Anna Wilsch

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.

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.

What works in auditory working memory? A neural oscillations perspective

Working memory is a limited resource: brains can only maintain small amounts of sensory input (memory load) over a brief period of time (memory decay). The dynamics of slow neural oscillations as recorded using magneto- and electroencephalography (M/EEG) provide a window into the neural mechanics of these limitations. Especially oscillations in the alpha range (8-13Hz) are a sensitive marker for memory load. Moreover, according to current models, the resultant working memory load is determined by the relative noise in the neural representation of maintained information. The auditory domain allows memory researchers to apply and test the concept of noise quite literally: Employing degraded stimulus acoustics increases memory load and, at the same time, allows assessing the cognitive resources required to process speech in noise in an ecologically valid and clinically relevant way. The present review first summarizes recent findings on neural oscillations, especially alpha power, and how they reflect memory load and memory decay in auditory working memory. The focus is specifically on memory load resulting from acoustic degradation. These findings are then contrasted with contextual factors that benefit neural as well as behavioral markers of memory performance, by reducing representational noise. We end on discussing the functional role of alpha power in auditory working memory and suggest extensions of the current methodological toolkit. This article is part of a Special Issue entitled SI: Auditory working memory.

Slow-delta phase concentration marks improved temporal expectations based on the passage of time

Temporal expectations enhance neural encoding precision, reflected in optimized alignment of slow neural oscillatory phase, and facilitate subsequent stimulus processing. If an events exact occurrence time is unknown, temporal expectations arise solely from the passage of time. Here, we show that this specific type of temporal expectation is also reflected in neural phase organization. While undergoing magnetoencephalography, participants performed an auditory-delayed matching-to-sample task with two syllables (S1, S2). Critically, S1-onset time varied in the 0.6-1.8-s (i.e., 0.6-1.7 Hz) range. Increasing S1-onset times led to increased slow-delta (0.6-0.9 Hz) phase coherence over right frontotemporal sensors during S1 encoding. Moreover, individuals with higher slow-delta coherence showed decreased alpha power (8-13 Hz) during subsequent memory retention. In sum, temporal expectations based on the passage of time optimize the precise alignment of neural oscillatory phase with an expected stimulus.

Transcranial alternating current stimulation with speech envelopes modulates speech comprehension

&NA; Cortical entrainment of the auditory cortex to the broadband temporal envelope of a speech signal is crucial for speech comprehension. Entrainment results in phases of high and low neural excitability, which structure and decode the incoming speech signal. Entrainment to speech is strongest in the theta frequency range (4–8 Hz), the average frequency of the speech envelope. If a speech signal is degraded, entrainment to the speech envelope is weaker and speech intelligibility declines. Besides perceptually evoked cortical entrainment, transcranial alternating current stimulation (tACS) entrains neural oscillations by applying an electric signal to the brain. Accordingly, tACS‐induced entrainment in auditory cortex has been shown to improve auditory perception. The aim of the current study was to modulate speech intelligibility externally by means of tACS such that the electric current corresponds to the envelope of the presented speech stream (i.e., envelope‐tACS). Participants performed the Oldenburg sentence test with sentences presented in noise in combination with envelope‐tACS. Critically, tACS was induced at time lags of 0–250 ms in 50‐ms steps relative to sentence onset (auditory stimuli were simultaneous to or preceded tACS). We performed single‐subject sinusoidal, linear, and quadratic fits to the sentence comprehension performance across the time lags. We could show that the sinusoidal fit described the modulation of sentence comprehension best. Importantly, the average frequency of the sinusoidal fit was 5.12 Hz, corresponding to the peaks of the amplitude spectrum of the stimulated envelopes. This finding was supported by a significant 5‐Hz peak in the average power spectrum of individual performance time series. Altogether, envelope‐tACS modulates intelligibility of speech in noise, presumably by enhancing and disrupting (time lag with in‐ or out‐of‐phase stimulation, respectively) cortical entrainment to the speech envelope in auditory cortex. HighlightsEnvelope‐tACS modulates entrainment to ongoing speech signal.Time lag between speech onset and auditory‐cortex response differs individually.Varying time lags between speech onset and tACS modulate comprehension sinusoidally.First evidence for possible clinical application of envelope‐tACS for hearing loss.

