No 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.

In recent years, hemispheric lateralisation of alpha power has emerged as a neural mechanism thought to underpin spatial attention across sensory modalities. Yet, how healthy ageing, beginning in middle adulthood, impacts the modulation of lateralised alpha power supporting auditory attention remains poorly understood. In the current electroencephalography study, middle-aged and older adults (N = 29; ~40-70 years) performed a dichotic listening task that simulates a challenging, multitalker scenario. We examined the extent to which the modulation of 8-12 Hz alpha power would serve as neural marker of listening success across age. With respect to the increase in interindividual variability with age, we examined an extensive battery of behavioural, perceptual and neural measures. Similar to findings on younger adults, middle-aged and older listeners' auditory spatial attention induced robust lateralisation of alpha power, which synchronised with the speech rate. Notably, the observed relationship between this alpha lateralisation and task performance did not co-vary with age. Instead, task performance was strongly related to an individual's attentional and working memory capacity. Multivariate analyses revealed a separation of neural and behavioural variables independent of age. Our results suggest that in age-varying samples as the present one, the lateralisation of alpha power is neither a sufficient nor necessary neural strategy for an individual's auditory spatial attention, as higher age might come with increased use of alternative, compensatory mechanisms. Our findings emphasise that explaining interindividual variability will be key to understanding the role of alpha oscillations in auditory attention in the ageing listener.

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.

SignificanceHow do brain networks shape our listening behavior? We here develop and test the hypothesis that, during challenging listening situations, intrinsic brain networks are reconfigured to adapt to the listening demands and thus, to enable successful listening. We find that, relative to a task-free resting state, networks of the listening brain show higher segregation of temporal auditory, ventral attention, and frontal control regions known to be involved in speech processing, sound localization, and effortful listening. Importantly, the relative change in modularity of this auditory control network predicts individuals’ listening success. Our findings shed light on how cortical communication dynamics tune selection and comprehension of speech in challenging listening situations and suggest modularity as the network principle of auditory attention.