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Beyond alpha power: EEG spatial and spectral gradients robustly stratify disorders of consciousness.

ABSTRACT: Neurophysiological markers can overcome the limitations of behavioural assessments of Disorders of Consciousness (DoC). EEG alpha power emerged as a promising marker for DoC, although long-standing literature reported alpha power being sustained during anesthetic-induced unconsciousness, and reduced during dreaming and hallucinations. We hypothesized that EEG power suppression caused by severe anoxia could explain this conflict. Accordingly, we split DoC patients (n = 87) in postanoxic and non-postanoxic cohorts. Alpha power was suppressed only in severe postanoxia but failed to discriminate un/consciousness in other aetiologies. Furthermore, it did not generalize to an independent reference dataset (n = 65) of neurotypical, neurological, and anesthesia conditions. We then investigated EEG spatio-spectral gradients, reflecting anteriorization and slowing, as alternative markers. In non-postanoxic DoC, these features, combined in a bivariate model, reliably stratified patients and indexed consciousness, even in unresponsive patients identified as conscious by an independent neural marker (the Perturbational Complexity Index). Crucially, this model optimally generalized to the reference dataset. Overall, alpha power does not index consciousness; rather, its suppression entails diffuse cortical damage, in postanoxic patients. As an alternative, EEG spatio-spectral gradients, reflecting distinct pathophysiological mechanisms, jointly provide a robust, parsimonious, and generalizable marker of consciousness, whose clinical application may guide rehabilitation efforts.

SUBMITTER: Colombo MA

PROVIDER: S-EPMC10233271 | biostudies-literature | 2023 May

REPOSITORIES: biostudies-literature

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Beyond alpha power: EEG spatial and spectral gradients robustly stratify disorders of consciousness.

Colombo Michele Angelo MA Comanducci Angela A Casarotto Silvia S Derchi Chiara-Camilla CC Annen Jitka J Viganò Alessandro A Mazza Alice A Trimarchi Pietro Davide PD Boly Melanie M Fecchio Matteo M Bodart Olivier O Navarro Jorge J Laureys Steven S Gosseries Olivia O Massimini Marcello M Sarasso Simone S Rosanova Mario M

Cerebral cortex (New York, N.Y. : 1991) 20230501 11

Neurophysiological markers can overcome the limitations of behavioural assessments of Disorders of Consciousness (DoC). EEG alpha power emerged as a promising marker for DoC, although long-standing literature reported alpha power being sustained during anesthetic-induced unconsciousness, and reduced during dreaming and hallucinations. We hypothesized that EEG power suppression caused by severe anoxia could explain this conflict. Accordingly, we split DoC patients (n = 87) in postanoxic and non-p ...[more]

PMID: 36977648

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Project description:IntroductionElectroencephalographic (EEG) data quality is severely compromised when recorded inside the magnetic resonance (MR) environment. Here we characterized the impact of the ballistocardiographic (BCG) artifact on resting-state EEG spectral properties and compared the effectiveness of seven common BCG correction methods to preserve EEG spectral features. We also assessed if these methods retained posterior alpha power reactivity to an eyes closure-opening (EC-EO) task and compared the results from EEG-informed fMRI analysis using different BCG correction approaches.MethodElectroencephalographic data from 20 healthy young adults were recorded outside the MR environment and during simultaneous fMRI acquisition. The gradient artifact was effectively removed from EEG-fMRI acquisitions using Average Artifact Subtraction (AAS). The BCG artifact was corrected with seven methods: AAS, Optimal Basis Set (OBS), Independent Component Analysis (ICA), OBS followed by ICA, AAS followed by ICA, PROJIC-AAS and PROJIC-OBS. EEG signal preservation was assessed by comparing the spectral power of traditional frequency bands from the corrected rs-EEG-fMRI data with the data recorded outside the scanner. We then assessed the preservation of posterior alpha functional reactivity by computing the ratio between the EC and EO conditions during the EC-EO task. EEG-informed fMRI analysis of the EC-EO task was performed using alpha power-derived BOLD signal predictors obtained from the EEG signals corrected with different methods.ResultsThe BCG artifact caused significant distortions (increased absolute power, altered relative power) across all frequency bands. Artifact residuals/signal losses were present after applying all correction methods. The EEG reactivity to the EC-EO task was better preserved with ICA-based correction approaches, particularly when using ICA feature extraction to isolate alpha power fluctuations, which allowed to accurately predict hemodynamic signal fluctuations during the EEG-informed fMRI analysis.DiscussionCurrent software solutions for the BCG artifact problem offer limited efficiency to preserve the EEG spectral power properties using this particular EEG setup. The state-of-the-art approaches tested here can be further refined and should be combined with hardware implementations to better preserve EEG signal properties during simultaneous EEG-fMRI. Existing and novel BCG artifact correction methods should be validated by evaluating signal preservation of both ERPs and spontaneous EEG spectral power.

Project description:Background/objectiveBehavioral examinations may fail to detect language function in patients with severe traumatic brain injury (TBI) due to confounds such as having an endotracheal tube. We investigated whether resting and stimulus-evoked electroencephalography (EEG) methods detect the presence of language function in patients with severe TBI.MethodsFour EEG measures were assessed: (1) resting background (applying Forgacs' criteria), (2) reactivity to speech, (3) background and reactivity (applying Synek's criteria); and (4) an automated support vector machine (classifier for speech versus rest). Cohen's kappa measured agreement between the four EEG measures and evidence of language function on a behavioral coma recovery scale-revised (CRS-R) and composite (CRS-R or functional MRI) reference standard. Sensitivity and specificity of each EEG measure were calculated against the reference standards.ResultsWe enrolled 17 adult patients with severe TBI (mean ± SD age 27.0 ± 7.0 years; median [range] 11.5 [2-1173] days post-injury) and 16 healthy subjects (age 28.5 ± 7.8 years). The classifier, followed by Forgacs' criteria for resting background, demonstrated the highest agreement with the behavioral reference standard. Only Synek's criteria for background and reactivity showed significant agreement with the composite reference standard. The classifier and resting background showed balanced sensitivity and specificity for behavioral (sensitivity = 84.6% and 80.8%; specificity = 57.1% for both) and composite reference standards (sensitivity = 79.3% and 75.9%, specificity = 50% for both).ConclusionsMethods applying an automated classifier, resting background, or resting background with reactivity may identify severe TBI patients with preserved language function. Automated classifier methods may enable unbiased and efficient assessment of larger populations or serial timepoints, while qualitative visual methods may be practical in community settings.

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Beyond alpha power: EEG spatial and spectral gradients robustly stratify disorders of consciousness.

Publications

Beyond alpha power: EEG spatial and spectral gradients robustly stratify disorders of consciousness.

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