Neural attentional-filter mechanisms of listening success in middle-aged and older individuals

Sarah Tune,Mohsen Alavash,Jonas Obleser,Lorenz Fiedler

doi:10.1038/s41467-021-24771-9

Sarah Tune, Mohsen Alavash + Show 2 more

Open Access

https://doi.org/10.1038/s41467-021-24771-9

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Abstract

Successful listening crucially depends on intact attentional filters that separate relevant from irrelevant information. Research into their neurobiological implementation has focused on two potential auditory filter strategies: the lateralization of alpha power and selective neural speech tracking. However, the functional interplay of the two neural filter strategies and their potency to index listening success in an ageing population remains unclear. Using electroencephalography and a dual-talker task in a representative sample of listeners (N = 155; age=39–80 years), we here demonstrate an often-missed link from single-trial behavioural outcomes back to trial-by-trial changes in neural attentional filtering. First, we observe preserved attentional–cue-driven modulation of both neural filters across chronological age and hearing levels. Second, neural filter states vary independently of one another, demonstrating complementary neurobiological solutions of spatial selective attention. Stronger neural speech tracking but not alpha lateralization boosts trial-to-trial behavioural performance. Our results highlight the translational potential of neural speech tracking as an individualized neural marker of adaptive listening behaviour.

Highlights

Successful listening crucially depends on intact attentional filters that separate relevant from irrelevant information
Neural attentional filters can be instantiated by different mechanistic principles and recent studies have predominantly focused on two potential but nonexclusive neural filter strategies originating from distinct research traditions: From the visual domain stems an influential line of research that supports the role of alpha-band (~8–12 Hz) oscillatory activity in the implementation of controlled, top-down suppression of behaviourally irrelevant information[5,6,7,8]
Sentence pairs were temporally aligned to the onset of these task-relevant final words which led to slightly asynchronous sentence onsets

Summary

Introduction

Successful listening crucially depends on intact attentional filters that separate relevant from irrelevant information Research into their neurobiological implementation has focused on two potential auditory filter strategies: the lateralization of alpha power and selective neural speech tracking. We lack understanding of whether or how modulations in lateralized alpha power and the neural tracking of attended versus ignored speech in the wider auditory cortex interact in the service of successful listening behaviour. Few studies using more real-life listening and speech-tracking measures were able to explicitly address the functional relevance of the discussed neural filter strategies, that is, their potency to explain behavioural listening success[27,28]. We manipulated the semantic predictability of upcoming speech via a semantic category cue

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