Spectral and temporal characterization of sleep spindles—methodological implications

Abstract

Objective. Nested into slow oscillations (SOs) and modulated by their up-states, spindles are electrophysiological hallmarks of N2 sleep stage that present a complex hierarchical architecture. However, most studies have only described spindles in basic statistical terms, which were limited to the spindle itself without analyzing the characteristics of the pre-spindle moments in which the SOs are originated. The aim of this study was twofold: (a) to apply spectral and temporal measures to the pre-spindle and spindle periods, as well as analyze the correlation between them, and (b) to evaluate the potential of these spectral and temporal measures in future automatic detection algorithms. Approach. An automatic spindle detection algorithm was applied to the overnight electroencephalographic recordings of 26 subjects. Ten complementary features (five spectral and five temporal parameters) were computed in the pre-spindle and spindle periods after their segmentation. These features were computed independently in each period and in a time-resolved way (sliding window). After the statistical comparison of both periods, a correlation analysis was used to assess their interrelationships. Finally, a receiver operating-characteristic (ROC) analysis along with a bootstrap procedure was conducted to further evaluate the degree of separability between the pre-spindle and spindle periods. Main results. The results show important time-varying changes in spectral and temporal parameters. The features calculated in pre-spindle and spindle periods are strongly and significantly correlated, demonstrating the association between the pre-spindle characteristics and the subsequent spindle. The ROC analysis exposes that the typical feature used in automatic spindle detectors, i.e. the power in the sigma band, is outperformed by other features, such as the spectral entropy in this frequency range. Significance. The novel features applied here demonstrate their utility as predictors of spindles that could be incorporated into novel algorithms of automatic spindle detectors, in which the analysis of the pre-spindle period becomes relevant for improving their performance. From the clinical point of view, these features may serve as novel precision therapeutic targets to enhance spindle production with the aim of improving memory, cognition, and sleep quality in healthy and clinical populations. The results evidence the need for characterizing spindles in terms beyond power and the spindle period itself to more dynamic measures and the pre-spindle period. Physiologically, these findings suggest that spindles are more than simple oscillations, but nonstable oscillatory bursts embedded in the complex pre-spindle dynamics.