Low-level Auditory Processing Research Articles

Probabilistic and explainable modeling of Phase–Phase Cross-Frequency Coupling patterns in EEG. Application to dyslexia diagnosis

This work explores the intricate neural dynamics associated with dyslexia through the lens of Cross-Frequency Coupling (CFC) analysis applied to electroencephalography (EEG) signals evaluated from 48 seven-year-old Spanish readers from the LEEDUCA research platform. The analysis focuses on CFS (Cross-Frequency phase Synchronization) maps, capturing the interaction between different frequency bands during low-level auditory processing stimuli. Then, making use of Gaussian Mixture Models (GMMs), CFS activations are quantified and classified, offering a compressed representation of EEG activation maps. The study unveils promising results specially at the Theta-Gamma coupling (Area Under the Curve = 0.821), demonstrating the method’s sensitivity to dyslexia-related neural patterns and highlighting potential applications in the early identification of dyslexic individuals.

Voice actors show enhanced neural tracking of pitch, prosody perception, and music perception

Experiences with sound that make strong demands on the precision of perception, such as musical training and experience speaking a tone language, can enhance auditory neural encoding. Are high demands on the precision of perception necessary for training to drive auditory neural plasticity? Voice actors are an ideal subject population for answering this question. Voice acting requires exaggerating prosodic cues to convey emotion, character, and linguistic structure, drawing upon attention to sound, memory for sound features, and accurate sound production, but not fine perceptual precision. Here we assessed neural encoding of pitch using the frequency-following response (FFR), as well as prosody, music, and sound perception, in voice actors and a matched group of non-actors. We find that the consistency of neural sound encoding, prosody perception, and musical phrase perception are all enhanced in voice actors, suggesting that a range of neural and behavioural auditory processing enhancements can result from training which lacks fine perceptual precision. However, fine discrimination was not enhanced in voice actors but was linked to degree of musical experience, suggesting that low-level auditory processing can only be enhanced by demanding perceptual training. These findings suggest that training which taxes attention, memory, and production but is not perceptually taxing may be a way to boost neural encoding of sound and auditory pattern detection in individuals with poor auditory skills.

Unraveling Brain Synchronisation Dynamics by Explainable Neural Networks using EEG Signals: Application to Dyslexia Diagnosis

The electrical activity of the neural processes involved in cognitive functions is captured in EEG signals, allowing the exploration of the integration and coordination of neuronal oscillations across multiple spatiotemporal scales. We have proposed a novel approach that combines the transformation of EEG signal into image sequences, considering cross-frequency phase synchronisation (CFS) dynamics involved in low-level auditory processing, with the development of a two-stage deep learning model for the detection of developmental dyslexia (DD). This deep learning model exploits spatial and temporal information preserved in the image sequences to find discriminative patterns of phase synchronisation over time achieving a balanced accuracy of up to 83%. This result supports the existence of differential brain synchronisation dynamics between typical and dyslexic seven-year-old readers. Furthermore, we have obtained interpretable representations using a novel feature mask to link the most relevant regions during classification with the cognitive processes attributed to normal reading and those corresponding to compensatory mechanisms found in dyslexia.Graphical

Low-Level Auditory Processing Correlates With Language Abilities: An ERP Study Investigating Sequence Learning and Auditory Processing in School-Aged Children.

Auditory processing and procedural learning deficits have been associated with language learning difficulties. We investigated the relationship of these skills and school-age language abilities in children with and without a history of late talking using auditory event related potentials (ERPs). Late talking (i.e., slow early language development) increases the risk of persistent language difficulties, but its causes remain unknown. Participants in this study were children with varying language abilities (n = 60). Half of the participants (n = 30) had a history of late talking. We measured procedural learning by manipulating the predictability of sine tone stimuli in a passive auditory ERP paradigm. Auditory processing was tested by examining how the presence of noise (increasing perceptual demands) affected the ERPs. Contrary to our hypotheses on auditory processing and language development, the effect of noise on ERPs did not correlate with school-age language abilities in children with or without a history of late talking. Our paradigm failed to reveal interpretable effects of predictability leaving us unable to assess the effects of procedural learning. However, better language abilities were related to weaker responses in a 75-175 ms time window, and stronger responses in a 150-250 ms time window. We suggest that the weak early responses in children with better language ability reflect efficient processing of low-level auditory information, allowing deeper processing of later, high-level auditory information. We assume that these differences reflect variation in brain maturation between individuals with varying language abilities.

