG and EEG.

Theta-band (∼6 Hz) rhythmic activity within and over the medial PFC ("midfrontal theta") has been identified as a distinctive signature of "response conflict," the competition between multiple actions when only one action is goal-relevant. Midfrontal theta is traditionally conceptualized and analyzed under the assumption that it is a unitary signature of conflict that can be uniquely identified at one electrode (typically FCz). Here we recorded simultaneous MEG and EEG (total of 328 sensors) in 9 human subjects (7 female) and applied a feature-guided multivariate source-separation decomposition to determine whether conflict-related midfrontal theta is a unitary or multidimensional feature of the data. For each subject, a generalized eigendecomposition yielded spatial filters (components) that maximized the ratio between theta and broadband activity. Components were retained based on significance thresholding and midfrontal EEG topography. All of the subjects individually exhibited multiple (mean 5.89, SD 2.47) midfrontal components that contributed to sensor-level midfrontal theta power during the task. Component signals were temporally uncorrelated and asynchronous, suggesting that each midfrontal theta component was unique. Our findings call into question the dominant notion that midfrontal theta represents a unitary process. Instead, we suggest that midfrontal theta spans a multidimensional space, indicating multiple origins, but can manifest as a single feature at the sensor level because of signal mixing.SIGNIFICANCE STATEMENT "Midfrontal theta" is a rhythmic electrophysiological signature of the competition between multiple response options. Midfrontal theta is traditionally considered to reflect a single process. However, this assumption could be erroneous because of "mixing" (multiple sources contributing to the activity recorded at a single electrode). We investigated the dimensionality of midfrontal theta by applying advanced multivariate analysis methods to a multimodal MEG/EEG dataset. We identified multiple topographically overlapping neural sources that drove response conflict-related midfrontal theta. Midfrontal theta thus reflects multiple uncorrelated signals that manifest with similar EEG scalp projections. In addition to contributing to the cognitive control literature, we demonstrate both the feasibility and the necessity of signal demixing to understand the narrowband neural dynamics underlying cognitive processes.

Narrowband multivariate source separation for semi-blind discovery of experiment contrasts.

BACKGROUND: Electrophysiological recordings contain mixtures of signals from distinct neural sources, impeding a straightforward interpretation of the sensor-level data. This mixing is particularly detrimental when distinct sources resonate in overlapping frequencies. Fortunately, the mixing is linear and instantaneous. Multivariate source separation methods may therefore successfully separate statistical sources, even with overlapping spatial distributions. NEW METHOD: We demonstrate a feature-guided multivariate source separation method that is tuned to narrowband frequency content as well as binary condition differences. This method - comparison scanning generalized eigendecomposition, csGED - harnesses the covariance structure of multichannel data to find directions (i.e., eigenvectors) that maximally separate two subsets of data. To drive condition specificity and frequency specificity, our data subsets were taken from different task conditions and narrowband-filtered prior to applying GED. RESULTS: To validate the method, we simulated MEG data in two conditions with shared noise characteristics and unique signal. csGED outperformed the best sensor at reconstructing the ground truth signals, even in the presence of large amounts of noise. We next applied csGED to a published empirical MEG dataset on visual perception vs. imagery. csGED identified sources in alpha, beta, and gamma bands, and successfully separated distinct networks in the same frequency band. COMPARISON WITH EXISTING METHOD(S): GED is a flexible feature-guided decomposition method that has previously successfully been applied. Our combined frequency- and condition-tuning is a novel adaptation that extends the power of GED in cognitive electrophysiology. CONCLUSIONS: We demonstrate successful condition-specific source separation by applying csGED to simulated and empirical data.