Envelope-tACS modulates intelligibility of speech in noise

Cortical entrainment of the auditory cortex to the broadband temporal envelope of a speech signal is crucial for speech comprehension. Entrainment results in phases of high and low neural excitability, which structure and decode the incoming speech signal. Entrainment to speech is strongest in the theta frequency range (4-8 Hz), the average frequency of the speech envelope. If a speech signal is degraded, entrainment to the speech envelope is weaker and speech intelligibility declines. Besides perceptually evoked cortical entrainment, transcranial alternating current stimulation (tACS) entrains neural oscillations by applying an electric signal to the brain. Accordingly, tACS-induced entrainment in auditory cortex has been shown to improve auditory perception. The aim of the current study was to modulate speech intelligibility externally by means of tACS such that the electric current corresponds to the envelope of the presented speech stream (i.e., envelope-tACS). Participants performed the Oldenburg sentence test with sentences presented in noise in combination with envelope-tACS. Critically, tACS was induced at time lags of 0 to 250 ms in 50-ms steps relative to sentence onset (auditory stimuli were simultaneous to or preceded tACS). We performed single-subject sinusoidal, linear, and quadratic fits to the sentence comprehension performance across the time lags. We could show that the sinusoidal fit described the modulation of sentence comprehension best. Importantly, the average frequency of the sinusoidal fit was 5.12 Hz, corresponding to the peaks of the amplitude spectrum of the stimulated envelopes. This finding was supported by a significant 5-Hz peak in the average power spectrum of individual performance time series. Altogether, envelope tACS modulates intelligibility of speech in noise, presumably by enhancing and disrupting (time lag with in- or out-of-phase stimulation, respectively) cortical entrainment to the speech envelope in auditory cortex.Cortical entrainment of the auditory cortex to the broad-band temporal envelope of a speech signal is crucial for speech comprehension. This entrainment results in phases of high and low neural excitability which structure and decode the incoming speech signal. Entrainment to speech is strongest in the theta frequency range (4–8 Hz), the average frequency of the speech envelope. If a speech signal is degraded, for example masked by irrelevant information such as noise, entrainment to the speech envelope is weaker and speech intelligibility declines. Besides perceptually evoked cortical entrainment, transcranial alternating current stimulation (tACS) can entrain neural oscillations by applying an electric signal to the brain. Accordingly, tACS-induced entrainment in auditory cortex has been shown to improve auditory perception. The aim of the current study was to externally modulate speech intelligibility by means of tACS such that the electric current corresponds to the envelope of the presented speech stream. Participants performed the Oldenburg sentence test with sentences presented in noise in combination with tACS. Critically, the time lag between sentence presentation and tACS was manipulated from 0 to 250 ms in 50-ms steps (auditory stimuli were simultaneous to or preceded tACS). First, we were able to show that envelope-tACS modulated sentence comprehension such that on average sentence comprehension at the time lag of the best performance was significantly better than sentence comprehension of the worst performance. Second, sentence comprehension across time lags was modulated sinusoidally. In sum, envelope tACS modulates intelligibility of speech in noise presumably by enhancing (time lag with in-phase stimulation) and disrupting (time lag with out-of-phase stimulation) cortical entrainment to the speech envelope in auditory cortex.

Temporal Expectation Modulates the Cortical Dynamics of Short-Term Memory

Increased memory load is often signified by enhanced neural oscillatory power in the alpha range (8–13 Hz), which is taken to reflect inhibition of task-irrelevant brain regions. The corresponding neural correlates of memory decay, however, are not yet well understood. In the current study, we investigated auditory short-term memory decay in humans using a delayed matching-to-sample task with pure-tone sequences. First, in a behavioral experiment, we modeled memory performance over six different delay-phase durations. Second, in a MEG experiment, we assessed alpha-power modulations over three different delay-phase durations. In both experiments, the temporal expectation for the to-be-remembered sound was manipulated so that it was either temporally expected or not. In both studies, memory performance declined over time, but this decline was weaker when the onset time of the to-be-remembered sound was expected. Similarly, patterns of alpha power in and alpha-tuned connectivity between sensory cortices changed parametrically with delay duration (i.e., decrease in occipitoparietal regions, increase in temporal regions). Temporal expectation not only counteracted alpha-power decline in heteromodal brain areas (i.e., supramarginal gyrus), but also had a beneficial effect on memory decay, counteracting memory performance decline. Correspondingly, temporal expectation also boosted alpha connectivity within attention networks known to play an active role during memory maintenance. The present data show how patterns of alpha power orchestrate short-term memory decay and encourage a more nuanced perspective on alpha power across brain space and time beyond its inhibitory role. SIGNIFICANCE STATEMENT Our sensory memories of the physical world fade quickly. We show here that this decay of short-term memory can be counteracted by so-called temporal expectation; that is, knowledge of when to expect a sensory event that an individual must remember. We also show that neural oscillations in the “alpha” (8–13 Hz) range index both the degree of memory decay (for brief sound patterns) and the respective memory benefit from temporal expectation. Spatially distributed cortical patterns of alpha power show opposing effects in auditory versus visual sensory cortices. Moreover, alpha-tuned connectivity changes within supramodal attention networks reflect the allocation of neural resources as short-term memory representations fade.

Temporal expectation modulates cortical dynamics of sensory memory

Increased memory load is often signified by enhanced neural oscillatory power in the alpha range (8–13 Hz), taken to reflect inhibition of task-irrelevant brain regions. The corresponding neural correlates of memory decay, however, are not yet well-understood. Here, we investigated auditory sensory memory decay using a delayed matching-to-sample task with pure-tone sequences. First, in a behavioral experiment we modeled memory behavior over six different delay-phase durations. Second, in a magnetoencephalography (MEG) experiment, we assessed alpha-power modulations over three different delay-phase durations. In both experiments, the temporal expectation for the to-be-remembered sound was manipulated, so that it was either temporally expected or not. In both studies, memory performance declined over time but this decline was less strong under a more precise temporal expectation. Similarly, patterns of alpha power in and alpha-tuned connectivity between sensory cortices changed parametrically with delay duration (i.e., decrease in occipito-parietal regions, increase in temporal regions). Notably, temporal expectation counteracted alpha-power decline in heteromodal brain areas (i.e., supramarginal gyrus), in line with its memory-decay counteracting effect on performance. Correspondingly, temporal expectation also boosted alpha connectivity within attention networks known to play an active role during memory maintenance. The present data outline how patterns of alpha power orchestrate sensory memory decay, and encourage a refined perspective on alpha power and its inhibitory role across brain space and time. Significance Statement Our sensory memories of the physical world fade quickly. We show here that this decay of sensory memory can be counteracted by so-called temporal expectation, that is, knowledge of when to expect the to-be-remembered sensory event (here, brief sound patterns). We also show that distinct patterns and modulations of neural oscillations in the “alpha” (8–13 Hz) range index both, the degree of memory decay, and any benefit from temporal expectation, both of which affect memory performance. Critically, spatially distributed cortical patterns of alpha power, with opposing effects in auditory vs. visual sensory cortices and alpha-tuned connectivity changes within supramodal attention networks, reflect the allocation of neural resources as sensory memory representations fade.