Auditory Cortical Processing Research Articles

Cortical ensemble activity discriminates auditory attentional states

Selective attention modulates sensory cortical activity. It remains unclear how auditory cortical activity represents stimuli that differ behaviorally. We designed a cross-modality task in which mice made decisions to obtain rewards based on attended visual or auditory stimuli. We recorded auditory cortical activity in behaving mice attending to, ignoring, or passively hearing auditory stimuli. Engaging in the task bidirectionally modulates neuronal responses to the auditory stimuli in both the attended and ignored conditions compared to passive hearing. Neuronal ensemble activity in response to stimuli under attended, ignored and passive conditions are readily distinguishable. Furthermore, ensemble activity under attended and ignored conditions are in closer states compared to passive condition, and they share a component of attentional modulation which drives them to the same direction in the population activity space. Our findings suggest that the ignored condition is very different from the passive condition, and the auditory cortical sensory processing under ignored, attended and passive conditions are modulated differently.

The impact of when, what and how predictions on auditory speech perception.

An impressive number of theoretical proposals and neurobiological studies argue that perceptual processing is not strictly feedforward but rather operates through an interplay between bottom-up sensory and top-down predictive mechanisms. The present EEG study aimed to further determine how prior knowledge on auditory syllables may impact speech perception. Prior knowledge was manipulated by presenting the participants with visual information indicative of the syllable onset (when), its phonetic content (what) and/or its articulatory features (how). While when and what predictions consisted of unnatural visual cues (i.e., a visual timeline and a visuo-orthographic cue), how prediction consisted of the visual movements of a speaker. During auditory speech perception, when and what predictions both attenuated the amplitude of N1/P2 auditory evoked potentials. Regarding how prediction, not only an amplitude decrease but also a latency facilitation of N1/P2 auditory evoked potentials were observed during audiovisual compared to unimodal speech perception. However, when and what predictability effects were then reduced or abolished, with only what prediction reducing P2 amplitude but increasing latency. Altogether, these results demonstrate the influence of when, what and how visually induced predictions at an early stage on cortical auditory speech processing. Crucially, they indicate a preponderant predictive role of the speaker's articulatory gestures during audiovisual speech perception, likely driven by attentional load and focus.

Auditory Cortical Temporal Processing and Hemispheric Asymmetry Revealed by N1 Dipole Source Activity in Adult Cochlear Implant Users

Auditory Cortical Temporal Processing and Hemispheric Asymmetry Revealed by N1 Dipole Source Activity in Adult Cochlear Implant Users

Cortical encoding of speech enhances task-relevant acoustic information.

Speech is the most important signal in our auditory environment, and the processing of speech is highly dependent on context. However, it is unknown how contextual demands influence the neural encoding of speech. Here, we examine the context dependence of auditory cortical mechanisms for speech encoding at the level of the representation of fundamental acoustic features (spectrotemporal modulations) using model-based functional magnetic resonance imaging. We found that the performance of different tasks on identical speech sounds leads to neural enhancement of the acoustic features in the stimuli that are critically relevant to task performance. These task effects were observed at the earliest stages of auditory cortical processing, in line with interactive accounts of speech processing. Our work provides important insights into the mechanisms that underlie the processing of contextually relevant acoustic information within our rich and dynamic auditory environment.

Cortical Pitch Response Components Correlate with the Pitch Salience of Resolved and Unresolved components of Mandarin Tones.

Cortical pitch responses (CPRs) are generated at the initiation of pitch-bearing sounds. CPR components have been shown to reflect the pitch salience of iterated rippled noise with different temporal periodicity. However, it is unclear whether features of the CPR correlate with the pitch salience of resolved and unresolved harmonics of speech when the temporal periodicity is identical, and whether CPRs could be a neural index for auditory cortical pitch processing. In this study, CPRs were recorded to two speech sounds: a set including only resolved harmonics and a set including only unresolved harmonics. Speech-shaped noise preceding and following the speech was used to temporally discriminate the neural activity coding the onset of acoustic energy from the onset of time-varying pitch. Analysis of CPR peak latency and peak amplitude (Na) showed that the peak latency to speech sounds with only resolved harmonics was significantly shorter than for sounds with unresolved harmonics (p = 0.01), and that peak amplitude to sounds with only resolved harmonics was significantly higher than for sounds with unresolved harmonics (p <; 0.001). Further, the CPR peak phase locking value in response to sounds with only resolved harmonics was significantly higher than to sounds with only unresolved harmonics (p <; 0.001). Our findings suggest that the CPR changes with pitch salience and that CPR is a potentially useful indicator of auditory cortical pitch processing.

