Global Forebrain Dynamics Predict Rat Behavioral States and Their Transitions

Abstract

The wake-sleep cycle, a spontaneous succession of global brain states that correspond to major overt behaviors, occurs in all higher vertebrates. The transitions between these states, at once rapid and drastic, remain poorly understood. Here, intracranial local field potentials (LFPs) recorded in the cortex, hippocampus, striatum, and thalamus were used to characterize the neurophysiological correlates of the rat wake-sleep cycle. By way of a new method for the objective classification and quantitative investigation of all major brain states, we demonstrate that global brain state transitions occur simultaneously across multiple forebrain areas as specific spectral trajectories with characteristic path, duration, and coherence bandwidth. During state transitions, striking changes in neural synchronization are effected by the prominent narrow-band LFP oscillations that mark state boundaries. Our results demonstrate that distant forebrain areas tightly coordinate the processing of neural information during and between global brain states, indicating a very high degree of functional integration across the entire wake-sleep cycle. We propose that transient oscillatory synchronization of synaptic inputs, which underlie the rapid switching of global brain states, may facilitate the exchange of information within and across brain areas at the boundaries of very distinct neural processing regimens.