Target enhancement but not distractor suppression in auditory neural tracking during continuous speech.

Selective attention modulates the neural tracking of speech in auditory cortical regions. It is unclear whether this attentional modulation is dominated by enhanced target tracking, or suppression of distraction. To settle this long-standing debate, we employed an augmented electroencephalography (EEG) speech-tracking paradigm with target, distractor, and neutral streams. Concurrent target speech and distractor (i.e., sometimes relevant) speech were juxtaposed with a third, never task-relevant speech stream serving as neutral baseline. Listeners had to detect short target repeats and committed more false alarms originating from the distractor than from the neutral stream. Speech tracking revealed target enhancement but no distractor suppression below the neutral baseline. Speech tracking of the target (not distractor or neutral speech) explained single-trial accuracy in repeat detection. In sum, the enhanced neural representation of target speech is specific to processes of attentional gain for behaviorally relevant target speech rather than neural suppression of distraction.

Slow neural oscillations explain temporal fluctuations in distractibility.

Human environments comprise various sources of distraction, which often occur unexpectedly in time. The proneness to distraction (i.e., distractibility) is posited to be independent of attentional sampling of targets, but its temporal dynamics and neurobiological basis are largely unknown. Brain oscillations in the theta band (3 - 8 Hz) have been associated with fluctuating neural excitability, which is hypothesised here to explain rhythmic modulation of distractibility. In a pitch discrimination task (N = 30) with unexpected auditory distractors, we show that distractor-evoked neural responses in the electroencephalogram and perceptual susceptibility to distraction were co-modulated and cycled approximately 3 - 5 times per second. Pre-distractor neural phase in left inferior frontal and insular cortex regions explained fluctuating distractibility. Thus, human distractibility is not constant but fluctuates on a subsecond timescale. Furthermore, slow neural oscillations subserve the behavioural consequences of a hitherto largely unexplained but ever-increasing phenomenon in modern environments - distraction by unexpected sound.

Effects of temporally regular versus irregular distractors on goal-directed cognition and behavior.

Human environments comprise plenty of task-irrelevant sensory inputs, which are potentially distracting. Auditory distractors often possess an inherent temporal structure. However, it is largely unknown whether and how the temporal regularity of distractors interferes with goal-directed cognitive processes, such as working memory. Here, we tested a total sample of N = 90 participants across four working memory tasks with sequences of temporally regular versus irregular distractors. Temporal irregularity was operationalized by a final tone onset time that violated an otherwise regular tone sequence (Experiment 1), by a sequence of tones with irregular onset-to-onset delays (Experiment 2), and by sequences of speech items with irregular onset-to-onset delays (Experiments 3 and 4). Across all experiments, temporal regularity of distractors did not modulate participants' primary performance metric, that is, accuracy in recalling items from working memory. Instead, temporal regularity of distractors modulated secondary performance metrics: for regular versus irregular distractors, recall of the first item from memory was faster (Experiment 3) and the response bias was more conservative (Experiment 4). Taken together, the present results provide evidence that the temporal regularity of task-irrelevant input does not inevitably affect the precision of memory representations (reflected in the primary performance metric accuracy) but rather the response behavior (reflected in secondary performance metrics like response speed and bias). Our findings emphasize that a comprehensive understanding of auditory distraction requires that existing models of attention include often-neglected secondary performance metrics to understand how different features of auditory distraction reach awareness and impact cognition and behavior.

Ten simple rules to study distractor suppression.

Distractor suppression refers to the ability to filter out distracting and task-irrelevant information. Distractor suppression is essential for survival and considered a key aspect of selective attention. Despite the recent and rapidly evolving literature on distractor suppression, we still know little about how the brain suppresses distracting information. What limits progress is that we lack mutually agreed upon principles of how to study the neural basis of distractor suppression and its manifestation in behavior. Here, we offer ten simple rules that we believe are fundamental when investigating distractor suppression. We provide guidelines on how to design conclusive experiments on distractor suppression (Rules 1-3), discuss different types of distractor suppression that need to be distinguished (Rules 4-6), and provide an overview of models of distractor suppression and considerations of how to evaluate distractor suppression statistically (Rules 7-10). Together, these rules provide a concise and comprehensive synopsis of promising advances in the field of distractor suppression. Following these rules will propel research on distractor suppression in important ways, not only by highlighting prominent issues to both new and more advanced researchers in the field, but also by facilitating communication between sub-disciplines.

