Oscillations, criticality and responsiveness in complex brain networks

Brain networks during unconscious states resulting from sleep, anesthesia, or traumatic injuries are associated with a limited capacity for complex responses to stimulation. Even during the conscious resting state, responsiveness to stimulus is highly dependent on spontaneous brain activities. Many empirical findings have been suggested that the brain responsiveness is determined mainly by the ongoing brain activity when a stimulus is given. However, there has been no systematic study exploring how such various brain activities with high or low synchronization, amplitude, and phase response to stimuli. In this model study, we simulated large-scale brain network dynamics in three brain states (below, near, and above the critical state) and investigated a relationship between ongoing oscillation properties and a stimulus decomposing the brain activity into fundamental oscillation properties (instantaneous global synchronization, amplitude, and phase). We identified specific stimulation conditions that produce varying levels of brain responsiveness. When a single pulsatile stimulus was applied to globally desynchronized low amplitude of oscillation, the network generated a large response. By contrast, when a stimulus was applied to specific phases of oscillation that were globally synchronized with high amplitude activity, the response was inhibited. This study proposes the oscillatory conditions to induce specific stimulation outcomes in the brain that can be systematically derived from networked oscillator properties, and reveals the presence of state-dependent temporal windows for optimal brain stimulation. The identified relationship will help advance understanding of the small/large responsiveness of the brain in different states of consciousness and suggest state-dependent methods to modulate responsiveness. Author Summary A responsiveness of the brain network to external stimulus is different across brain states such as wakefulness, sleep, anesthesia, and traumatic injuries. It has been shown that responsiveness of the brain during conscious state also varies due to the diverse transient states of the brain characterized by different global and local oscillation properties. In this computational model study using large-scale brain network, we hypothesized that the brain responsiveness is determined by the interactions of networked oscillators when a stimulus is applied to the brain. We examined relationships between responsiveness of the brain network, global synchronization levels, and instantaneous oscillation properties such as amplitude and phase in different brain states. We found specific stimulation conditions of the brain that produce large or small levels of responsiveness. The identified relationship suggests the existence of temporal windows that periodically inhibit sensory information processing during conscious state and develops state-dependent methods to modulate brain responsiveness considering dynamically changed functional brain network.