Advancing EEG-based assessment of consciousness and cognition in prolonged disorders of consciousness

Abstract

Background: Accurate assessment of residual awareness in patients with Prolonged Disorders of Consciousness (PDoC) remains a major clinical challenge, as conventional behavioural tools can underestimate covert cognition. This study evaluates whether a structured, multi-phase motor imagery Brain–Computer Interface (MI-BCI) protocol provides objective electroencephalography (EEG)-based indicators of awareness that complement behavioural assessments. Methods: Forty-four participants (N = 44) completed repeated imagined-movement tasks using wearable EEG (PDoC: Unresponsive Wakefulness Syndrome (UWS, n = 14), Minimally Conscious State (MCS, n = 17), Locked-In Syndrome (LIS, n = 11); two able-bodied participants as benchmarks; ClinicalTrials.gov: NCT03827187; 30-01-2019). The protocol assessed sensorimotor rhythm modulation, training with and without neurofeedback, and binary question answering across phases. Standard behavioural assessments (CRS-R and WHIM) were administered at each session. Results: Significant MI-BCI decoding accuracy (DA) is achieved by 73.8% of patients, of whom 90% progress to Q&A testing and frequently exceed the 70% usability threshold, revealing marked inter-individual heterogeneity. For significant MI-BCI runs, LIS outperform MCS (p = 0.007) and UWS (p = 0.048), while UWS exceed MCS during Q&A (p = 0.049), driven by familiar-voice stimuli. Using leave-one-subject-out cross-validation, combining predictions from DA and behavioural assessments improves balanced diagnostic accuracy to 62% (from 55%), increasing sensitivity to MCS (39% to 69%), with a modest reduction in LIS sensitivity (78% to 67%). Task-related activity over sensorimotor and parietal cortices differentiate diagnostic groups. Conclusions: The structured MI-BCI protocol demonstrates potential as a movement-independent, EEG-based tool for distinguishing UWS, MCS and LIS. Integrating DA and spatial patterns yields diagnostic information that may augment behavioural assessment and advance objective tools for evaluating awareness in PDoC.