Auditory Cortex Research Articles

Preserved functional organization of auditory cortex in two individuals missing one temporal lobe from infancy

Human cortical responses to natural sounds, measured with fMRI, can be approximated as the weighted sum of a small number of canonical response patterns (components), each having interpretable functional and anatomical properties. Here, we asked whether this organization is preserved in cases where only one temporal lobe is available due to early brain damage by investigating a unique family: one sibling missing their left temporal lobe from infancy, another missing the right temporal lobe from infancy, and a third anatomically neurotypical. None of the siblings manifested behavioral deficits. We analyzed fMRI responses to diverse natural sounds within the intact hemispheres of these individuals and compared them to 12 neurotypical participants. All siblings manifested typical-like auditory responses in their intact hemispheres. These results suggest that the development of the auditory cortex in each hemisphere does not depend on the existence of the other hemisphere, highlighting the redundancy and equipotentiality of the bilateral auditory system.

Decoding contextual influences on auditory perception from primary auditory cortex.

Perception can be highly dependent on stimulus context, but whether and how sensory areas encode the context remains uncertain. We used an ambiguous auditory stimulus - a tritone pair - to investigate the neural activity associated with a preceding contextual stimulus that strongly influenced the tritone pair's perception: either as an ascending or a descending step in pitch. We recorded single-unit responses from a population of auditory cortical cells in awake ferrets listening to the tritone pairs preceded by the contextual stimulus. We find that the responses adapt locally to the contextual stimulus, consistent with human MEG recordings from the auditory cortex under the same conditions. Decoding the population responses demonstrates that cells responding to pitch-class-changes are able to predict well the context-sensitive percept of the tritone pairs. Conversely, decoding the individual pitch-class representations and taking their distance in the circular Shepard tone space predicts the opposite of the percept. The various percepts can be readily captured and explained by a neural model of cortical activity based on populations of adapting, pitch-class and pitch-class-direction cells, aligned with the neurophysiological responses. Together, these decoding and model results suggest that contextual influences on perception may well be already encoded at the level of the primary sensory cortices, reflecting basic neural response properties commonly found in these areas.

Errors in the Assumptions of Bekesy's Traveling Wave Theory

This article examines the fundamental statements of Bekesy's traveling wave theory in hearing and proposes an updated perspective on auditory information processing mechanisms. It argues that the traditional theory does not adequately account for non-mammalian auditory mechanisms, as many species effectively perceive sound without a basilar membrane or cochlear fluids. It suggests alternative pathways for sound signal reception directly to the receptor, bypassing traditional structures like the basilar membrane. This reevaluation raises significant doubts about the resonance capability and the actual role of the basilar membrane in hearing, suggesting that current understandings of auditory processing may be fundamentally limited and not universally applicable across different species.

Subcortical origin of nonlinear sound encoding in auditory cortex

A major challenge in neuroscience is to understand how neural representations of sensory information are transformed by the network of ascending and descending connections in each sensory system. By recording from neurons at several levels of the auditory pathway, we show that much of the nonlinear encoding of complex sounds in auditory cortex can be explained by transformations in the midbrain and thalamus. Modeling cortical neurons in terms of their inputs across these subcortical populations enables their responses to be predicted with unprecedented accuracy. By contrast, subcortical responses cannot be predicted from descending cortical inputs, indicating that ascending transformations are irreversible, resulting in increasingly lossy, higher-order representations across the auditory pathway. Rather, auditory cortex selectively modulates the nonlinear aspects of thalamic auditory responses and the functional coupling between subcortical neurons without affecting the linear encoding of sound. These findings reveal the fundamental role of subcortical transformations in shaping cortical responses.

Primary auditory thalamus relays directly to cortical layer 1 interneurons.

Inhibitory interneurons within cortical layer 1 (L1-INs) integrate inputs from diverse brain regions to modulate sensory processing and plasticity, but the sensory inputs that recruit these interneurons have not been identified. Here we used monosynaptic retrograde tracing and whole-cell electrophysiology to characterize the thalamic inputs onto two major subpopulations of L1-INs in the mouse auditory cortex. We find that the vast majority of auditory thalamic inputs to these L1-INs unexpectedly arise from the ventral subdivision of the medial geniculate body (MGBv), the tonotopically-organized primary auditory thalamus. Moreover, these interneurons receive robust functional monosynaptic MGBv inputs that are comparable to those recorded in the L4 excitatory pyramidal neurons. Our findings identify a direct pathway from the primary auditory thalamus to the L1-INs, suggesting that these interneurons are uniquely positioned to integrate thalamic inputs conveying precise sensory information with top-down inputs carrying information about brain states and learned associations.