Target enhancement or distractor suppression? Functionally distinct alpha oscillations form the basis of attention.

Recent advances in attention research have been propelled by the debate on target enhancement versus distractor suppression. A predominant neural correlate of attention is the modulation of alpha oscillatory power (~10 Hz), which signifies shifts of attention in time, space and between sensory modalities. However, the underspecified functional role of alpha oscillations limits the progress of tracking down the neurocognitive basis of attention. In this short opinion article, we review and critically examine a synthesis of three conceptual and methodological aspects that are indispensable for a mechanistic understanding of the role of alpha oscillations for attention. (a) Precise mapping of the anatomical source and the temporal response profile of neural signals reveals distinct alpha oscillatory processes that implement facilitatory versus suppressive components of attention. (b) A testable framework enables unanimous association of alpha modulation with either target enhancement or different forms of distractor suppression (active vs. automatic). (c) Linking anatomically specified alpha oscillations to behavior reveals the causal nature of alpha oscillations for attention. The three reviewed aspects substantially enrich study design, data analysis and interpretation of results to achieve the goal of understanding how anatomically specified and functionally relevant neural oscillations contribute to the implementation of facilitatory versus suppressive components of attention.

Personality captures dissociations of subjective versus objective hearing in noise.

Acoustic noise is pervasive in human environments. Some individuals are more tolerant to noise than others. We demonstrate the explanatory potential of Big-5 personality traits neuroticism (being emotionally unstable) and extraversion (being enthusiastic, outgoing) on subjective self-report and objective psycho-acoustic metrics of hearing in noise in two samples (total N = 1103). Under statistical control for demographics and in agreement with pre-registered hypotheses, lower neuroticism and higher extraversion independently explained superior self-reported noise resistance, speech-hearing ability and acceptable background noise levels. Surprisingly, objective speech-in-noise recognition instead increased with higher levels of neuroticism. In turn, the bias in subjectively overrating one's own hearing in noise decreases with higher neuroticism but increases with higher extraversion. Of benefit to currently underspecified frameworks of hearing in noise and tailored audiological treatments, these results show that personality explains inter-individual differences in coping with acoustic noise, which is a ubiquitous source of distraction and a health hazard.

Unilateral Acoustic Degradation Delays Attentional Separation of Competing Speech.

Hearing loss is often asymmetric such that hearing thresholds differ substantially between the two ears. The extreme case of such asymmetric hearing is single-sided deafness. A unilateral cochlear implant (CI) on the more severely impaired ear is an effective treatment to restore hearing. The interactive effects of unilateral acoustic degradation and spatial attention to one sound source in multitalker situations are at present unclear. Here, we simulated some features of listening with a unilateral CI in young, normal-hearing listeners (N = 22) who were presented with 8-band noise-vocoded speech to one ear and intact speech to the other ear. Neural responses were recorded in the electroencephalogram to obtain the spectrotemporal response function to speech. Listeners made more mistakes when answering questions about vocoded (vs. intact) attended speech. At the neural level, we asked how unilateral acoustic degradation would impact the attention-induced amplification of tracking target versus distracting speech. Interestingly, unilateral degradation did not per se reduce the attention-induced amplification but instead delayed it in time: Speech encoding accuracy, modelled on the basis of the spectrotemporal response function, was significantly enhanced for attended versus ignored intact speech at earlier neural response latencies (<∼250 ms). This attentional enhancement was not absent but delayed for vocoded speech. These findings suggest that attentional selection of unilateral, degraded speech is feasible but induces delayed neural separation of competing speech, which might explain listening challenges experienced by unilateral CI users.

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 vulnerability of working memory to distraction is rhythmic.