Assessing Functional Brain Network Dynamics in Dyslexia from fNIRS Data.

Developmental dyslexia is characterized by a deficit of phonological awareness whose origin is related to atypical neural processing of speech streams. This can lead to differences in the neural networks that encode audio information for dyslexics. In this work, we investigate whether such differences exist using functional near-infrared spectroscopy (fNIRS) and complex network analysis. We have explored functional brain networks derived from low-level auditory processing of nonspeech stimuli related to speech units such as stress, syllables or phonemes of skilled and dyslexic seven-year-old readers. A complex network analysis was performed to examine the properties of functional brain networks and their temporal evolution. We characterized aspects of brain connectivity such as functional segregation, functional integration or small-worldness. These properties are used as features to extract differential patterns in controls and dyslexic subjects. The results corroborate the presence of discrepancies in the topological organizations of functional brain networks and their dynamics that differentiate between control and dyslexic subjects, reaching an Area Under ROC Curve (AUC) up to 0.89 in classification experiments.

Under-resourced or overloaded? Rethinking working memory deficits in developmental language disorder.

Dominant theoretical accounts of developmental language disorder (DLD) commonly invoke working memory capacity limitations. In the current report, we present an alternative view: That working memory in DLD is not under-resourced but overloaded due to operating on speech representations with low discriminability. This account is developed through computational simulations involving deep convolutional neural networks trained on spoken word spectrograms in which information is either retained to mimic typical development or degraded to mimic the auditory processing deficits identified among some children with DLD. We assess not only spoken word recognition accuracy and predictive probability and entropy (i.e., predictive distribution spread), but also use mean-field-theory based manifold analysis to assess; (a) internal speech representation dimensionality and (b) classification capacity, a measure of the networks' ability to isolate any given internal speech representation that is used as a proxy for attentional control. We show that instantiating a low-level auditory processing deficit results in the formation of internal speech representations with atypically high dimensionality, and that classification capacity is exhausted due to low representation separability. These representation and control deficits underpin not only lower performance accuracy but also greater uncertainty even when making accurate predictions in a simulated spoken word recognition task (i.e., predictive distributions with low maximum probability and high entropy), which replicates the response delays and word finding difficulties often seen in DLD. Overall, these simulations demonstrate a theoretical account of speech representation and processing deficits in DLD in which working memory capacity limitations play no causal role. (PsycInfo Database Record (c) 2023 APA, all rights reserved).

Asymmetrical cross-modal influence on neural encoding of auditory and visual features in natural scenes

Natural scenes contain multi-modal information, which is integrated to form a coherent perception. Previous studies have demonstrated that cross-modal information can modulate neural encoding of low-level sensory features. These studies, however, mostly focus on the processing of single sensory events or rhythmic sensory sequences. Here, we investigate how the neural encoding of basic auditory and visual features is modulated by cross-modal information when the participants watch movie clips primarily composed of non-rhythmic events. We presented audiovisual congruent and audiovisual incongruent movie clips, and since attention can modulate cross-modal interactions, we separately analyzed high- and low-arousal movie clips. We recorded neural responses using electroencephalography (EEG), and employed the temporal response function (TRF) to quantify the neural encoding of auditory and visual features. The neural encoding of sound envelope is enhanced in the audiovisual congruent condition than the incongruent condition, but this effect is only significant for high-arousal movie clips. In contrast, audiovisual congruency does not significantly modulate the neural encoding of visual features, e.g., luminance or visual motion. In summary, our findings demonstrate asymmetrical cross-modal interactions during the processing of natural scenes that lack rhythmicity: Congruent visual information enhances low-level auditory processing, while congruent auditory information does not significantly modulate low-level visual processing.