Evolutionary Elongation of the Time Window of Integration in Auditory Cortex: Macaque vs. Human Comparison of the Effects of Sound Duration on Auditory Evoked Potentials.

The auditory cortex integrates auditory information over time to obtain neural representations of sound events, the time scale of which critically affects perception. This work investigated the species differences in the time scale of integration by comparing humans and monkeys regarding how their scalp-recorded cortical auditory evoked potentials (CAEPs) decrease in amplitude as stimulus duration is shortened from 100 ms (or longer) to 2 ms. Cortical circuits tuned to processing sounds at short time scales would continue to produce large CAEPs to brief sounds whereas those tuned to longer time scales would produce diminished responses. Four peaks were identified in the CAEPs and labeled P1, N1, P2, and N2 in humans and mP1, mN1, mP2, and mN2 in monkeys. In humans, the N1 diminished in amplitude as sound duration was decreased, consistent with the previously described temporal integration window of N1 (>50 ms). In macaques, by contrast, the mN1 was unaffected by sound duration, and it was clearly elicited by even the briefest sounds. Brief sounds also elicited significant mN2 in the macaque, but not the human N2. Regarding earlier latencies, both P1 (humans) and mP1 (macaques) were elicited at their full amplitudes even by the briefest sounds. These findings suggest an elongation of the time scale of late stages of human auditory cortical processing, as reflected by N1/mN1 and later CAEP components. Longer time scales of integration would allow neural representations of complex auditory features that characterize speech and music.

Early and late auditory information processing show opposing deviations in aniridia

Aniridia is a congenital disorder, predominantly caused by heterozygous mutations of the PAX6 gene. While ocular defects have been extensively characterized in this population, brain-related anatomical and functional abnormalities are emerging as a prominent feature of the disorder. Individuals with aniridia frequently exhibit auditory processing deficits despite normal audiograms. While previous studies have reported hypoplasia of the anterior commissure and corpus callosum in some of these individuals, the neurophysiological basis of these impairments remains unexplored. This study provides direct assessment of neural activity related to auditory processing in aniridia. Participants were presented with tones designed to elicit an auditory steady-state response (ASSR) at 22 Hz, 40 Hz, and 84 Hz, and infrequent broadband target tones to maintain attention during electroencephalography (EEG) recording. Persons with aniridia showed increased early cortical responses (P50 AEP) in response to all tones, and increased high-frequency oscillatory entrainment (84 Hz ASSR). In contrast, this group showed a decreased cortical integration response (P300 AEP to target tones) and reduced neural entrainment to cortical beta-band stimuli (22 Hz ASSR). Collectively, our results suggest that subcortical and early cortical auditory processing is augmented in aniridia, while functional cortical integration of auditory information is deficient in this population.

Distilling the essence of TMS-evoked EEG potentials (TEPs): A call for securing mechanistic specificity and experimental rigor

Distilling the essence of TMS-evoked EEG potentials (TEPs): A call for securing mechanistic specificity and experimental rigor

Interaction Between Cortical Auditory Processing and Vagal Regulation of Heart Rate in Language Tasks: A Randomized, Prospective, Observational, Analytical and Cross-Sectional Study