BOLD fMRI responses to amplitude-modulated sounds across age in adult listeners

Abstract Age-related alterations in the auditory system have been suggested to affect the processing of temporal envelope amplitude modulations (AM) at different levels of the auditory hierarchy, yet few studies have used functional magnetic resonance imaging (fMRI) to study this noninvasively in humans with high spatial resolution. In this study, we utilized sparse-sampling fMRI at 3 Tesla (3T) to investigate regional blood oxygenation level-dependent (BOLD) responses to AM noise stimuli in 65 individuals ranging in age from 19 to 77 years. We contrasted BOLD responses to AM noise stimuli modulated at 4 Hz or 80 Hz with responses to unmodulated stimuli. This allowed us to derive functional measures of regional neural sensitivity to the imposed AM. Compared with unmodulated noise, slowly varying 4 Hz AM noise stimuli elicited significantly greater BOLD responses in the left and right auditory cortex along the Heschl’s gyrus (HG). BOLD responses to the 80 Hz AM stimuli were significantly greater than responses to unmodulated stimuli in putatively primary auditory cortical regions in the lateral HG. BOLD responses to 4 Hz AM stimuli were significantly greater in magnitude than responses to 80 Hz AM stimuli in auditory cortical regions. We find no discernible effects of age on the functional recruitment of the auditory cortex by AM stimuli. While the results affirm the involvement of the auditory cortex in processing temporal envelope rate information, they provide no support for age-related effects on these measures. We discuss potential caveats in assessing age-related changes in responses to AM stimuli in the auditory pathway.

Contributions of cortical neuron firing patterns, synaptic connectivity, and plasticity to task performance

Neuronal responses during behavior are diverse, ranging from highly reliable ‘classical’ responses to irregular ‘non-classically responsive’ firing. While a continuum of response properties is observed across neural systems, little is known about the synaptic origins and contributions of diverse responses to network function, perception, and behavior. To capture the heterogeneous responses measured from auditory cortex of rodents performing a frequency recognition task, we use a novel task-performing spiking recurrent neural network incorporating spike-timing-dependent plasticity. Reliable and irregular units contribute differentially to task performance via output and recurrent connections, respectively. Excitatory plasticity shifts the response distribution while inhibition constrains its diversity. Together both improve task performance with full network engagement. The same local patterns of synaptic inputs predict spiking response properties of network units and auditory cortical neurons from in vivo whole-cell recordings during behavior. Thus, diverse neural responses contribute to network function and emerge from synaptic plasticity rules.

Perceptual awareness of near-threshold tones scales gradually with auditory cortex activity and pupil dilation

Negative-going responses in sensory cortex co-vary with perceptual awareness of sensory stimuli. Given that this awareness negativity has also been observed for undetected stimuli, some have challenged its role for perception. To address this question, we combined magnetoencephalography, electroencephalography, and pupillometry to study how sustained attention and response criterion affect the auditory awareness negativity. Participants first detected distractor sounds and denied hearing task-irrelevant near-threshold tones, which evoked neither awareness negativity nor pupil dilation. These same tones evoked both responses when task-relevant, stronger for hit but also present for miss trials. Participants then rated their perception on a six-point scale to test whether response criterion explains the presence of these responses for miss trials. Decreasing perception ratings were associated with gradually reduced evoked responses, consistent with signal detection theory. These results support the concept of an awareness negativity that is modulated by attention but does not require a non-linear threshold mechanism.

Bidirectional remodeling of the central auditory system caused by unilateral auditory deprivation.