While you were sleeping: Evidence for high-level executive processing of an auditory narrative during sleep

During sleep we lack conscious awareness of the external environment. Yet, our internal mental state suggests that high-level cognitive processes persist. The nature and extent to which the external environment is processed during sleep remain largely unexplored. Here, we used an fMRI synchronization-based approach to examine responses to a narrative during wakefulness and sleep. The stimulus elicited the auditory network and a frontoparietal pattern of activity, consistent with high-level narrative plot-following. During REM sleep, the same frontoparietal pattern was observed in one of three participants, and partially in one other, confirming that it is possible to track and follow the moment-to-moment complexities of a narrative during REM sleep. Auditory network recruitment was observed in both non-REM and REM sleep, demonstrating preservation of low-level auditory processing, even in deep sleep. This novel approach investigating cognitive processing at different levels of awareness demonstrates that the brain can meaningfully process the external environment during REM sleep.

Complex network modeling of EEG band coupling in dyslexia: An exploratory analysis of auditory processing and diagnosis

Complex network analysis has an increasing relevance in the study of neurological disorders, enhancing the knowledge of brain’s structural and functional organization. Network structure and efficiency reveal different brain states along with different ways of processing the information. This work is structured around the exploratory analysis of the brain processes involved in low-level auditory processing. A complex network analysis was performed on the basis of brain coupling obtained from electroencephalography (EEG) data, while different auditory stimuli were presented to the subjects. This coupling is inferred from the Phase-Amplitude coupling (PAC) from different EEG electrodes to explore differences between control and dyslexic subjects. Coupling data allows the construction of a graph, and then, graph theory is used to study the characteristics of the complex networks throughout time for control and dyslexic subjects. This results in a set of metrics including clustering coefficient, path length and small-worldness. From this, different characteristics linked to the temporal evolution of networks and coupling are pointed out for dyslexics. Our study revealed patterns related to Dyslexia as losing the small-world topology. Finally, these graph-based features are used to classify between control and dyslexic subjects by means of a Support Vector Machine (SVM).

Auditory hypersensitivity and processing deficits in a rat model of fragile X syndrome

Fragile X (FX) syndrome is one of the leading inherited causes of autism spectrum disorder (ASD). A majority of FX and ASD patients exhibit sensory hypersensitivity, including auditory hypersensitivity or hyperacusis, a condition in which everyday sounds are perceived as much louder than normal. Auditory processing deficits in FX and ASD also afford the opportunity to develop objective and quantifiable outcome measures that are likely to translate between humans and animal models due to the well-conserved nature of the auditory system and well-developed behavioral read-outs of sound perception. Therefore, in this study we characterized auditory hypersensitivity in a Fmr1 knockout (KO) transgenic rat model of FX using an operant conditioning task to assess sound detection thresholds and suprathreshold auditory reaction time-intensity (RT-I) functions, a reliable psychoacoustic measure of loudness growth, at a variety of stimulus frequencies, bandwidths, and durations. Male Fmr1 KO and littermate WT rats both learned the task at the same rate and exhibited normal hearing thresholds. However, Fmr1 KO rats had faster auditory RTs over a broad range of intensities and steeper RT-I slopes than WT controls, perceptual evidence of excessive loudness growth in Fmr1 KO rats. Furthermore, we found that Fmr1 KO animals exhibited abnormal perceptual integration of sound duration and bandwidth, with diminished temporal but enhanced spectral integration of sound intensity. Because temporal and spectral integration of sound stimuli were altered in opposite directions in Fmr1 KO rats, this suggests that abnormal RTs in these animals are evidence of aberrant auditory processing rather than generalized hyperactivity or altered motor responses. Together, these results are indicative of fundamental changes to low-level auditory processing in Fmr1 KO animals. Finally, we demonstrated that antagonism of metabotropic glutamate receptor 5 (mGlu5) selectively and dose-dependently restored normal loudness growth in Fmr1 KO rats, suggesting a pharmacologic approach for alleviating sensory hypersensitivity associated with FX. This study leverages the tractable nature of the auditory system and the unique behavioral advantages of rats to provide important insights into the nature of a centrally important yet understudied aspect of FX and ASD.

Detecting Phase-Synchrony Connectivity Anomalies in EEG Signals. Application to Dyslexia Diagnosis.

