Transcranial stimulation of alpha oscillations modulates brain state dynamics in sustained attention

The brain is a complex system from which cognition is thought to arise as an emergent behavior, but the mechanisms underlying such processes remain unclear. We approached this problem based on the recognition of the two primary organizational architectures of the brain—large-scale networks and oscillatory synchrony—and their fundamental importance in cognition. Here, we applied high-definition alpha-frequency transcranial alternating-current stimulation (HD α -tACS) in a sustained attention task during functional resonance imaging (fMRI) to causally elucidate organizing principles of these major architectures (particularly, the role of alpha oscillatory synchrony) in cognition. We demonstrated that α -tACS both increased electroencephalogram (EEG) alpha power and improved sustained attention, degrees of which were positively correlated. Using Hidden Markov Modeling (HMM) of fMRI timeseries, we further uncovered five functionally important brain states (defined by distinct activity patterns of large-scale networks) and revealed the regulation of their temporal dynamics by α -tACS such that a Task-Negative state (characterized by activation of the default mode network/DMN) and Distraction state (with activation of the ventral attention and visual networks) was suppressed. These findings confirm the role of alpha oscillations in sustained attention, and more importantly, they afford a complex systems account that sustained attention is underpinned by multiple transient, recurrent brain states, whose dynamical balances are regulated by alpha oscillations. The study also highlights the efficacy of non-invasive oscillatory neuromodulation in probing the operation of the complex brain system and encourages future clinical applications to improve neural system health and cognitive performance. Significance Statement The brain operates a well-organized complex system to support mental activities. Along with well-known fluctuations in attention, we uncovered that the brain undergoes dynamic vacillations of functional states that are organized through large-scale neural networks and regulated by neural oscillations. We showcased that during sustained attention over an extended period time, the brain maintains a tug-of-war between functional “on” and “off” states. Applying α -tACS, we further demonstrated that the brain self-organizes this complex system through alpha oscillations, regulating the balance of such dynamic states in the upkeeping of cognitive performance. ### Competing Interest Statement The authors have declared no competing interest.