Recent research posits that the cognitive system samples target stimuli in a rhythmic fashion, characterized by target detection fluctuating at frequencies of ~3-8 Hz. Besides prioritized encoding of targets, a key cognitive function is the protection of working memory from distractor intrusion. Here, we test to which degree the vulnerability of working memory to distraction is rhythmic. In an Irrelevant-Speech Task, N = 23 human participants had to retain the serial order of nine numbers in working memory while being distracted by task-irrelevant speech with variable temporal onsets. The magnitude of the distractor-evoked N1 component in the event-related potential as well as behavioural recall accuracy, both measures of memory distraction, were periodically modulated by distractor onset time in approximately 2-4 cycles per second (Hz). Critically, an underlying 2.5-Hz rhythm explained variation in both measures of distraction such that stronger phasic distractor encoding mediated lower phasic memory recall accuracy. In a behavioural follow-up experiment, we tested whether these results would replicate in a task design without rhythmic presentation of target items. Participants (N = 6 with on average >2500 trials, each) retained two line-figures in memory while being distracted by acoustic noise of varying onset across trials. In agreement with the main experiment, the temporal onset of the distractor periodically modulated memory performance. These results suggest that during working memory retention, the human cognitive system implements distractor suppression in a temporally dynamic fashion, reflected in ~400-ms long cycles of high versus low distractibility.

Does Closing the Eyes Enhance Auditory Attention? Eye Closure Increases Attentional Alpha-Power Modulation but Not Listening Performance.

In challenging listening conditions, closing the eyes is a strategy with intuitive appeal to improve auditory attention and perception. On the neural level, closing the eyes increases the power of alpha oscillations (∼10 Hz), which are a prime signature of auditory attention. Here, we test whether eye closure benefits neural and behavioral signatures of auditory attention and perception. Participants (n = 22) attended to one of two alternating streams of spoken numbers with open or closed eyes in a darkened chamber. After each trial, participants indicated whether probes had been among the to-be-attended or to-be-ignored numbers. In the EEG, states of relative high versus low alpha power accompanied the presentation of attended versus ignored numbers. Importantly, eye closure did not only increase the overall level of absolute alpha power but also the attentional modulation thereof. Behaviorally, however, neither perceptual sensitivity nor response criterion was affected by eye closure. To further examine whether this behavioral null result would conceptually replicate in a simple auditory detection task, a follow-up experiment was conducted that required participants (n = 19) to detect a near-threshold target tone in noise. As in the main experiment, our results provide evidence for the absence of any difference in perceptual sensitivity and criterion for open versus closed eyes. In summary, we demonstrate here that the modulation of the human alpha rhythm by auditory attention is increased when participants close their eyes. However, our results speak against the widely held belief that eye closure per se improves listening behavior.

Alpha Oscillations in the Human Brain Implement Distractor Suppression Independent of Target Selection.

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 recordings of N = 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.SIGNIFICANCE STATEMENT Although 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.

Working-memory disruption by task-irrelevant talkers depends on degree of talker familiarity.

When one is listening, familiarity with an attended talker's voice improves speech comprehension. Here, we instead investigated the effect of familiarity with a distracting talker. In an irrelevant-speech task, we assessed listeners' working memory for the serial order of spoken digits when a task-irrelevant, distracting sentence was produced by either a familiar or an unfamiliar talker (with rare omissions of the task-irrelevant sentence). We tested two groups of listeners using the same experimental procedure. The first group were undergraduate psychology students (N = 66) who had attended an introductory statistics course. Critically, each student had been taught by one of two course instructors, whose voices served as the familiar and unfamiliar task-irrelevant talkers. The second group of listeners were family members and friends (N = 20) who had known either one of the two talkers for more than 10 years. Students, but not family members and friends, made more errors when the task-irrelevant talker was familiar versus unfamiliar. Interestingly, the effect of talker familiarity was not modulated by the presence of task-irrelevant speech: Students experienced stronger working memory disruption by a familiar talker, irrespective of whether they heard a task-irrelevant sentence during memory retention or merely expected it. While previous work has shown that familiarity with an attended talker benefits speech comprehension, our findings indicate that familiarity with an ignored talker disrupts working memory for target speech. The absence of this effect in family members and friends suggests that the degree of familiarity modulates the memory disruption.