Cortical auditory evoked potentials (CAEP) throughout a language task is beneficial during psychophysiological evaluation to advance identification of language disorders. So as to better comprehend human communication and to provide additional elements for neuropsychological examinations we aimed to (1) examine the influence of language tasks on cortical auditory processing and vagal control of heart rate and (2) to verify a possible association between the parasympathetic cardiac regulation and cortical auditory processing in language tasks. This study was completed with 49 women. The subjects were separated into two groups: (1) phonological language tasks (N = 21) and (2) semantic (N = 21) language tasks. Heart rate variability (HRV) and CAEP were evaluated before and after the tests. HRV reduced (small effect size) and P3 wave latency increased after the phonological task. Identical variables were significantly correlated after the phonological task and linear regression indicated significant interaction between pNN50 (percentage of adjacent RR intervals with a difference of duration greater than 50 milliseconds) and P3 latency (16.9%). In conclusion, phonological language tasks slightly reduced parasympathetic control of HR and increased cognitive effort. The association between HRV and CAEP are anticipated to be involved in this mechanism.

Auditory brain oscillatory responses in drug-naïve patients with Parkinson’s disease

Parkinson’s Disease (PD) is a common neurodegenerative disorder affecting the function of dopaminergic cells in basal ganglia. Besides the motor symptoms, tremor, and dysfunction of sensory systems. In the literature, there was limited studies which investigates the basic sensorial processing in PD. Therefore, we aimed to establish the sensorial processing of simple auditory stimulations in naïve PD comparing to healthy controls (HC) via delta, theta, and alpha brain oscillatory responses. 12 naïve PD and 12 HC participated to the study. Brain responses recorded via the 64-channel electroencephalography (EEG) system in an electromagnetically and acoustically isolated room. The auditory stimuli (1500 Hz, 60 dB SPL, 500 ms) were delivered to the subjects via a headphone. The inter-stimulus interval was ranged between 2.5–4.5 s. The peak-to-peak maximum amplitudes were measured in the delta, theta and alpha frequency bands on 11 electrodes (including the frontal, central and parietal areas) for the statistical analysis in which one-way ANOVA test was employed for the comparisons between PD and HC. For the delta oscillatory responses, PD group has bigger amplitudes in frontal, central and parietal areas in comparison with HC. For the theta and alpha oscillatory responses, PD group has bigger amplitudes in parietal areas in comparison with HC. As a result, amplitudes of brain oscillatory responses in PD group were significantly bigger than the HC. In this context, decreased inhibitory mechanisms of cortical auditory processing due to the dysfunction of the dopaminergic activity may lead the increased evoked responses in PD group.

Homology and Specificity of Natural Sound-Encoding in Human and Monkey Auditory Cortex.

Understanding homologies and differences in auditory cortical processing in human and nonhuman primates is an essential step in elucidating the neurobiology of speech and language. Using fMRI responses to natural sounds, we investigated the representation of multiple acoustic features in auditory cortex of awake macaques and humans. Comparative analyses revealed homologous large-scale topographies not only for frequency but also for temporal and spectral modulations. In both species, posterior regions preferably encoded relatively fast temporal and coarse spectral information, whereas anterior regions encoded slow temporal and fine spectral modulations. Conversely, we observed a striking interspecies difference in cortical sensitivity to temporal modulations: While decoding from macaque auditory cortex was most accurate at fast rates (> 30 Hz), humans had highest sensitivity to ~3 Hz, a relevant rate for speech analysis. These findings suggest that characteristic tuning of human auditory cortex to slow temporal modulations is unique and may have emerged as a critical step in the evolution of speech and language.

Auditory P300 in Noise in Younger and Older Adults.

