Neural desynchronization and arousal differentially shape brain states for optimal sensory performance

Instantaneous brain states have consequences for our sensation, perception, and behaviour. Both fluctuations in arousal and in neural desynchronization likely pose perceptually relevant states. However, their relationship and their relative impact on perception is unclear. We here provide evidence that, at the single-trial level in humans, desynchronization in sensory cortex (expressed as time series entropy) and pupil-linked arousal differentially impact optimal perceptual processing. While we recorded electroencephalography (EEG) and pupillometry data, stimuli of a demanding auditory discrimination task were presented into states of high or low desynchronization of auditory cortex via a real-time closed-loop setup. Desynchronization and arousal distinctly influenced stimulus-evoked activity and shaped behaviour displaying an inverted u-shaped relationship: States of intermediate desynchronization elicited minimal response bias and fastest responses, while states of intermediate arousal gave rise to highest response sensitivity. Our results speak to a model in which independent states of global arousal and local desynchronization jointly optimise sensory processing and performance.