Malte Wöstmann

Adverse Listening Conditions and Memory Load Drive a Common Alpha Oscillatory Network

How does acoustic degradation affect the neural mechanisms of working memory? Enhanced alpha oscillations (8–13 Hz) during retention of items in working memory are often interpreted to reflect increased demands on storage and inhibition. We hypothesized that auditory signal degradation poses an additional challenge to human listeners partly because it draws on the same neural mechanisms. In an adapted Sternberg paradigm, auditory memory load and acoustic degradation were parametrically varied and the magnetoencephalographic response was analyzed in the time–frequency domain. Notably, during the stimulus-free delay interval, alpha power monotonically increased at central–parietal sensors as functions of memory load (higher alpha power with more memory load) and of acoustic degradation (also higher alpha power with more severe acoustic degradation). This alpha effect was superadditive when highest load was combined with most severe degradation. Moreover, alpha oscillatory dynamics during stimulus-free delay were predictive of response times to the probe item. Source localization of alpha power during stimulus-free delay indicated that alpha generators in right parietal, cingulate, supramarginal, and superior temporal cortex were sensitive to combined memory load and acoustic degradation. In summary, both challenges of memory load and acoustic degradation increase activity in a common alpha-frequency network. The results set the stage for future studies on how chronic or acute degradations of sensory input affect mechanisms of executive control.

Cortical alpha oscillations as a tool for auditory selective inhibition

Listening to speech is often demanding because of signal degradations and the presence of distracting sounds (i.e., “noise”). The question how the brain achieves the task of extracting only relevant information from the mixture of sounds reaching the ear (i.e., “cocktail party problem”) is still open. In analogy to recent findings in vision, we propose cortical alpha (~10 Hz) oscillations measurable using M/EEG as a pivotal mechanism to selectively inhibit the processing of noise to improve auditory selective attention to task-relevant signals. We review initial evidence of enhanced alpha activity in selective listening tasks, suggesting a significant role of alpha-modulated noise suppression in speech. We discuss the importance of dissociating between noise interference in the auditory periphery (i.e., energetic masking) and noise interference with more central cognitive aspects of speech processing (i.e., informational masking). Finally, we point out the adverse effects of age-related hearing loss and/or cognitive decline on auditory selective inhibition. With this perspective article, we set the stage for future studies on the inhibitory role of alpha oscillations for speech processing in challenging listening situations.

Neural alpha dynamics in younger and older listeners reflect acoustic challenges and predictive benefits

Speech comprehension in multitalker situations is a notorious real-life challenge, particularly for older listeners. Younger listeners exploit stimulus-inherent acoustic detail, but are they also actively predicting upcoming information? And further, how do older listeners deal with acoustic and predictive information? To understand the neural dynamics of listening difficulties and according listening strategies, we contrasted neural responses in the alpha-band (∼10 Hz) in younger (20–30 years, n = 18) and healthy older (60–70 years, n = 20) participants under changing task demands in a two-talker paradigm. Electroencephalograms were recorded while humans listened to two spoken digits against a distracting talker and decided whether the second digit was smaller or larger. Acoustic detail (temporal fine structure) and predictiveness (the degree to which the first digit predicted the second) varied orthogonally. Alpha power at widespread scalp sites decreased with increasing acoustic detail (during target digit presentation) but also with increasing predictiveness (in-between target digits). For older compared with younger listeners, acoustic detail had a stronger impact on task performance and alpha power modulation. This suggests that alpha dynamics plays an important role in the changes in listening behavior that occur with age. Last, alpha power variations resulting from stimulus manipulations (of acoustic detail and predictiveness) as well as task-independent overall alpha power were related to subjective listening effort. The present data show that alpha dynamics is a promising neural marker of individual difficulties as well as age-related changes in sensation, perception, and comprehension in complex communication situations.