Unilateral auditory deprivation (UAD) results in cross-modal reorganization of the auditory cortex (AC), which can impair auditory and cognitive functions and diminish the recovery effect of cochlear implantation. Moreover, the subcortical areas provide extensive ascending projections to the AC. To date, a thorough systematic study of subcortical auditory neural plasticity has not been undertaken. Therefore, this review aims to summarize the current evidence on the bidirectional remodeling of the central auditory system caused by UAD, particularly the changes in subcortical neural plasticity. Lateral changes occur in the cochlear nucleus, lateral superior olive, medial nucleus of the trapezoid body, inferior colliculus, and AC of individuals with UAD. Moreover, asymmetric neural activity becomes less prominent in the higher auditory nuclei, which may be due to cross-projection regulation of the bilateral pathway. As a result, subcortical auditory neural plasticity caused by UAD may contribute to the outcomes of cochlear implantation in patients with single-sided deafness (SSD), and the development of intervention strategies for patients with SSD is crucial. Considering that previous studies have focused predominantly on the neural plasticity of the AC, we believe that bidirectional remodeling of subcortical areas after UAD is also crucial for investigating the mechanisms of interventions.

Temporal gamma tACS and auditory stimulation affect verbal memory in healthy adults.

Research suggests a potential of gamma oscillation entrainment for enhancing memory in Alzheimer's disease and healthy subjects. Gamma entrainment can be accomplished with oscillatory electrical, but also sensory stimulation. However, comparative studies between sensory stimulation and transcranial alternating current stimulation (tACS) effects on memory processes are lacking. This study examined the effects of rhythmic gamma auditory stimulation (rAS) and temporal gamma-tACS on verbal long-term memory (LTM) and working memory (WM) in 74 healthy individuals. Participants were assigned to two groups according to the stimulation techniques (rAS or tACS). Memory was assessed in three experimental blocks, in which each participant was administered with control, 40, and 60 Hz stimulation in counterbalanced order. All interventions were well-tolerated, and participants reported mostly comparable side effects between real stimulation (40 and 60 Hz) and the control condition. LTM immediate and delayed recall remained unaffected by stimulations, while immediate recall intrusions decreased during 60 Hz stimulation. Notably, 40 Hz interventions improved WM compared to control stimulations. These results highlight the potential of 60 and 40 Hz temporal cortex stimulation for reducing immediate LTM recall intrusions and improving WM performance, respectively, probably due to the entrainment of specific gamma oscillations in the auditory cortex. The results also shed light on the comparative effects of these neuromodulation tools on memory functions, and their potential applications for cognitive enhancement and in clinical trials.

Preliminary Validation of the Children's Auditory Performance Scale (CHAPS) and the Auditory Processing Domain Questionnaire (APDQ) in Greek Cypriot Children.

Identification of auditory processing disorders is achieved using questionnaires along with linguistic, non-linguistic, and auditory processing tests. Notably, the questionnaires "Children's Auditory Performance Scale" (CHAPS) and "Auditory Processing Domain Questionnaire" (APDQ) are widely recognized and used. The current study investigated the psychometric properties of the CHAPS and APDQ in Greek Cypriot children. The CHAPS and APDQ questionnaires were completed by parents of 40 Greek Cypriot children, 16 typically developing (TD) children, and 24 children with a history of Speech Sound Disorders (SSDs). There were significant differences between the two groups on both questionnaires. Cronbach's alpha was calculated at α = 0.922 for the CHAPS total score and α = 0.926 for the APDQ total score. The Receiver Operating Curve (ROC) analysis provided a cut-off point equal to -0.30 (AUC 0.849, p < 0.001) for CHAPS and a cut-off point equal to 90.00 (AUC 0.820, p < 0.001) for APDQ. Significant positive Spearman ρ correlations were observed between the CHAPS and APDQ (ρ = 0.639, p = 0.001). The CHAPS and APDQ can identify distinct auditory processing characteristics between in children with SSDs and TD children.

The Influence of Asymmetric Hearing Loss on Peripheral and Central Auditory Processing Abilities in Patients With Vestibular Schwannoma.