Objective Dyslexia diagnosis is a challenging task, since traditional diagnosis methods are not based on biological markers but on behavioural tests. Although dyslexia diagnosis has been addressed by these tests in clinical practice, it is difficult to extract information about the brain processes involved in the different tasks and, then, to go deeper into its biological basis. Thus, the use of biomarkers can contribute not only to the diagnosis but also to a better understanding of specific learning disorders such as dyslexia. In this work, we use Electroencephalography (EEG) signals to discover differences among controls and dyslexic subjects using signal processing and artificial intelligence techniques. Specifically, we measure phase synchronization among channels, to reveal the functional brain network activated during auditory processing. On the other hand, to explore synchronicity patterns risen by low-level auditory processing, we used specific stimuli consisting in band-limited white noise, modulated in amplitude at different frequencies. The differential information contained in the functional (i.e., synchronization) network has been processed by an anomaly detection system that addresses the problem of subjects variability by an outlier-detection method based on vector quantization. The results, obtained for 7 years-old children, show that the proposed method constitutes an useful tool for clinical use, with the area under ROC curve (AUC) values up to 0.95 in differential diagnosis tasks.

Auditory Processing of Non-speech Stimuli by Children in Dual-Language Immersion Programs.

Perception of low-level auditory cues such as frequency modulation (FM) and rise time (RT) is crucial for development of phonemic representations, segmentation of word boundaries, and attunement to prosodic patterns in language. While learning an additional language, children may develop an increased sensitivity to these cues to extract relevant information from multiple types of linguistic input. Performance on these auditory processing tasks such as FM and RT by children learning another language is, however, unknown. Here we examine 92 English-speaking 7–8-year-olds in the U.S. and their performance in FM and RT perceptual tasks at the end of their second year in Cantonese or Spanish dual-language immersion compared to children in general English education programs. Results demonstrate that children in immersion programs have greater sensitivity to FM, but not RT, controlling for various factors. The immersion program students were also observed to have better phonological awareness performance. However, individual differences in FM sensitivity were not associated with phonological awareness, a pattern typically observed in monolinguals. These preliminary findings suggest a possible impact of formal language immersion on low-level auditory processing. Additional research is warranted to understand causal relationships and ultimate impact on language skills in multilinguals.

Central auditory processing deficits in schizophrenia: Effects of auditory-based cognitive training

BackgroundSensory processing abnormalities are common in schizophrenia (SZ) and impact everyday functions, such as speech perception in noisy environments. Auditory-based targeted cognitive training (TCT) is a “bottom up” cognitive remediation intervention designed to enhance the speed and accuracy of low-level auditory information processing. However, the effects of TCT on behavioral measures of central auditory processing (CAP) and the role of CAP function on verbal learning outcomes in SZ are unknown. MethodsSZ (n = 42) and healthy subjects (CTL; n = 18) underwent comprehensive clinical, neurocognitive, and auditory assessments, including tests of hearing sensitivity and speech recognition (Words-in-Noise (WIN), Quick Speech-in-Noise (SIN)). SZ patients were randomized to receive either treatment-as-usual (TAU); or 30-h of TCT + TAU using a stratified, parallel design. SZ patients repeated assessments ~10–12 weeks later. ResultsPatients exhibited deficits in both WIN (p < 0.05, d = 0.50) and SIN (p < 0.01, d = 0.63). A treatment × time interaction on WIN (p < 0.05, d = 0.74), but not SIN discriminability, was seen in the TCT group relative to TAU. Specific enhancements in the 4-dB over background range drove gains in WIN performance. Moreover, SZ patients with greater CAP deficits experienced robust gains in verbal learning after 30-h of TCT relative to SZ patients without CAP impairment (p < 0.01, d = 1.28). ConclusionFindings demonstrate that intensive auditory training enhances the fidelity of auditory processing and perception, such that specific CAP deficits were ‘normalized’ and were predictive of gains in verbal learning after TCT. It is conceivable that patients with deficiencies in CAP measures may benefit most from TCT and other interventions targeting auditory dysfunction in SZ.