Spatiotemporal dynamics of auditory attention synchronize with speech

Significance Attending and ignoring play fundamental roles in our everyday behavior in spatially and temporally fast-varying environments. Does focused attention to a specific stimulus adapt to these spatiotemporal dynamics? Using magnetoencephalography, we investigated the differential time courses of sensory encoding of two simultaneous, bottom-up rhythmic speech streams versus neural signatures of top-down spatial attention to one of the two streams. As expected, spatial attention modulated the power of ∼10-Hz (alpha) oscillations and their lateralization across the two cerebral hemispheres. Critically, this lateralization of alpha activity was modulated in temporal synchrony with the speech rate and predicted participants’ speech comprehension. Our results demonstrate that alpha activity acts as a spatiotemporal filter to control the read-out of attended and ignored sensory content. Attention plays a fundamental role in selectively processing stimuli in our environment despite distraction. Spatial attention induces increasing and decreasing power of neural alpha oscillations (8–12 Hz) in brain regions ipsilateral and contralateral to the locus of attention, respectively. This study tested whether the hemispheric lateralization of alpha power codes not just the spatial location but also the temporal structure of the stimulus. Participants attended to spoken digits presented to one ear and ignored tightly synchronized distracting digits presented to the other ear. In the magnetoencephalogram, spatial attention induced lateralization of alpha power in parietal, but notably also in auditory cortical regions. This alpha power lateralization was not maintained steadily but fluctuated in synchrony with the speech rate and lagged the time course of low-frequency (1–5 Hz) sensory synchronization. Higher amplitude of alpha power modulation at the speech rate was predictive of a listener’s enhanced performance of stream-specific speech comprehension. Our findings demonstrate that alpha power lateralization is modulated in tune with the sensory input and acts as a spatiotemporal filter controlling the read-out of sensory content.

Hearing loss impacts neural alpha oscillations under adverse listening conditions

Degradations in external, acoustic stimulation have long been suspected to increase the load on working memory (WM). One neural signature of WM load is enhanced power of alpha oscillations (6–12 Hz). However, it is unknown to what extent common internal, auditory degradation, that is, hearing impairment, affects the neural mechanisms of WM when audibility has been ensured via amplification. Using an adapted auditory Sternberg paradigm, we varied the orthogonal factors memory load and background noise level, while the electroencephalogram was recorded. In each trial, participants were presented with 2, 4, or 6 spoken digits embedded in one of three different levels of background noise. After a stimulus-free delay interval, participants indicated whether a probe digit had appeared in the sequence of digits. Participants were healthy older adults (62–86 years), with normal to moderately impaired hearing. Importantly, the background noise levels were individually adjusted and participants were wearing hearing aids to equalize audibility across participants. Irrespective of hearing loss (HL), behavioral performance improved with lower memory load and also with lower levels of background noise. Interestingly, the alpha power in the stimulus-free delay interval was dependent on the interplay between task demands (memory load and noise level) and HL; while alpha power increased with HL during low and intermediate levels of memory load and background noise, it dropped for participants with the relatively most severe HL under the highest memory load and background noise level. These findings suggest that adaptive neural mechanisms for coping with adverse listening conditions break down for higher degrees of HL, even when adequate hearing aid amplification is in place.

Acoustic detail guides attention allocation in a selective listening task

The flexible allocation of attention enables us to perceive and behave successfully despite irrelevant distractors. How do acoustic challenges influence this allocation of attention, and to what extent is this ability preserved in normally aging listeners? Younger and healthy older participants performed a masked auditory number comparison while EEG was recorded. To vary selective attention demands, we manipulated perceptual separability of spoken digits from a masking talker by varying acoustic detail (temporal fine structure). Listening conditions were adjusted individually to equalize stimulus audibility as well as the overall level of performance across participants. Accuracy increased, and response times decreased with more acoustic detail. The decrease in response times with more acoustic detail was stronger in the group of older participants. The onset of the distracting speech masker triggered a prominent contingent negative variation (CNV) in the EEG. Notably, CNV magnitude decreased parametrically with increasing acoustic detail in both age groups. Within identical levels of acoustic detail, larger CNV magnitude was associated with improved accuracy. Across age groups, neuropsychological markers further linked early CNV magnitude directly to individual attentional capacity. Results demonstrate for the first time that, in a demanding listening task, instantaneous acoustic conditions guide the allocation of attention. Second, such basic neural mechanisms of preparatory attention allocation seem preserved in healthy aging, despite impending sensory decline.