Older adults often report difficulty hearing in background noise which is not completely attributable to peripheral hearing loss. Although age-related declines in cognition and hearing in background noise occur, the underlying age-related changes in processing of auditory stimuli in background noise has yet to be fully understood. The auditory P300 has the potential to elucidate the effects of age on auditory and cognitive processing of stimuli in background noise, but additional research is warranted. The purpose of this study was to investigate age-related differences in cognitive processing of auditory stimuli by evoking the auditory P300 at multiple signal-to-noise ratios (SNRs). A two-group, repeated measures study design was used. A convenience sample of 35 participants, 15 older adults (mean age of 66.4 yr) and 20 younger adults (mean age of 21.1 yr), participated in the study. All participants had negative otologic and neurological histories. The auditory P300 was evoked using an oddball paradigm with 500 (frequent) and 1000 Hz (target) tonal stimuli in quiet and in the presence of background noise at +20, +10, and 0 SNRs. P300 amplitudes and latencies were measured in each condition for every participant. Repeated measures analyses of variance were conducted for the amplitude and latency measures of the P300 for each group. Results from this study demonstrated P300 latencies were significantly longer in older adults in noise at the most challenging condition (0 SNR) compared with the quiet condition and between the +10 SNR and 0 SNR conditions. Although older adults had significantly longer P300 latencies compared with younger adults, no significant group by listening condition interaction existed. No significant P300 amplitude differences were found for group, noise, or group × listening condition interactions. Results provide evidence that auditory cortical processing, regardless of age, is poorer at more difficult SNRs. However, results also demonstrate that older adults perform significantly poorer than younger adults. This supports the notion that some degree of age-related decline in synchronous firing and rate of transmission of the auditory cortical neurons contributing to the auditory P300 exists. Studies are needed to further understand the impact of noise on auditory cortical processing across populations.

Recent advances in understanding the auditory cortex.

Our ability to make sense of the auditory world results from neural processing that begins in the ear, goes through multiple subcortical areas, and continues in the cortex. The specific contribution of the auditory cortex to this chain of processing is far from understood. Although many of the properties of neurons in the auditory cortex resemble those of subcortical neurons, they show somewhat more complex selectivity for sound features, which is likely to be important for the analysis of natural sounds, such as speech, in real-life listening conditions. Furthermore, recent work has shown that auditory cortical processing is highly context-dependent, integrates auditory inputs with other sensory and motor signals, depends on experience, and is shaped by cognitive demands, such as attention. Thus, in addition to being the locus for more complex sound selectivity, the auditory cortex is increasingly understood to be an integral part of the network of brain regions responsible for prediction, auditory perceptual decision-making, and learning. In this review, we focus on three key areas that are contributing to this understanding: the sound features that are preferentially represented by cortical neurons, the spatial organization of those preferences, and the cognitive roles of the auditory cortex.

Active Sound Localization Sharpens Spatial Tuning in Human Primary Auditory Cortex.

Spatial hearing sensitivity in humans is dynamic and task-dependent, but the mechanisms in human auditory cortex that enable dynamic sound location encoding remain unclear. Using functional magnetic resonance imaging (fMRI), we assessed how active behavior affects encoding of sound location (azimuth) in primary auditory cortical areas and planum temporale (PT). According to the hierarchical model of auditory processing and cortical functional specialization, PT is implicated in sound location ("where") processing. Yet, our results show that spatial tuning profiles in primary auditory cortical areas (left primary core and right caudo-medial belt) sharpened during a sound localization ("where") task compared with a sound identification ("what") task. In contrast, spatial tuning in PT was sharp but did not vary with task performance. We further applied a population pattern decoder to the measured fMRI activity patterns, which confirmed the task-dependent effects in the left core: sound location estimates from fMRI patterns measured during active sound localization were most accurate. In PT, decoding accuracy was not modulated by task performance. These results indicate that changes of population activity in human primary auditory areas reflect dynamic and task-dependent processing of sound location. As such, our findings suggest that the hierarchical model of auditory processing may need to be revised to include an interaction between primary and functionally specialized areas depending on behavioral requirements.SIGNIFICANCE STATEMENT According to a purely hierarchical view, cortical auditory processing consists of a series of analysis stages from sensory (acoustic) processing in primary auditory cortex to specialized processing in higher-order areas. Posterior-dorsal cortical auditory areas, planum temporale (PT) in humans, are considered to be functionally specialized for spatial processing. However, this model is based mostly on passive listening studies. Our results provide compelling evidence that active behavior (sound localization) sharpens spatial selectivity in primary auditory cortex, whereas spatial tuning in functionally specialized areas (PT) is narrow but task-invariant. These findings suggest that the hierarchical view of cortical functional specialization needs to be extended: our data indicate that active behavior involves feedback projections from higher-order regions to primary auditory cortex.

