Tracking transient changes in the neural frequency architecture: harmonic relationships between theta and alpha peaks facilitate cognitive performance

The synchronisation between neural oscillations at different frequencies has been proposed as a core mechanism for the coordination and integration of neural systems at different spatio-temporal scales. Since 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 ‘non-harmonic’ alpha:theta cross-frequency relationships (i.e. alphapeak/thetapeak = 1.1-1.6) which showed a higher incidence during rest compared to the arithmetic task. The observation that alpha and theta rhythms shifted into ‘harmonic’ versus ‘non-harmonic’ 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’.status: Published onlin