The viability of the frequency following response characteristics for use as biomarkers of cognitive therapeutics in schizophrenia

Deficits in early auditory information processing contribute to cognitive and psychosocial disability; this has prompted development of interventions that target low-level auditory processing, which may alleviate these disabilities. The frequency following response (FFR) is a constellation of event-related potential and frequency characteristics that reflect the processing of acoustic stimuli at the level of the brainstem and ascending portions of the auditory pathway. While FFR is a promising candidate biomarker of response to auditory-based cognitive training interventions, the psychometric properties of FFR in schizophrenia patients have not been studied. Here we assessed the psychometric reliability and magnitude of group differences across 18 different FFR parameters to determine which of these parameters demonstrate adequate internal consistency. Electroencephalography from 40 schizophrenia patients and 40 nonpsychiatric comparison subjects was recorded during rapid presentation of an auditory speech stimulus (6000 trials). Patients showed normal response amplitudes but longer latencies for most FFR peaks and lower signal-to-noise ratios (SNRs) than healthy subjects. Analysis of amplitude and latency estimates of peaks, however, indicated a need for a substantial increase in task length to obtain internal consistency estimates above 0.80. In contrast, excellent internal consistency (>0.95) was shown for FFR sustained responses. Only SNR scores reflecting the FFR sustained response yielded significant group differences and excellent internal consistency, suggesting that this measure is a viable candidate for use in clinical treatment studies. The present study highlights the use of internal consistency estimates to select FFR characteristics for use in future intervention studies interested in individual differences among patients.

Delayed cortical processing of auditory stimuli in children with autism spectrum disorder: A meta-analysis of electrophysiological studies

Several researchers have hypothesised that individuals with Autism Spectrum Disorder (ASD) show encoding delays in their obligatory event-related potentials (ERPs)/ event-related fields (ERFs) for low-level auditory information compared to neurotypical (NT) samples. However, empirical research has yielded varied findings, such as low-level auditory processing in ASD samples being unimpaired, superior, or impaired compared to NT samples. Diverse outcomes have also been reported for studies investigating ASD-NT differences in functional lateralisation of delays. The lack of consistency across studies has prevented a comprehensive understanding of the overall effects in the autistic population. Therefore, this meta-analysis compared long-latency ERPs and ERFs produced by autistic and NT individuals to non-linguistic auditory stimuli to test, firstly, the robustness of auditory processing differences and, secondly, whether these differences are observed in one or both hemispheres. Nine articles meeting the inclusion criteria were included in the meta-analysis. Meta-analytic results indicated that autistic individuals demonstrate bilaterally delayed P1/ M50 peaks and lateralised delays in the right but not left hemisphere N1/ M100 peak. These results further inform our understanding of auditory processing and lateralisation across the autism spectrum.

Neural and Behavioral Evidence for Frequency-Selective Context Effects in Rhythm Processing in Humans.

When listening to music, people often perceive and move along with a periodic meter. However, the dynamics of mapping between meter perception and the acoustic cues to meter periodicities in the sensory input remain largely unknown. To capture these dynamics, we recorded the electroencephalography while nonmusician and musician participants listened to nonrepeating rhythmic sequences, where acoustic cues to meter frequencies either gradually decreased (from regular to degraded) or increased (from degraded to regular). The results revealed greater neural activity selectively elicited at meter frequencies when the sequence gradually changed from regular to degraded compared with the opposite. Importantly, this effect was unlikely to arise from overall gain, or low-level auditory processing, as revealed by physiological modeling. Moreover, the context effect was more pronounced in nonmusicians, who also demonstrated facilitated sensory-motor synchronization with the meter for sequences that started as regular. In contrast, musicians showed weaker effects of recent context in their neural responses and robust ability to move along with the meter irrespective of stimulus degradation. Together, our results demonstrate that brain activity elicited by rhythm does not only reflect passive tracking of stimulus features, but represents continuous integration of sensory input with recent context.

Auditory cortical representation of music favours the perceived beat.