Tracking the signal, cracking the code: speech and speech comprehension in non-invasive human electrophysiology

ABSTRACT Magneto- and electroencephalographic (M/EEG) signals recorded from the human scalp have allowed for substantial advances for neural models of speech comprehension over the past decades. These methods are currently advancing rapidly and continue to offer unparalleled insight in the near-to-real-time neural dynamics of speech processing. We provide a historically informed overview over dependent measures in the time and frequency domain and highlight recent advances resulting from these measures. We discuss the notorious challenges (and solutions) speech and language researchers are faced with when studying auditory brain responses in M/EEG. We argue that a key to understanding the neural basis of speech comprehension will lie in studying interactions between the neural tracking of speech and the functional neural network dynamics. This article is intended for both, non-experts who want to learn how to use M/EEG to study speech comprehension and scholars aiming for an overview of state-of-the-art M/EEG analysis methods.

Acoustic Detail But Not Predictability of Task-Irrelevant Speech Disrupts Working Memory.

Attended speech is comprehended better not only if more acoustic detail is available, but also if it is semantically highly predictable. But can more acoustic detail or higher predictability turn into disadvantages and distract a listener if the speech signal is to be ignored? Also, does the degree of distraction increase for older listeners who typically show a decline in attentional control ability? Adopting the irrelevant-speech paradigm, we tested whether younger (age 23–33 years) and older (60–78 years) listeners’ working memory for the serial order of spoken digits would be disrupted by the presentation of task-irrelevant speech varying in its acoustic detail (using noise-vocoding) and its semantic predictability (of sentence endings). More acoustic detail, but not higher predictability, of task-irrelevant speech aggravated memory interference. This pattern of results did not differ between younger and older listeners, despite generally lower performance in older listeners. Our findings suggest that the focus of attention determines how acoustics and predictability affect the processing of speech: first, as more acoustic detail is known to enhance speech comprehension and memory for speech, we here demonstrate that more acoustic detail of ignored speech enhances the degree of distraction. Second, while higher predictability of attended speech is known to also enhance speech comprehension under acoustically adverse conditions, higher predictability of ignored speech is unable to exert any distracting effect upon working memory performance in younger or older listeners. These findings suggest that features that make attended speech easier to comprehend do not necessarily enhance distraction by ignored speech.

Large-scale network dynamics of beta-band oscillations underlie auditory perceptual decision-making

Perceptual decisions vary in the speed at which we make them. Evidence suggests that translating sensory information into perceptual decisions relies on distributed interacting neural populations, with decision speed hinging on power modulations of the neural oscillations. Yet the dependence of perceptual decisions on the large-scale network organization of coupled neural oscillations has remained elusive. We measured magnetoencephalographic signals in human listeners who judged acoustic stimuli composed of carefully titrated clouds of tone sweeps. These stimuli were used in two task contexts, in which the participants judged the overall pitch or direction of the tone sweeps. We traced the large-scale network dynamics of the source-projected neural oscillations on a trial-by-trial basis using power-envelope correlations and graph-theoretical network discovery. In both tasks, faster decisions were predicted by higher segregation and lower integration of coupled beta-band (∼16–28 Hz) oscillations. We also uncovered the brain network states that promoted faster decisions in either lower-order auditory or higher-order control brain areas. Specifically, decision speed in judging the tone sweep direction critically relied on the nodal network configurations of anterior temporal, cingulate, and middle frontal cortices. Our findings suggest that global network communication during perceptual decision-making is implemented in the human brain by large-scale couplings between beta-band neural oscillations. Author Summary The speed at which we make perceptual decisions varies. This translation of sensory information into perceptual decisions hinges on dynamic changes in neural oscillatory activity. However, the large-scale neural-network embodiment supporting perceptual decision-making is unclear. We addressed this question by experimenting two auditory perceptual decision-making situations. Using graph-theoretical network discovery, we traced the large-scale network dynamics of coupled neural oscillations to uncover the brain network states that support the speed of auditory perceptual decisions. We found that higher network segregation of coupled beta-band oscillations supports faster auditory perceptual decisions over trials. Moreover, when auditory perceptual decisions are relatively difficult, the decision speed benefits from higher segregation of frontal cortical areas, but lower segregation and greater integration of auditory cortical areas.

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 individuals 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 individuals 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.