Asymmetric or unilateral hearing loss (AHL) may cause irreversible changes in the processing of acoustic signals in the auditory system. We aim to provide a comprehensive view of the auditory processing abilities for subjects with acquired AHL, and to examine the influence of AHL on speech perception under difficult conditions, and on auditory temporal and intensity processing. We examined peripheral and central auditory functions for 25 subjects with AHL resulting from vestibular schwannoma, and compared them to those from 24 normal-hearing controls that were matched with the AHL subjects in mean age and hearing thresholds in the healthy ear. Besides the basic hearing threshold assessment, the tests comprised the detection of tones and gaps in a continuous noise, comprehension of speech in babble noise, binaural interactions, difference limen of intensity, and detection of frequency modulation. For the AHL subjects, the selected tests were performed separately for the healthy and diseased ear. We observed that binaural speech comprehension, gap detection, and frequency modulation detection abilities were dominated by the healthy ear and were comparable for both groups. The AHL subjects were less sensitive to interaural delays, however, they exhibited a higher sensitivity to sound level, as indicated by lower difference limen of intensity and a higher sensitivity to interaural intensity difference. Correlations between the individual test scores indicated that speech comprehension by the AHL subjects was associated with different auditory processing mechanisms than for the control subjects. The data suggest that AHL influences both peripheral and central auditory processing abilities and that speech comprehension under difficult conditions relies on different mechanisms for the AHL subjects than for normal-hearing controls.

Speech-in-Noise and Dichotic Auditory Training Students With Autism Spectrum Disorder.

Individuals diagnosed with autism spectrum disorder (ASD) often exhibit auditory processing issues, including poor speech recognition in background noise and dichotic processing (integration of different stimuli presented to the two ears). Auditory training could mitigate these auditory difficulties. However, few auditory training programs have been designed to target specific listening deficits for students with ASD. The present study summarizes the development of an innovative, one-on-one, clinician-developed speech-in-noise (SIN) training program that has not been previously described and an existing dichotic auditory training program to address common auditory processing deficits in students with ASD. Twenty verbal students with ASD, ages 7-17 years, completed a one-on-one, clinician-developed SIN training program and a commercially available dichotic training program 2-3 times a week (30-45 min per session) for 12 weeks. Maximum and minimum training levels from the SIN and dichotic training programs were analyzed statistically to document changes in training level over the training period. Analyses of the pre- and posttraining data revealed significant improvements in training level for both the SIN and dichotic training programs. Overall, the proposed SIN training resulted in significant improvements in training level and may be used along with dichotic training to improve some of the most common auditory processing issues documented in verbal individuals with ASD requiring minimal support. Both types of auditory training may be implemented in one-on-one therapy in clinics and in the schools.

Neural oscillations suggest periodicity encoding during auditory beat processing in the premature brain.

When exposed to rhythmic patterns with temporal regularity, adults exhibit an inherent ability to extract and anticipate an underlying sequence of regularly spaced beats, which is internally constructed, as beats are experienced even when no events occur at beat positions (e.g., in the case of rests). Perception of rhythm and synchronization to periodicity is indispensable for development of cognitive functions, social interaction, and adaptive behavior. We evaluated neural oscillatory activity in premature newborns (n=19, mean age, 32±2.59weeks gestational age) during exposure to an auditory rhythmic sequence, aiming to identify early traces of periodicity encoding and rhythm processing through entrainment of neural oscillations at this stage of neurodevelopment. The rhythmic sequence elicited a systematic modulation of alpha power, synchronized to expected beat locations coinciding with both tones and rests, and independent of whether the beat was preceded by tone or rest. In addition, the periodic alpha-band fluctuations reached maximal power slightly before the corresponding beat onset times. Together, our results show neural encoding of periodicity in the premature brain involving neural oscillations in the alpha range that are much faster than the beat tempo, through alignment of alpha power to the beat tempo, consistent with observations in adults on predictive processing of temporal regularities in auditory rhythms. RESEARCH HIGHLIGHTS: In response to the presented rhythmic pattern, systematic modulations of alpha power showed that the premature brain extracted the temporal regularity of the underlying beat. In contrast to evoked potentials, which are greatly reduced when there is no sounds event, the modulation of alpha power occurred for beats coinciding with both tones and rests in a predictive way. The findings provide the first evidence for the neural coding of periodicity in auditory rhythm perception before the age of term.

A social cognition perspective on misophonia.

