Phase and amplitude electroencephalography correlations change with disease progression in people with idiopathic rapid eye-movement sleep behavior disorder

Abstract

Study Objectives Increased phase synchronization in electroencephalography (EEG) bands might reflect the activation of compensatory mechanisms of cognitive decline in people with neurodegenerative diseases. Here, we investigated whether altered large-scale couplings of brain oscillations could be linked to the balancing of cognitive decline in a longitudinal cohort of people with idiopathic rapid eye-movement sleep behavior disorder (iRBD). Methods We analyzed 18 patients (17 males, 69.7±7.5 years) with iRBD undergoing high-density EEG (HD-EEG), presynaptic dopaminergic imaging, and clinical and neuropsychological assessments at two time points (time interval 24.2±5.9 months). We thus quantified the HD-EEG power distribution, orthogonalized amplitude correlation and weighted phase lag index at both time points and correlated them with clinical, neuropsychological and imaging data. Results Four patients phenoconverted at follow-up (three cases of parkinsonism and one of dementia). At the group level, neuropsychological scores decreased over time, without reaching statistical significance. However, alpha phase synchronization increased and delta amplitude correlations decreased significantly at follow-up compared to baseline. Both large-scale network connectivity metrics were significantly correlated with neuropsychological scores but not with sleep quality indices or presynaptic dopaminergic imaging data. Conclusions These results suggest that increased alpha phase synchronization and reduced delta amplitude correlation may be considered electrophysiological signs of an active compensatory mechanism of cognitive impairment in people with iRBD. Large-scale functional modifications may be helpful biomarkers in the characterization of prodromal stages of alpha-synucleinopathies.

Large-scale network metrics improve the classification performance of rapid-eye-movement sleep behavior disorder patients

“…These works reported a slowing of the alpha rhythm (Fantini et al, 2003;Rodrigues Brazète et al, 2016) and alterations in phase synchronization (Roascio et al, 2021;Sunwoo et al, 2017) and amplitude correlations (Roascio et al, 2021). Several lines of evidence suggest that NDDs are characterized by network deficiencies, and that the investigation of the cross-talk between different brain areas provides a better understanding of the diseases and their progression (Pusil et al, 2019;Roascio et al, 2021;Sunwoo et al, 2017).…”

“…Previous studies highlighted significant electrophysiological changes in iRBD patients (Fantini et al, 2003;Roascio et al, 2021;Rodrigues Brazète et al, 2016;Sunwoo et al, 2017) suggesting the importance of EEG-based features in differentiating iRBD from healthy subjects. These works reported a slowing of the alpha rhythm (Fantini et al, 2003;Rodrigues Brazète et al, 2016) and alterations in phase synchronization (Roascio et al, 2021;Sunwoo et al, 2017) and amplitude correlations (Roascio et al, 2021).…”

“…Previous studies highlighted significant electrophysiological changes in iRBD patients (Fantini et al, 2003;Roascio et al, 2021;Rodrigues Brazète et al, 2016;Sunwoo et al, 2017) suggesting the importance of EEG-based features in differentiating iRBD from healthy subjects. These works reported a slowing of the alpha rhythm (Fantini et al, 2003;Rodrigues Brazète et al, 2016) and alterations in phase synchronization (Roascio et al, 2021;Sunwoo et al, 2017) and amplitude correlations (Roascio et al, 2021). Several lines of evidence suggest that NDDs are characterized by network deficiencies, and that the investigation of the cross-talk between different brain areas provides a better understanding of the diseases and their progression (Pusil et al, 2019;Roascio et al, 2021;Sunwoo et al, 2017).…”

“…These brain oscillations represent a mechanism for neuronal communications (Fries, 2015) where coherent field oscillations facilitate stimulus propagation within a network of brain areas. In physiological conditions, increased phase synchronization facilitates communication while abnormal increase can be predictive of several pathological conditions such as Parkinson’s disease (Roascio et al, 2021; Sunwoo et al, 2017), Alzheimer’s disease (Pusil et al, 2019), and epilepsy (Avoli, 2014; Jiruska et al, 2013).…”

“…Many studies highlighted electrophysiological changes in iRBD patients (Fantini et al, 2003; Roascio et al, 2021; Rodrigues Brazète et al, 2016; Sunwoo et al, 2017) suggesting the importance of EEG features in differentiating iRBD from healthy subjects. It is known that the “slowing down” of the power spectrum is a typical characteristic of people with iRBD compared to healthy subjects (Fantini et al, 2003; Rodrigues Brazète et al, 2016).…”