Previous research has shown that musical beat perception is a surprisingly complex phenomenon involving widespread neural coordination across higher-order sensory, motor and cognitive areas. However, the question of how low-level auditory processing must necessarily shape these dynamics, and therefore perception, is not well understood. Here, we present evidence that the auditory cortical representation of music, even in the absence of motor or top-down activations, already favours the beat that will be perceived. Extracellular firing rates in the rat auditory cortex were recorded in response to 20 musical excerpts diverse in tempo and genre, for which musical beat perception had been characterized by the tapping behaviour of 40 human listeners. We found that firing rates in the rat auditory cortex were on average higher on the beat than off the beat. This ‘neural emphasis’ distinguished the beat that was perceived from other possible interpretations of the beat, was predictive of the degree of tapping consensus across human listeners, and was accounted for by a spectrotemporal receptive field model. These findings strongly suggest that the ‘bottom-up’ processing of music performed by the auditory system predisposes the timing and clarity of the perceived musical beat.

Basic auditory processing deficits in infants at risk for dyslexia during the sensitive period predict future language

It is widely agreed that poor reading and spelling performances in individuals with developmental dyslexia underlie problems with processing phonetic units. According to recent child and adult data, such processing deficits likely are the consequence of compromised low-level auditory processing. A possible causal relationship can be explored by testing infants based on their familial risk of dyslexia. Using magnetoencephalography, the study at hand investigates low-level auditory processing in infants at risk for dyslexia across 6 and 12 months of age—a sensitive period in early language development when the auditory system specializes in native phoneme perception. Results showed smaller and shorter neural responses to simple sounds in at-risk infants at 6 than at 12 months, a pattern that was reversed in age-matched typically developing infants. This interaction was significant both when fitting equivalent current dipoles and when using distributed source modeling and localized to left temporal and left frontal brain regions, indicating its potential impact on early language learning. In addition, atypical auditory responses in at-risk infants consistently predicted later language skills, such as syntactic processing and word production, thus identifying a possible biomarker of dyslexia in the infant brain.

Auditory identification of frequency-modulated sweeps and reading difficulties in Chinese

BackgroundIn Chinese Mandarin, lexical tones play an important role of providing contrasts in word meaning. They are pitch patterns expressed by frequency-modulated (FM) signals. Yet, few studies have looked at the relationship between low-level auditory processing of frequency signals and Chinese reading skills. AimsThe study aims to identify the role of auditory frequency processing in Chinese lexical tone awareness as well as character recognition in Chinese-speaking children. MethodsChildren with (N = 28) and without (N = 27) developmental dyslexia (DD) were recruited. All participants completed two linguistic tasks, Chinese character recognition and lexical tone awareness, and two auditory frequency processing tasks, frequency discrimination and FM sweep direction identification. ResultsThe results revealed that Chinese-speaking children with DD were significantly poorer at all tasks. Particularly, Chinese character recognition was significantly related to FM sweep identification. Lexical tone awareness was significantly associated with both auditory frequency processing tasks. Regression analyses suggested the influence of FM sweep identification on Chinese character recognition contributed through lexical tone awareness. Conclusions and implicationThis study suggests that poor auditory frequency processing may associate with Chinese developmental dyslexia with phonological deficits. In support of the phonological deficit hypothesis, what underlies phonological deficit is likely to be auditory-basis. A potential clinical implication is to reinforce auditory perception and sensitivity through intervention for phonological processing.

Musicians at the Cocktail Party: Neural Substrates of Musical Training During Selective Listening in Multispeaker Situations.

Musical training has been demonstrated to benefit speech-in-noise perception. It is however unknown whether this effect translates to selective listening in cocktail party situations, and if so what its neural basis might be. We investigated this question using magnetoencephalography-based speech envelope reconstruction and a sustained selective listening task, in which participants with varying amounts of musical training attended to 1 of 2 speech streams while detecting rare target words. Cortical frequency-following responses (FFR) and auditory working memory were additionally measured to dissociate musical training-related effects on low-level auditory processing versus higher cognitive function. Results show that the duration of musical training is associated with a reduced distracting effect of competing speech on target detection accuracy. Remarkably, more musical training was related to a robust neural tracking of both the to-be-attended and the to-be-ignored speech stream, up until late cortical processing stages. Musical training-related increases in FFR power were associated with a robust speech tracking in auditory sensory areas, whereas training-related differences in auditory working memory were linked to an increased representation of the to-be-ignored stream beyond auditory cortex. Our findings suggest that musically trained persons can use additional information about the distracting stream to limit interference by competing speech.