Misophonia is commonly classified by intense emotional reactions to common everyday sounds. The condition has an impact both on the mental health of its sufferers and societally. As yet, formal models on the basis of misophonia are in their infancy. Based on developing behavioural and neuroscientific research we are gaining a growing understanding of the phenomenology and empirical findings in misophonia, such as the importance of context, types of coping strategies used and the activation of particular brain regions. In this article, we argue for a model of misophonia that includes not only the sound but also the context within which sound isperceived and the emotional reaction triggered. We review the current behavioural and neuroimaging literature, which lends support to this idea. Based on the current evidence, we propose that misophonia should be understood within the broader context of social perception and cognition, and notrestricted within the narrow domain of being a disorder of auditory processing. We discuss the evidence in support of this hypothesis, as well as the implications for potential treatment approaches. This article is part of the theme issue 'Sensing and feeling: an integrative approach to sensory processing and emotional experience'.

Microplastic polyethylene induced inner ear dysfunction in murine model

While the hazardous effects of microplastics (MPs) are increasingly reported, it remains uncertain if MPs induce inner ear dysfunction. Nonetheless, prevalence of inner ear dysfunction was observed across all age groups. In this study, we investigated whether MP polyethylene affect inner ear function in a murine model. To detect hearing loss and balance defect after polyethylene (PE) exposure, we evaluated hearing threshold levels, assessed cerebral glucose metabolism, conducted transcriptome analysis, and performed behavioral studies. C57BL/6 J mice (5-week-old) were grouped into control (n = 10) and PE-fed groups (n = 10). Mice were orally administered 100 ppm/100 μL (equivalent to 10 μg) of PE every day for 4 months. We identified the accumulation of PE in the cochlea and vestibular region. The fragmented PE in inner ear was 3.00 ± 0.38 µm in size; the administered PE concentration was 1.14 ± 1.06 mg/g. Fourier transform infrared spectrometry confirmed that the properties of the MP were identical with those of PE fed to the mice. Transcriptomic analysis showed up-regulation of PER1, NR4A3 and CEBPB at the PE exposed inner ear tissue and it was confirmed using qRT-PCR, western blotting, and immunofluorescence staining. We observed abnormalities in balance related behavior assessment in the PE group. Exposure to PE increased the hearing thresholds and decreased glucose metabolism in the bilateral lateral entorhinal cortex, right primary auditory cortex, and right secondary auditory cortex. We can conclude that PE exposure induced inner ear dysfunction such as hearing loss and balance disorder.

Repetition-Dependent Adaptation and Prediction Error Signalling in Schizophrenia Patients With Auditory Hallucinations: A Roving Mismatch Negativity Study

BackgroundDysregulated prediction error-signalling may explain auditory hallucinations in schizophrenia (SZ-AH). Roving mismatch negativity (rMMN) is an event-related potential (ERP) index where the deviant tone becomes the new standard with repetitions. Longer repetitions of standard stimuli yield a more positive sensory-adaptation response (Repetition Positivity–RP), elicit a stronger deviance-detection when interrupted (deviant negativity–DN), and the difference waveform between them reflects the strength of prediction-error signalling (mismatch negativity–MMN). MethodsTwenty-three SZ-AH patients and twenty-three healthy controls (HC) underwent rMMN assessment. Various standard stimuli were repeated in sets of 3, 8 and 33 yielding three components for RP (RP3, RP8, RP33), DN (DN3, DN8, DN33), and MMN (MMN3, MMN8, MMN33). Amplitudes and latencies were compared across groups. Correlation between (a) rMMN amplitudes and latencies, and clinical variables in SZ-AH, and (b) the RP-DN amplitude pair for all three repetition sets (3, 8, 33) were also examined. ResultsAll DN and MMN33 amplitudes were significantly suppressed in SZ-AH, while RP amplitudes were not. MMN33 latency was significantly longer in SZ-AH than HC. A few amplitudes and latencies significantly correlated with the frequency of AH. HC showed a significant positive correlation between RP-DN amplitude pairs for sets of 3 and 8 but not for 33; SZ-AH group’s correlation profile was opposite to this. DiscussionThe link between repetition-dependent sensory-adaptation and deviance-detection is perturbed in SZ-AH. The unimpaired RP profile in SZ-AH is due to potential interference of AH with auditory information processing, and does not indicate a preserved short-term plasticity of the echoic memory trace.

Does pre-speech auditory modulation reflect processes related to feedback monitoring or speech movement planning?

