Electroencephalogram criticality in cognitive impairment: a monitoring biomarker?

Unlabelled: Critical states present scale-free dynamics, optimizing neuronal complexity and serving as a potential biomarker in cognitively impaired patients. We explored electroencephalogram (EEG) criticality in amnesic Mild Cognitive Impairment patients with clinical improvement in working memory, verbal memory, verbal fluency and overall executive functions after the completion of a 6-month prospective memory training. We compared "before" and "after" stationary resting-state EEG records of right-handed MCI patients (n = 17; 11 females), using the method of critical fluctuations and Haar wavelet analysis. Improvement of criticality indices was observed in most electrodes, with mean values being higher after prospective memory training. Significant criticality enhancement was found in the subgroup analysis of frontotemporal electrodes [mean dif: 0.10; Z = 7,  = 0.019]. In the isolated electrode signal analysis, significant post-intervention improvement was noted in pooled criticality indices of electrodes T6 [mean dif: 0.204; t(10) = -2.3,  = 0.044] and F4 [mean dif: 0.0194; t(10) = -2.82;  = 0.018]. EEG criticality agreed with clinical improvement, consisting a possible quantifiable and easy-to-obtain biomarker in MCI and Alzheimer's disease (AD), especially in patients under cognitive training/rehabilitation. We highlight the role of EEG in prognostication, monitoring and potentially early treatment optimization in MCI or AD patients. Further standardization of the methodology in larger patient cohorts could be valuable for AD theragnostics in patients receiving disease-modifying treatments by providing insights regarding synaptic brain plasticity.

Graphical Abstract: Critical states' scale-free dynamics optimize neuronal complexity, emerging as biomarkers in cognitive neuroscience. Applying the method of critical fluctuations and Haar wavelet analysis in stationary EEG time-series, we demonstrate criticality enhancement in the frontotemporal electroencephalographic (EEG) recordings of mild cognitive impairment (MCI) patients after a 6-month prospective memory training, suggesting EEG criticality as a possible monitoring biomarker in MCI and Alzheimer's disease.

Supplementary Information: The online version contains supplementary material available at 10.1007/s11571-024-10155-4.