Attentional rather than sensory differences characterize auditory processing in Williams syndrome

Individuals with Williams Syndrome (WS) exhibit an atypical auditory profile. Across two experiments, we used event-related potentials (ERPs) in a three-stimulus auditory oddball task to examine early sensory (P1, N1, P2) and later cognitive (P3a, P3b) stages of cortical auditory processing in adults with WS and age-matched typical peers. In Study 1, piano chords served as standard, target, and novel stimuli; whereas, in Study 2, a variety of non-piano sounds comprised the novel stimuli. Across both experiments, there were no group differences in the earliest stages of sensory encoding (P1, N1), along with evidence for atypically large P2 responses in participants with WS. Persons with WS exhibited larger than typical P3a responses when the novel stimuli were perceptually distinct from the standard and the target stimuli (Study 2), but not when task-relevant and -irrelevant stimuli were perceptually similar (Study 1). Further, the WS group demonstrated reduced goal-directed attention (attenuated P3b response). These group differences in ERPs were not directly related to IQ. Our results in the context of an active discrimination task point to a more complex profile of auditory processing in persons with WS than previously reported, with group differences emerging during the later stages of stimulus categorization and evaluation, but not within early stimulus detection and feature encoding.

Distortion and Western Music Chord Processing

Guitar distortion used in rock music modifies a chord so that new frequencies appear in its harmonic structure. A distorted dyad (power chord) has a special role in heavy metal music due to its harmonics that create a major third interval, making it similar to a major chord. We investigated how distortion affects cortical auditory processing of chords in musicians and nonmusicians. Electric guitar chords with or without distortion and with or without the interval of the major third (i.e., triads or dyads) were presented in an oddball design where one of them served as a repeating standard stimulus and others served as occasional deviants. This enabled the recording of event-related potentials (ERPs) of the electroencephalogram (EEG) related to deviance processing (the mismatch negativity MMN and the attention-related P3a component) in an ignore condition. MMN and P3a responses were elicited in most paradigms. Distorted chords in a nondistorted context only elicited early P3a responses. However, the power chord did not demonstrate a special role in the level of the ERPs. Earlier and larger MMN and P3a responses were elicited when distortion was modified compared to when only harmony (triad vs. dyad) was modified between standards and deviants. The MMN responses were largest when distortion and harmony deviated simultaneously. Musicians demonstrated larger P3a responses than nonmusicians. The results suggest mostly independent cortical auditory processing of distortion and harmony in Western individuals, and facilitated chord change processing in musicians compared to nonmusicians. While distortion has been used in heavy rock music for decades, this study is among the first ones to shed light on its cortical basis.

Differences in Click and Speech Auditory Brainstem Responses and Cortical Response Patterns: A Pilot Study

Hearing loss has adverse developmental, cognitive and social impacts on individual’s lives. To improve its diagnosis and remediation outcomes, development of objective hearing methods offer new ways of optimizing care strategy. Complementary to the classical click-evoked brainstem and cortical responses, interest grows regarding the speech auditory brainstem responses, whose components, namely the onset and frequency following responses, are proposed as biomarkers of speech encoding at the brainstem level. To improve the understanding of auditory processing in the human brainstem and its effect on cortical processing, we used a multimodal set-up and recorded brainstem and cortical potentials in response to click stimuli and speech stimuli presented at different stimulation intensities in normal hearing adults. We hypothesized that even though click- and onset responses of the speechauditory brainstem responses share some similarities; their underlying mechanisms are in some point distinct. We also presumed that using a noninvasive method we could assess the generators underlying click, onset and frequency following responses and the time wise influence of brainstem encoding on cortical processing of click and speech stimuli. Results showed evidence regarding mechanisms underlying onset response and frequency following response components at the brainstem level. A direct time wise relationship between subcortical encoding and cortical encoding was revealed: cortical activity in the left cortex was related to the onset response latency at the brainstem level. These results highlight the potential use of new methods in speech processing electroencephalographic studies and provide qualitative and topographical data regarding subcortical and cortical auditory processing network.

