Alpha (8-12 Hz) frequency band oscillations are among the most informative features in electroencephalographic (EEG) assessment of patients with disorders of consciousness (DoC). Because interareal alpha synchrony is thought to facilitate long-range communication in healthy brains, coherence measures of resting-state alpha oscillations may provide insights into a patients capacity for higher-order cognition beyond channel-wise estimates of alpha power. In multi-channel EEG, global coherence methods may be used to augment standard spectral analysis methods by both estimating the strength and identifying the structure of coherent oscillatory networks. We performed global coherence analysis in 95 separate clinical EEG recordings (28 healthy controls and 33 patients with acute or chronic DoC, 25 of whom returned for follow-up) collected between two academic medical centers. We found that posterior alpha coherence is associated with recovery of higher-level cognition. We developed a measure of network organization, based on the distance between eigenvectors of the alpha cross-spectral matrix, that detects recovery of posterior alpha networks. In patients who have emerged from a minimally conscious state, we showed that coherence-based alpha networks are reconfigured prior to restoration of alpha power to resemble those seen in healthy controls. This alpha network measure performs well in classifying recovery from DoC (AUC = 0.78) compared to common representations of functional connectivity using the weighted phase lag index (AUC = 0.50 - 0.57). Lastly, we observed that activity within these alpha networks is suppressed during positive responses to task-based EEG command-following paradigms, supporting the potential utility of this biomarker to detect covert cognition. Our findings suggest that restored alpha networks may represent a sensitive early signature of cognitive recovery in patients with DoC. Therefore, network detection methods may augment the utility of EEG assessments for DoC.

The authors declare no competing interests. The views expressed are purely those of the authors and may not in any circumstances be regarded as stating an official position of the European Research Council Executive Agency (ERCEA) and the European Commission.

This study was supported by the NIH T32 Neurobiological Engineering Training Program (T32EB019940, DWZ), NIH Directors Office (DP2HD101400, BLE), James S. McDonnell Foundation (BLE), Tiny Blue Dot Foundation (BLE), and Chen Institute MGH Research Scholars Award (BLE).

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The details of the IRB/oversight body that provided approval or exemption for the research described are given below:

IRBs of Massachusetts General Hospital and Weill Cornell Medical Center gave ethical approval for this work.

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The cross-spectral resampling, global coherence, and subspace analytical techniques used in this study can be found in the gcoh+: Global Coherence Toolbox Plus GitHub repository (https://github.com/dvwz/gcoh_plus). Data are available upon request from the corresponding author.

https://github.com/dvwz/gcoh_plus