Dynamic Formation of a Posterior-to-Anterior Peak-Alpha-Frequency Gradient Driven by Two Distinct Processes

eNeuro. 2024 Aug 29;11(8):ENEURO.0273-24.2024. doi: 10.1523/ENEURO.0273-24.2024. Print 2024 Aug.

Abstract

Peak-alpha frequency varies across individuals and mental states, but it also forms a negative gradient from posterior to anterior regions in association with increases in cortical thickness and connectivity, reflecting a cortical hierarchy in temporal integration. Tracking the spatial standard deviation of peak-alpha frequency in scalp EEG, we observed that a posterior-to-anterior gradient dynamically formed and dissolved. Periods of high spatial standard deviation yielded robustly negative posterior-to-anterior gradients-the "gradient state"-while periods of low spatial standard deviation yielded globally converged peak-alpha frequency-the "uniform state." The state variations were characterized by a combination of slow (0.3-0.5 Hz) oscillations and random-walk-like fluctuations. They were relatively independently correlated with peak-alpha frequency variations in anterior regions and peak-alpha power variations in central regions driven by posterior regions (together accounting for ∼50% of the state variations), suggesting that two distinct mechanisms modulate the state variations: an anterior mechanism that directly adjusts peak-alpha frequencies and a posterior-central mechanism that indirectly adjusts them by influencing synchronization. The state variations likely reflect general operations as their spatiotemporal characteristics remained unchanged while participants engaged in a variety of tasks (breath focus, vigilance, working memory, mental arithmetic, and generative thinking) with their eyes closed or watched a silent nature video. The ongoing state variations may dynamically balance two global processing modes, one that facilitates greater temporal integration (and potentially also information influx) toward anterior regions in the gradient state and the other that facilitates flexible global communication (via phase locking) in the uniform state.

Keywords: EEG; dynamics; neural oscillation; peak-alpha frequency; posterior–anterior gradient.

MeSH terms

  • Adult
  • Alpha Rhythm* / physiology
  • Brain / physiology
  • Brain Mapping
  • Cerebral Cortex / physiology
  • Electroencephalography
  • Female
  • Humans
  • Male
  • Young Adult