Musical Expectations Enhance Auditory Cortical Processing in Musicians: A Magnetoencephalography Study

The present study investigated the influence of musical expectations on auditory representations in musicians and non-musicians using magnetoencephalography (MEG). Neuroscientific studies have demonstrated that musical syntax is processed in the inferior frontal gyri, eliciting an early right anterior negativity (ERAN), and anatomical evidence has shown that interconnections occur between the frontal cortex and the belt and parabelt regions in the auditory cortex (AC). Therefore, we anticipated that musical expectations would mediate neural activities in the AC via an efferent pathway. To test this hypothesis, we measured the auditory-evoked fields (AEFs) of seven musicians and seven non-musicians while they were listening to a five-chord progression in which the expectancy of the third chord was manipulated (highly expected, less expected, and unexpected). The results revealed that highly expected chords elicited shorter N1m (negative AEF at approximately 100 ms) and P2m (positive AEF at approximately 200 ms) latencies and larger P2m amplitudes in the AC than less-expected and unexpected chords. The relations between P2m amplitudes/latencies and harmonic expectations were similar between the groups; however, musicians’ results were more remarkable than those of non-musicians. These findings suggest that auditory cortical processing is enhanced by musical knowledge and long-term training in a top-down manner, which is reflected in shortened N1m and P2m latencies and enhanced P2m amplitudes in the AC.

Amplitude modulation rate dependent topographic organization of the auditory steady-state response in human auditory cortex

Periodic modulations of an acoustic feature, such as amplitude over a certain frequency range, leads to phase locking of neural responses to the envelope of the modulation. Using electrophysiological methods this neural activity pattern, also called the auditory steady-state response (aSSR), is visible following frequency transformation of the evoked response as a clear spectral peak at the modulation frequency. Despite several studies employing the aSSR that show, for example, strongest responses for ∼40 Hz and an overall right-hemispheric dominance, it has not been investigated so far to what extent within auditory cortex different modulation frequencies elicit aSSRs at a homogenous source or whether the localization of the aSSR is topographically organized in a systematic manner. The latter would be suggested by previous neuroimaging works in monkeys and humans showing a periodotopic organization within and across distinct auditory fields. However, the sluggishness of the signal from these neuroimaging works prohibit inferences with regards to the fine-temporal features of the neural response. In the present study, we employed amplitude-modulated (AM) sounds over a range between 4 and 85 Hz to elicit aSSRs while recording brain activity via magnetoencephalography (MEG). Using beamforming and a fine spatially resolved grid restricted to auditory cortical processing regions, our study revealed a topographic representation of the aSSR that depends on AM rate, in particular in the medial-lateral (bilateral) and posterior-anterior (right auditory cortex) direction. In summary, our findings confirm previous studies that showing different AM rates to elicit maximal response in distinct neural populations. They extend these findings however by also showing that these respective neural ensembles in auditory cortex actually phase lock their activity over a wide modulation frequency range.

Cell-specific gain modulation by synaptically released zinc in cortical circuits of audition.

In many excitatory synapses, mobile zinc is found within glutamatergic vesicles and is coreleased with glutamate. Ex vivo studies established that synaptically released (synaptic) zinc inhibits excitatory neurotransmission at lower frequencies of synaptic activity but enhances steady state synaptic responses during higher frequencies of activity. However, it remains unknown how synaptic zinc affects neuronal processing in vivo. Here, we imaged the sound-evoked neuronal activity of the primary auditory cortex in awake mice. We discovered that synaptic zinc enhanced the gain of sound-evoked responses in CaMKII-expressing principal neurons, but it reduced the gain of parvalbumin- and somatostatin-expressing interneurons. This modulation was sound intensity-dependent and, in part, NMDA receptor-independent. By establishing a previously unknown link between synaptic zinc and gain control of auditory cortical processing, our findings advance understanding about cortical synaptic mechanisms and create a new framework for approaching and interpreting the role of the auditory cortex in sound processing.