Prestimulus neural alpha power predicts confidence in discriminating identical auditory stimuli.

When deciding upon a sensory stimulus, the power of prestimulus neural alpha oscillations (~10 Hz) has been shown to hold information on a perceiver's bias, or confidence, as opposed to perceptual sensitivity per se. Here, we test whether this link between prestimulus alpha power and decision confidence, previously established in vision and somatosensation, also holds in the auditory modality. Moreover, confidence usually depends on the physical evidence available in the stimulus as well as on decision accuracy. It is unclear in how far the link between prestimulus alpha power and confidence holds when physical stimulus evidence is entirely absent, and thus accuracy does not vary. We here analysed electroencephalography data from a paradigm where human listeners (N = 17) rated their confidence in the discrimination of the pitch of two tones that were, unbeknownst to the listeners, identical. Lower prestimulus alpha power as recorded at central channel sites was predictive of higher confidence ratings. Furthermore, this link was not mediated by auditory evoked activity. Our results support a direct link between prestimulus alpha power and decision confidence. This effect, first, shows up in the auditory modality similar to vision and somatosensation, and second, is present also in the complete absence of physical evidence in the stimulus and in the absence of varying accuracy. These findings speak to a model wherein low prestimulus alpha power increases neural baseline excitability, which is reflected in enhanced stimulus-evoked neural responses and higher confidence.

Late cortical tracking of ignored speech facilitates neural selectivity in acoustically challenging conditions.

Listening requires selective neural processing of the incoming sound mixture, which in humans is borne out by a surprisingly clean representation of attended-only speech in auditory cortex. How this neural selectivity is achieved even at negative signal-to-noise ratios (SNR) remains unclear. We show that, under such conditions, a late cortical representation (i.e., neural tracking) of the ignored acoustic signal is key to successful separation of attended and distracting talkers (i.e., neural selectivity). We recorded and modeled the electroencephalographic response of 18 participants who attended to one of two simultaneously presented stories, while the SNR between the two talkers varied dynamically between +6 and -6 dB. The neural tracking showed an increasing early-to-late attention-biased selectivity. Importantly, acoustically dominant (i.e., louder) ignored talkers were tracked neurally by late involvement of fronto-parietal regions, which contributed to enhanced neural selectivity. This neural selectivity, by way of representing the ignored talker, poses a mechanistic neural account of attention under real-life acoustic conditions.

Opposite effects of lateralised transcranial alpha versus gamma stimulation on auditory spatial attention.

BACKGROUND: Spatial attention relatively increases the power of neural 10-Hz alpha oscillations in the hemisphere ipsilateral to attention, and decreases alpha power in the contralateral hemisphere. For gamma oscillations (>40 Hz), the opposite effect has been observed. The functional roles of lateralised oscillations for attention are currently unclear. HYPOTHESIS: If lateralised oscillations are functionally relevant for attention, transcranial stimulation of alpha versus gamma oscillations in one hemisphere should differentially modulate the accuracy of spatial attention to the ipsi-versus contralateral side. METHODS: 20 human participants performed a dichotic listening task under continuous transcranial alternating current stimulation (tACS, vs sham) at alpha (10 Hz) or gamma (47 Hz) frequency. On each trial, participants attended to four spoken numbers on the left or right ear, while ignoring numbers on the other ear. In order to stimulate a left temporo-parietal cortex region, which is known to show marked modulations of alpha power during auditory spatial attention, tACS (1 mA peak-to-peak amplitude) was applied at electrode positions TP7 and FC5 over the left hemisphere. RESULTS: As predicted, unihemispheric alpha-tACS relatively decreased the recall of targets contralateral to stimulation, but increased recall of ipsilateral targets. Importantly, this spatial pattern of results was reversed for gamma-tACS. CONCLUSIONS: Results provide a proof of concept that transcranially stimulated oscillations can enhance spatial attention and facilitate attentional selection of speech. Furthermore, opposite effects of alpha versus gamma stimulation support the view that states of high alpha are incommensurate with active neural processing as reflected by states of high gamma.

