In principle, selective attention is the net result of target selection and distractor suppression. The way in which both mechanisms are implemented neurally has remained contested. Neural oscillatory power in the alpha frequency band (ϳ10 Hz) has been implicated in the selection of to-be-attended targets, but there is lack of empirical evidence for its involvement in the suppression of to-be-ignored distractors. Here, we use electroencephalography recordings of N ϭ 33 human participants (males and females) to test the preregistered hypothesis that alpha power directly relates to distractor suppression and thus operates independently from target selection. In an auditory spatial pitch discrimination task, we modulated the location (left vs right) of either a target or a distractor tone sequence, while fixing the other in the front. When the distractor was fixed in the front, alpha power relatively decreased contralaterally to the target and increased ipsilaterally. Most importantly, when the target was fixed in the front, alpha lateralization reversed in direction for the suppression of distractors on the left versus right. These data show that target-selection-independent alpha power modulation is involved in distractor suppression. Although both lateralized alpha responses for selection and for suppression proved reliable, they were uncorrelated and distractor-related alpha power emerged from more anterior, frontal cortical regions. Lending functional significance to suppression-related alpha oscillations, alpha lateralization at the individual, single-trial level was predictive of behavioral accuracy. These results fuel a renewed look at neurobiological accounts of selection-independent suppressive filtering in attention.

In principle, selective attention is the net result of target selection and distractor suppression. The way in which both mechanisms are implemented neurally has remained contested. Neural oscillatory power in the alpha frequency band (~10 Hz) has been implicated in the selection of to-be-attended targets, but there is lack of empirical evidence for its involvement in the suppression of to-be-ignored distractors. Here, we use electroencephalography (EEG) recordings of N = 33 human participants (males and females) to test the pre-registered hypothesis that alpha power directly relates to distractor suppression and thus operates independently from target selection. In an auditory spatial pitch discrimination task, we modulated the location (left vs right) of either a target or a distractor tone sequence, while fixing the other in the front. When the distractor was fixed in the front, alpha power relatively decreased contralaterally to the target and increased ipsilaterally. Most importantly, when the target was fixed in the front, alpha lateralization reversed in direction for the suppression of distractors on the left versus right. These data show that target-selection–independent alpha power modulation is involved in distractor suppression. While both lateralized alpha responses for selection and for suppression proved reliable, they were uncorrelated and distractor-related alpha power emerged from more anterior, frontal cortical regions. Lending functional significance to suppression-related alpha oscillations, alpha lateralization at the individual, single-trial level was predictive of behavioral accuracy. These results fuel a renewed look at neurobiological accounts of selection-independent suppressive filtering in attention.Significance statementAlthough well-established models of attention rest on the assumption that irrelevant sensory information is filtered out, the neural implementation of such a filter mechanism is unclear. Using an auditory attention task that decouples target selection from distractor suppression, we demonstrate that two sign-reversed lateralized alpha responses reflect target selection versus distractor suppression. Critically, these alpha responses are reliable, independent of each other, and generated in more anterior, frontal regions for suppression versus selection. Prediction of single-trial task performance from alpha modulation after stimulus onset agrees with the view that alpha modulation bears direct functional relevance as a neural implementation of attention. Results demonstrate that the neurobiological foundation of attention implies a selection-independent alpha oscillatory mechanism to suppress distraction.

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.

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.

Speech comprehension in noisy, multi-talker situations poses a challenge. Human listeners differ substantially in the degree to which they adapt behaviorally and can listen successfully under such circumstances. How cortical networks embody this adaptation, particularly at the individual level, is currently unknown. We here explain this adaptation from reconfiguration of brain networks for a challenging listening task (i.e., a novel linguistic variant of the Posner paradigm with concurrent speech) in an age-varying sample of N = 49 healthy adults undergoing resting-state and task fMRI. We here provide evidence for the hypothesis that more successful listeners exhibit stronger task-specific reconfiguration, hence better adaptation, of brain networks. From rest to task, brain networks become reconfigured towards more localized cortical processing characterized by higher topological segregation. This reconfiguration is dominated by the functional division of an auditory and a cingulo-opercular module, and the emergence of a conjoined auditory and ventral attention module along bilateral middle and posterior temporal cortices. Supporting our hypothesis, the degree to which modularity of this fronto-temporal auditory-control network is increased relative to resting state predicts individuals’ listening success in states of divided and selective attention. Our findings elucidate how fine-tuned cortical communication dynamics shape selection and comprehension of speech. Our results highlight modularity of the auditory-control network as a key organizational principle in cortical implementation of auditory spatial attention in challenging listening situations.Significance StatementHow 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 spatial attention.