Previous studies have revealed that auditory processing is modulated during the planning phase immediately prior to speech onset. To date, the functional relevance of this pre-speech auditory modulation (PSAM) remains unknown. Here, we investigated whether PSAM reflects neuronal processes that are associated with preparing auditory cortex for optimized feedback monitoring as reflected in online speech corrections. Combining electroencephalographic PSAM data from a previous data set with new acoustic measures of the same participants' speech, we asked whether individual speakers' extent of PSAM is correlated with the implementation of within-vowel articulatory adjustments during /b/-vowel-/d/ word productions. Online articulatory adjustments were quantified as the extent of change in inter-trial formant variability from vowel onset to vowel midpoint (a phenomenon known as centering). This approach allowed us to also consider inter-trial variability in formant production and its possible relation to PSAM at vowel onset and midpoint separately. Results showed that inter-trial formant variability was significantly smaller at vowel midpoint than at vowel onset. PSAM was not significantly correlated with this amount of change in variability as an index of within-vowel adjustments. Surprisingly, PSAM was negatively correlated with inter-trial formant variability not only in the middle but also at the very onset of the vowels. Thus, speakers with more PSAM produced formants that were already less variable at vowel onset. Findings suggest that PSAM may reflect processes that influence speech acoustics as early as vowel onset and, thus, that are directly involved in motor command preparation (feedforward control) rather than output monitoring (feedback control).

Newborn's neural representation of instrumental and vocal music as revealed by fMRI: A dynamic effective brain connectivity study.

Music is ubiquitous, both in its instrumental and vocal forms. While speech perception at birth has been at the core of an extensive corpus of research, the origins of the ability to discriminate instrumental or vocal melodies is still not well investigated. In previous studies comparing vocal and musical perception, the vocal stimuli were mainly related to speaking, including language, and not to the non-language singing voice. In the present study, to better compare a melodic instrumental line with the voice, we used singing as a comparison stimulus, to reduce the dissimilarities between the two stimuli as much as possible, separating language perception from vocal musical perception. In the present study, 45 newborns were scanned, 10 full-term born infants and 35 preterm infants at term-equivalent age (mean gestational age at test = 40.17 weeks, SD = 0.44) using functional magnetic resonance imaging while listening to five melodies played by a musical instrument (flute) or sung by a female voice. To examine the dynamic task-based effective connectivity, we employed a psychophysiological interaction of co-activation patterns (PPI-CAPs) analysis, using the auditory cortices as seed region, to investigate moment-to-moment changes in task-driven modulation of cortical activity during an fMRI task. Our findings reveal condition-specific, dynamically occurring patterns of co-activation (PPI-CAPs). During the vocal condition, the auditory cortex co-activates with the sensorimotor and salience networks, while during the instrumental condition, it co-activates with the visual cortex and the superior frontal cortex. Our results show that the vocal stimulus elicits sensorimotor aspects of the auditory perception and is processed as a more salient stimulus while the instrumental condition activated higher-order cognitive and visuo-spatial networks. Common neural signatures for both auditory stimuli were found in the precuneus and posterior cingulate gyrus. Finally, this study adds knowledge on the dynamic brain connectivity underlying the newborns capability of early and specialized auditory processing, highlighting the relevance of dynamic approaches to study brain function in newborn populations.

Orbitofrontal cortex modulates auditory cortical sensitivity and sound perception in Mongolian gerbils

Sensory perception is dynamic, quickly adapting to sudden shifts in environmental or behavioral context. Although decades of work have established that these dynamics are mediated by rapid fluctuations in sensory cortical activity, we have a limited understanding of the brain regions and pathways that orchestrate these changes. Neurons in the orbitofrontal cortex (OFC) encode contextual information, and recent data suggest that some of these signals are transmitted to sensory cortices. Whether and how these signals shape sensory encoding and perceptual sensitivity remain uncertain. Here, we asked whether the OFC mediates context-dependent changes in auditory cortical sensitivity and sound perception by monitoring and manipulating OFC activity in freely moving Mongolian gerbils of both sexes under two behavioral contexts: passive sound exposure and engagement in an amplitude modulation (AM) detection task. We found that the majority of OFC neurons, including the specific subset that innervates the auditory cortex, were strongly modulated by task engagement. Pharmacological inactivation of the OFC prevented rapid context-dependent changes in auditory cortical firing and significantly impaired behavioral AM detection. Our findings suggest that contextual information from the OFC mediates rapid plasticity in the auditory cortex and facilitates the perception of behaviorally relevant sounds.