The Benefit of Attention-to-Memory Depends on the Interplay of Memory Capacity and Memory Load.

Humans can be cued to attend to an item in memory, which facilitates and enhances the perceptual precision in recalling this item. Here, we demonstrate that this facilitating effect of attention-to-memory hinges on the overall degree of memory load. The benefit an individual draws from attention-to-memory depends on her overall working memory performance, measured as sensitivity (d') in a retroactive cue (retro-cue) pitch discrimination task. While listeners maintained 2, 4, or 6 auditory syllables in memory, we provided valid or neutral retro-cues to direct listeners' attention to one, to-be-probed syllable in memory. Participants' overall memory performance (i.e., perceptual sensitivity d') was relatively unaffected by the presence of valid retro-cues across memory loads. However, a more fine-grained analysis using psychophysical modeling shows that valid retro-cues elicited faster pitch-change judgments and improved perceptual precision. Importantly, as memory load increased, listeners' overall working memory performance correlated with inter-individual differences in the degree to which precision improved (r = 0.39, p = 0.029). Under high load, individuals with low working memory profited least from attention-to-memory. Our results demonstrate that retrospective attention enhances perceptual precision of attended items in memory but listeners' optimal use of informative cues depends on their overall memory abilities.

Alpha-gamma phase amplitude coupling subserves information transfer during perceptual sequence learning.

Cross-frequency coupling is suggested to serve transfer of information between wide-spread neuronal assemblies and has been shown to underlie many cognitive functions including learning and memory. In previous work, we found that alpha (8-13 Hz) - gamma (30-48 Hz) phase amplitude coupling (αγPAC) is decreased during sequence learning in bilateral frontal cortex and right parietal cortex. We interpreted this to reflect decreased demands for visuo-motor mapping once the sequence has been encoded. In the present study, we put this hypothesis to the test by adding a "simple" condition to the standard serial reaction time task (SRTT) with minimal needs for visuo-motor mapping. The standard SRTT in our paradigm entailed a perceptual sequence allowing for implicit learning of a sequence of colors with randomly assigned motor responses. Sequence learning in this case was thus not associated with reduced demands for visuo-motor mapping. Analysis of oscillatory power revealed a learning-related alpha decrease pointing to a stronger recruitment of occipito-parietal areas when encoding the perceptual sequence. Replicating our previous findings but in contrast to our hypothesis, αγPAC was decreased in sequence compared to random trials over right frontal and parietal cortex. It also tended to be smaller compared to trials requiring a simple motor sequence. We additionally analyzed αγPAC in resting-state data of a separate cohort. PAC in electrodes over right parietal cortex was significantly stronger compared to sequence trials and tended to be higher compared to simple and random trials of the SRTT data. We suggest that αγPAC in right parietal cortex reflects a "default-mode" brain state, which gets perturbed to allow for encoding of visual regularities into memory.

Probing the limits of alpha power lateralisation as a neural marker of selective attention in middle-aged and older listeners.

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.

States and traits of neural irregularity in the age-varying human brain.

Sensory representations, and thus human percepts, of the physical world are susceptible to fluctuations in brain state or "neural irregularity". Furthermore, aging brains display altered levels of neural irregularity. We here show that a single, within-trial, information-theoretic measure (weighted permutation entropy) captures neural irregularity in the human electroencephalogram as a proxy for both, trait-like differences between individuals of varying age, and state-like fluctuations that bias perceptual decisions. First, the overall level of neural irregularity increased with participants' age, paralleled by a decrease in variability over time, likely indexing age-related changes at structural and functional levels of brain activity. Second, states of higher neural irregularity were associated with optimized sensory encoding and a subsequently increased probability of choosing the first of two physically identical stimuli to be higher in pitch. In sum, neural irregularity not only characterizes behaviourally relevant brain states, but also can identify trait-like changes that come with age.