The brain operates an advanced complex system to support mental activities. Cognition is thought to emerge from dynamic states of the complex brain system, which are organized spatially through large-scale neural networks and temporally via neural synchrony. However, specific mechanisms underlying these processes remain obscure. Applying high-definition alpha-frequency transcranial alternating-current stimulation (HD α-tACS) in a continuous performance task (CPT) during functional resonance imaging (fMRI), we causally elucidate these major organizational architectures in a key cognitive operation-sustained attention. We demonstrated that α-tACS enhanced both electroencephalogram (EEG) alpha power and sustained attention, in a correlated fashion. Akin to temporal fluctuations inherent in sustained attention, our hidden Markov modeling (HMM) of fMRI timeseries uncovered several recurrent, dynamic brain states, which were organized through a few major neural networks and regulated by the alpha oscillation. Specifically, during sustain attention, α-tACS regulated the temporal dynamics of the brain states by suppressing 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). These findings thus linked dynamic states of major neural networks and alpha oscillations, providing important insights into systems-level mechanisms of attention. They also highlight the efficacy of non-invasive oscillatory neuromodulation in probing the functioning of the complex brain system and encourage future clinical applications to improve neural systems health and cognitive performance.
Keywords: Attention; Biological sciences; Cognitive neuroscience; Computational neuroscience; Dynamical systems; Human behaviour; Neuroscience; Psychology; Social science; complex systems; dynamics; hidden states; non-invasive brain stimulation (NIBS); simultaneous fMRI-tACS.