Slower EEG alpha generation, synchronization and “flow”—possible biomarkers of cognitive impairment and neuropathology of minor stroke

Abstract

BackgroundWe investigated EEG rhythms, particularly alpha activity, and their relationship to post-stroke neuropathology and cognitive functions in the subacute and chronic stages of minor strokes.MethodsWe included 10 patients with right middle cerebral artery (MCA) ischemic strokes and 11 healthy controls. All the assessments of stroke patients were done both in the subacute and chronic stages. Neurological impairment was measured using the National Institute of Health Stroke Scale (NIHSS), whereas cognitive functions were assessed using the Montreal Cognitive Assessment (MoCA) and MoCA memory index (MoCA-MIS). The EEG was recorded using a 19 channel EEG system with standard EEG electrode placement. In particular, we analyzed the EEGs derived from the four lateral frontal (F3, F7, F4, F8), and corresponding lateral posterior (P3, P4, T5, T6) electrodes. Quantitative EEG analysis included: the group FFT spectra, the weighted average of alpha frequency (αAVG), the group probability density distributions of all conventional EEG frequency band relative amplitudes (EEG microstructure), the inter- and intra-hemispheric coherences, and the topographic distribution of alpha carrier frequency phase potentials (PPs). Statistical analysis was done using a Kruskal–Wallis ANOVA with a post-hoc Mann–Whitney U two-tailed test, and Spearman’s correlation.ResultsWe demonstrated transient cognitive impairment alongside a slower alpha frequency (αAVG) in the subacute right MCA stroke patients vs. the controls. This slower alpha frequency showed no amplitude change, but was highly synchronized intra-hemispherically, overlying the ipsi-lesional hemisphere, and inter-hemispherically, overlying the frontal cortex. In addition, the disturbances in EEG alpha activity in subacute stroke patients were expressed as a decrease in alpha PPs over the frontal cortex and an altered “alpha flow”, indicating the sustained augmentation of inter-hemispheric interactions. Although the stroke induced slower alpha was a transient phenomenon, the increased alpha intra-hemispheric synchronization, overlying the ipsi-lesional hemisphere, the increased alpha F3–F4 inter-hemispheric synchronization, the delayed alpha waves, and the newly established inter-hemispheric “alpha flow” within the frontal cortex, remained as a permanent consequence of the minor stroke. This newly established frontal inter-hemispheric “alpha flow” represented a permanent consequence of the “hidden” stroke neuropathology, despite the fact that cognitive impairment has been returned to the control values. All the detected permanent changes at the EEG level with no cognitive impairment after a minor stroke could be a way for the brain to compensate for the lesion and restore the lost function. DiscussionOur study indicates slower EEG alpha generation, synchronization and “flow” as potential biomarkers of cognitive impairment onset and/or compensatory post-stroke re-organizational processes.

Spectral Resting-State EEG (rsEEG) in Chronic Aphasia Is Reliable, Sensitive, and Correlates With Functional Behavior

“…For the left and right hemisphere montages, the average reference was calculated separately using only the electrodes in that hemisphere to ensure that only activation in the hemisphere of interest was included. Previous research has reported on hemispheric comparisons in both healthy controls and individuals post-stroke, indicating a need for information regarding the stability and reliability of such measures (e.g., Hensel et al, 2004 ; Spironelli and Angrilli, 2009 ; Spironelli et al, 2013 ; Herron et al, 2014 ; Petrovic et al, 2017 ). Also, neuroimaging studies have long utilized hemispheric comparisons and/or examined hemispheric differences and related behaviors (e.g., French and Beaumont, 1984 ; Bolduc et al, 2003 ; Szaflarski et al, 2006 ; Learmonth et al, 2017 ; Othman et al, 2020 ).…”

“…Spectral task-based EEG in 11 German-speaking PWAs (five non-fluent, six fluent) demonstrated that decreased left hemisphere delta power corresponded to significant language recovery in the first year post stroke, but no changes in language recovery or delta power were seen in the second year post stroke ( Hensel et al, 2004 ). In a similar study of cognitive function (measured by the MoCA) following mild right hemisphere stroke in 10 Serbian-speaking participants, Petrovic et al (2017) reported that spectral rsEEG features measured approximately 10 days post-stroke did not fully resolve 1–1.5 years post-stroke, even when cognitive behavioral performance did. It was posited that these permanent changes in rsEEG were a result of neural adaptations to support cognition in the face of a lesion.…”

“…Acceptable specificity and test-retest reliability has yet to be investigated or established for specific patient populations. Despite this very limited psychometric evidence to support the use of spectral EEG as a repeated measure, it is already being used in this manner in research (e.g., Rozelle and Budzynski, 1995 ; Hensel et al, 2004 ; Stojanovic et al, 2013 ; Wu et al, 2015 ; Petrovic et al, 2017 ). Defining specificity and reliability of spectral rsEEG measures utilizing varied electrode montages post-stroke is critical to ensuring appropriate application of these measures and preventing research waste (for a discussion of research waste as it pertains to biomarkers, see Ioannidis and Bossuyt, 2017 ).…”

The influence of diversity on the measurement of functional impairment: An international validation of the Amsterdam IADL Questionnaire in eight countries

“…The present study included data from 3571 individuals with a completed A‐IADL‐Q from memory clinics and cognition studies from eight countries: The Netherlands (Amsterdam Dementia Cohort 18 and European Prevention of Alzheimer's Dementia Longitudinal Cohort Study, EPAD 19,20 ), Spain (Compostela Aging Study 21,22 ; EPAD; and Alfa + project 23 ), France (investigation of Alzheimer's predictors in subjective memory complainers (INSIGHT‐preAD) study 24 ; EPAD; and Socrates study), United States (Butler Alzheimer's Prevention Registry 25 ), United Kingdom (EPAD and software architecture for mental health self management (SAMS) project 26 ), Greece (Greek Association for Alzheimer's Disease and Related Disorders), Serbia (Niš Clinic of Neurology 27 ), and Finland (Helsinki Small Vessel Disease study).…”

Driving Oscillatory Dynamics: Neuromodulation for Recovery After Stroke

“…After stroke, alpha oscillations in human patients are lower in frequency and more synchronised (Petrovic et al, 2017), while desynchronisation of this activity during recovery is associated with improved motor outcome (Westlake et al, 2012;Ray et al, 2020). Alpha oscillatory power has also been shown to be increased in both the unaffected and affected hemispheres in mice 9 days after stroke when compared to controls (Vallone et al, 2016).…”