Local cortical desynchronization and pupil-linked arousal differentially shape brain states for optimal sensory performance.

Leonhard Waschke,Jonas Obleser,Sarah Tune

doi:10.7554/elife.51501

Abstract

Instantaneous brain states have consequences for our sensation, perception, and behaviour. Fluctuations in arousal and neural desynchronization likely pose perceptually relevant states. However, their relationship and their relative impact on perception is unclear. We here show that, at the single-trial level in humans, local desynchronization in sensory cortex (expressed as time-series entropy) versus pupil-linked arousal differentially impact 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 local desynchronization and global arousal jointly optimise sensory processing and performance.

Highlights

The way we sense and perceive our environment is not determined by physical input through the senses alone
We combined linear mixed-effects models and psychophysical modelling to test the effects of local cortical desynchronization as well as pupil-linked arousal on (1) ongoing as well as sensory-related EEG activity, and on (2) perceptual performance
This study tested the influence of local cortical desynchronization and pupil-linked arousal on sensory processing and perceptual performance

Summary

Introduction

The way we sense and perceive our environment is not determined by physical input through the senses alone. Instantaneous fluctuations of both pupil-linked arousal (McGinley et al., 2015b; Lee et al, 2018; Pfeffer et al, 2018) and neural desynchronization (Curto et al., 2009; Marguet and Harris, 2011; Pachitariu et al, 2015) have been highlighted as sources of such sensory and perceptual variation: Arousal and cortical desynchronization are two ways of characterizing the brain state, which strongly influences sensory cortical responses, the encoding of information, perception and behaviour. Pupil-linked arousal, which captures locus coeruleus-norepinephrine activity (LC–NE; Aston-Jones & Cohen, 2005; Joshi, Li, Kalwani, & Gold, 2016; Reimer et al, 2016) has been shown to influence sensory evoked activity (McGinley et al, 2015a, 2015b; Gelbard-Sagiv et al, 2018) and the processing of task-relevant information (Murphy et al, 2014; Lee et al, 2018). Despite evidence for an inverted u-shaped relation of tonic LC–NE activity to performance long suspected from the Yerkes-Dodson law (Yerkes and Dodson, 1908), the precise associations between arousal, sensory processing, and behaviour are underspecified: optimal performance at intermediate levels of arousal has reliably been observed (Murphy et al, 2014; McGinley et al, 2015b, 2015a; van den Brink et al, 2016; Faller et al, 2019), reports of linear effects on performance (Gelbard-Sagiv et al, 2018) or evoked activity (Neske and McCormick, 2018) in different tasks and species complicate this picture

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