Network Model With Reduced Metabolic Rate Predicts Spatial Synchrony of Neuronal Activity

In a cerebral hypometabolic state, cortical neurons exhibit slow synchronous oscillatory activity with sparse firing. How such a synchronization spatially organizes as the cerebral metabolic rate decreases have not been systemically investigated. We developed a network model of leaky integrate-and-fire neurons with an additional dependency on ATP dynamics. Neurons were scattered in a 2D space, and their population activity patterns at varying ATP levels were simulated. The model predicted a decrease in firing activity as the ATP production rate was lowered. Under hypometabolic conditions, an oscillatory firing pattern, that is, an ON-OFF cycle arose through a failure of sustainable firing due to reduced excitatory positive feedback and rebound firing after the slow recovery of ATP concentration. The firing rate oscillation of distant neurons developed at first asynchronously that changed into burst suppression and global synchronization as ATP production further decreased. These changes resembled the experimental data obtained from anesthetized rats, as an example of a metabolically suppressed brain. Together, this study substantiates a novel biophysical mechanism of neuronal network synchronization under limited energy supply conditions.