Transient oscillation dynamics during sleep provide a robust basis for electroencephalographic phenotyping and biomarker identification

Abstract

AbstractTransient oscillatory events in the sleep electroencephalogram represent short-term coordinated network activity. Of particular importance, sleep spindles are transient oscillatory events associated with memory consolidation, which are altered in aging and in several psychiatric and neurodegenerative disorders. Spindle identification, however, currently contains implicit assumptions derived from what waveforms were historically easiest to discern by eye, and has recently been shown to select only a high-amplitude subset of transient events. Moreover, spindle activity is typically averaged across a sleep stage, collapsing continuous dynamics into discrete states. What information can be gained by expanding our view of transient oscillatory events and their dynamics? In this paper, we develop a novel approach to electroencephalographic phenotyping, characterizing a generalized class of transient time-frequency events across a wide frequency range using continuous dynamics. We demonstrate that the complex temporal evolution of transient events during sleep is highly stereotyped when viewed as a function of slow oscillation power (an objective, continuous metric of depth-of-sleep) and phase (a correlate of cortical up/down states). This two-fold power-phase representation has large intersubject variability—even within healthy controls—yet strong night-to-night stability for individuals, suggesting a robust basis for phenotyping. As a clinical application, we then analyze patients with schizophrenia, confirming established spindle (12–15 Hz) deficits as well as identifying novel differences in transient non-rapid eye movement events in low-alpha (7–10 Hz) and theta (4–6 Hz) ranges. Overall, these results offer an expanded view of transient activity, describing a broad class of events with properties varying continuously across spatial, temporal, and phase-coupling dimensions.