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

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.

Orienting auditory attention in time: Lateralized alpha power reflects spatio-temporal filtering

The deployment of neural alpha (8-12 Hz) lateralization in service of spatial attention is well-established: Alpha power increases in the cortical hemisphere ipsilateral to the attended hemifield, and decreases in the contralateral hemisphere, respectively. Much less is known about humans’ ability to deploy such alpha lateralization in time, and to thus exploit alpha power as a spatio-temporal filter. Here we show that spatially lateralized alpha power does signify - beyond the direction of spatial attention - the distribution of attention in time and thereby qualifies as a spatio-temporal attentional filter. Participants (N = 20) selectively listened to spoken numbers presented on one side (left vs right), while competing numbers were presented on the other side. Key to our hypothesis, temporal foreknowledge was manipulated via a visual cue, which was either instructive and indicated the to-be-probed number position (70% valid) or neutral. Temporal foreknowledge did guide participants’ attention, as they recognized numbers from the to-be-attended side more accurately following valid cues. In the magnetoencephalogram (MEG), spatial attention to the left versus right side induced lateralization of alpha power in all temporal cueing conditions. Modulation of alpha lateralization at the 0.8-Hz presentation rate of spoken numbers was stronger following instructive compared to neutral temporal cues. Critically, we found stronger modulation of lateralized alpha power specifically at the onsets of temporally cued numbers. These results suggest that the precisely timed hemispheric lateralization of alpha power qualifies as a spatio-temporal attentional filter mechanism susceptible to top-down behavioural goals.

The impact of neural attentional filters on listening behavior in a large cohort of aging individuals

Successful listening crucially depends on intact attentional filters that separate relevant from irrelevant information. Research into their neurobiological implementation has focused on one of two 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 aging population remains unclear. Using electroencephalography and a dual-talker task in a representative sample of aging listeners (N=155; age=39–80 years), we here demonstrate an often-missed link from single-trial behavioral outcomes back to trial-by-trial changes in neural attentional filtering. First, we observed preserved attentional– cue-driven modulation of both neural filters across chronological age and hearing levels. Second, neural filter states varied independently of one another, demonstrating a functional trade-off between distinct neurobiological attentional filter mechanisms. Stronger neural speech tracking but not alpha lateralization boosted trial-to-trial behavioral performance. Our results highlight the translational potential of neural speech tracking as an individualized neural marker of adaptive listening behavior.Significance statementSuccessful listening requires a form of attentional filtering into behaviorally relevant and irrelevant acoustic information. Most previous studies have focused on one of two candidate neural filter strategies: the lateralization of alpha power and selective neural speech tracking. Closing the gap between hitherto separate lines of research, we used electroencephalography and a dual-talker task in a large sample of aging listeners to directly probe the functional relevance of state- and trait-level changes in these neural filter strategies to listening success. We demonstrate the co-existence of largely independent neural filters that establish alternating regimes of strong alpha lateralization versus neural speech tracking. Additionally, our results emphasize the utility of neural speech tracking over alpha lateralization as a potential neural marker of an individual’s adaptive listening behavior.