Tracking Transient Changes in the Neural Frequency Architecture: Harmonic Relationships between Theta and Alpha Peaks Facilitate Cognitive Performance.

Abstract

The synchronization between neural oscillations at different frequencies has been proposed as a core mechanism for the coordination and integration of neural systems at different spatiotemporal scales. Because neural oscillations of different frequencies can only fully synchronize when their "peak" frequencies form harmonic relationships (e.g., f2 = f1/2), the present study explored whether the transient occurrence of harmonic cross-frequency relationship between task-relevant rhythms underlies efficient cognitive processing. Continuous EEG recordings (51 human participants; 14 males) were obtained during an arithmetic task, rest and breath focus. In two separate experiments, we consistently show that the proportion of epochs displaying a 2:1 harmonic relationship between alpha (8-14 Hz) and theta (4-8 Hz) peak frequencies (i.e., alphapeak ≈ 10.6 Hz; thetapeak ≈ 5.3 Hz), was significantly higher when cognitive demands increased. In addition, a higher incidence of 2:1 harmonic cross-frequency relationships was significantly associated with increased alpha-theta phase synchrony and improved arithmetic task performance, thereby underlining the functional relevance of this cross-frequency configuration. Notably, opposite dynamics were identified for a specific range of "nonharmonic" alpha-theta cross-frequency relationships (i.e., alphapeak/thetapeak = 1.1-1.6), which showed a higher incidence during rest compared with the arithmetic task. The observation that alpha and theta rhythms shifted into harmonic versus nonharmonic cross-frequency relationships depending on (cognitive) task demands is in line with the notion that the neural frequency architecture entails optimal frequency arrangements to facilitate cross-frequency "coupling" and "decoupling".SIGNIFICANCE STATEMENT Neural activity is known to oscillate within discrete frequency bands and the interplay between these brain rhythms is hypothesized to underlie cognitive functions. A recent theory posits that shifts in the peak frequencies of oscillatory rhythms form the principal mechanism by which cross-frequency coupling and decoupling is implemented in the brain. In line with this notion, we show that the occurrence of a cross-frequency arrangement that mathematically enables coupling between alpha and theta rhythms is more prominent during active cognitive processing (compared with rest and non-cognitively demanding tasks) and is associated with improved cognitive performance. Together, our results open new vistas for future research on cross-frequency dynamics in the brain and their functional role in cognitive processing.