Cortical compensation for hearing loss, but not age, in neural tracking of the fundamental frequency of the voice.

Auditory processing is affected by advancing age and hearing loss, but the underlying mechanisms are still unclear. We investigated the effects of age and hearing loss on temporal processing of naturalistic stimuli in the auditory system. We used a recently developed objective measure for neural phase-locking to the fundamental frequency of the voice (f0) which uses continuous natural speech as a stimulus, that is, "f0-tracking." The f0-tracking responses from 54 normal-hearing and 14 hearing-impaired adults of varying ages were analyzed. The responses were evoked by a Flemish story with a male talker and contained contributions from both subcortical and cortical sources. Results indicated that advancing age was related to smaller responses with less cortical response contributions. This is consistent with an age-related decrease in neural phase-locking ability at frequencies in the range of the f0, possibly due to decreased inhibition in the auditory system. Conversely, hearing-impaired subjects displayed larger responses compared with age-matched normal-hearing controls. This was due to additional cortical response contributions in the 38- to 50-ms latency range, which were stronger for participants with more severe hearing loss. This is consistent with hearing-loss-induced cortical reorganization and recruitment of additional neural resources to aid in speech perception.NEW & NOTEWORTHY Previous studies disagree on the effects of age and hearing loss on the neurophysiological processing of the fundamental frequency of the voice (f0), in part due to confounding effects. Using a novel electrophysiological technique, natural speech stimuli, and controlled study design, we quantified and disentangled the effects of age and hearing loss on neural f0 processing. We uncovered evidence for underlying neurophysiological mechanisms, including a cortical compensation mechanism for hearing loss, but not for age.

Neural tracking of the fundamental frequency of the voice: The effect of voice characteristics.

Traditional electrophysiological methods to study temporal auditory processing of the fundamental frequency of the voice (f0) often use unnaturally repetitive stimuli. In this study, we investigated f0 processing of meaningful continuous speech. EEG responses evoked by stories in quiet were analysed with a novel method based on linear modelling that characterizes the neural tracking of the f0. We studied both the strength and the spatio-temporal properties of the f0-tracking response. Moreover, different samples of continuous speech (six stories by four speakers: two male and two female) were used to investigate the effect of voice characteristics on the f0 response. The results indicated that response strength is inversely related to f0 frequency and rate of f0 change throughout the story. As a result, the male-narrated stories in this study (low and steady f0) evoked stronger f0-tracking compared to female-narrated stories (high and variable f0), for which many responses were not significant. The spatio-temporal analysis revealed that f0-tracking response generators were not fixed in the brainstem but were voice-dependent as well. Voices with high and variable f0 evoked subcortically dominated responses with a latency between 7 and 12 ms. Voices with low and steady f0 evoked responses that are both subcortically (latency of 13-15 ms) and cortically (latency of 23-26 ms) generated, with the right primary auditory cortex as a likely cortical source. Finally, additional experiments revealed that response strength greatly improves for voices with strong higher harmonics, which is particularly useful to boost the small responses evoked by voices with high f0.

Neural tracking as a diagnostic tool to assess the auditory pathway.

When a person listens to sound, the brain time-locks to specific aspects of the sound. This is called neural tracking and it can be investigated by analysing neural responses (e.g., measured by electroencephalography) to continuous natural speech. Measures of neural tracking allow for an objective investigation of a range of auditory and linguistic processes in the brain during natural speech perception. This approach is more ecologically valid than traditional auditory evoked responses and has great potential for research and clinical applications. This article reviews the neural tracking framework and highlights three prominent examples of neural tracking analyses: neural tracking of the fundamental frequency of the voice (f0), the speech envelope and linguistic features. Each of these analyses provides a unique point of view into the human brain's hierarchical stages of speech processing. F0-tracking assesses the encoding of fine temporal information in the early stages of the auditory pathway, i.e., from the auditory periphery up to early processing in the primary auditory cortex. Envelope tracking reflects bottom-up and top-down speech-related processes in the auditory cortex and is likely necessary but not sufficient for speech intelligibility. Linguistic feature tracking (e.g. word or phoneme surprisal) relates to neural processes more directly related to speech intelligibility. Together these analyses form a multi-faceted objective assessment of an individual's auditory and linguistic processing.

Enhanced Neural Tracking of the Fundamental Frequency of the Voice.

OBJECTIVE: 'F0 tracking' is a novel method that investigates neural processing of the fundamental frequency of the voice (f0) in continuous speech. Using linear modelling, a feature that reflects the f0 of a presented speech stimulus is predicted from neural EEG responses. The correlation between the predicted and the 'actual' f0 feature is a measure for neural response strength. In this study, we aimed to design a new f0 feature that approximates the expected human EEG response to the f0 in order to improve neural tracking results. METHODS: Two techniques were explored: constructing the feature with a phenomenological model to simulate neural processing in the auditory periphery and low-pass filtering the feature to approximate the effect of more central processing. RESULTS: Analysis of EEG-data evoked by a Flemish story in 34 subjects indicated that both the auditory model and the low-pass filter significantly improved the correlations between the actual and reconstructed feature. The combination of both strategies almost doubled the mean correlation across subjects, from 0.078 to 0.13. Moreover, canonical correlation analysis revealed two distinct processes contributing to the f0 response: one driven by broad range of auditory nerve fibers with center frequency up to 8 kHz and one driven by a more narrow selection of auditory nerve fibers, possibly responding to unresolved harmonics. CONCLUSION: Optimizing the f0 feature towards the expected neural response, significantly improves f0-tracking correlations. SIGNIFICANCE: The optimized f0 feature enhances the f0-tracking method, facilitating future research on temporal auditory processing in the human brain.

From modulated noise to natural speech: The effect of stimulus parameters on the envelope following response.

Envelope following responses (EFRs) can be evoked by a wide range of auditory stimuli, but for many stimulus parameters the effect on EFR strength is not fully understood. This complicates the comparison of earlier studies and the design of new studies. Furthermore, the most optimal stimulus parameters are unknown. To help resolve this issue, we investigated the effects of four important stimulus parameters and their interactions on the EFR. Responses were measured in 16 normal hearing subjects evoked by stimuli with four levels of stimulus complexity (amplitude modulated noise, artificial vowels, natural vowels and vowel-consonant-vowel combinations), three fundamental frequencies (105 Hz, 185 Hz and 245 Hz), three fundamental frequency contours (upward sweeping, downward sweeping and flat) and three vowel identities (Flemish /a:/, /u:/, and /i:/). We found that EFRs evoked by artificial vowels were on average 4-6 dB SNR larger than responses evoked by the other stimulus complexities, probably because of (unnaturally) strong higher harmonics. Moreover, response amplitude decreased with fundamental frequency but response SNR remained largely unaffected. Thirdly, fundamental frequency variation within the stimulus did not impact EFR strength, but only when rate of change remained low (e.g. not the case for sweeping natural vowels). Finally, the vowel /i:/ appeared to evoke larger response amplitudes compared to /a:/ and /u:/, but analysis power was too small to confirm this statistically. Vowel-dependent differences in response strength have been suggested to stem from destructive interference between response components. We show how a model of the auditory periphery can simulate these interference patterns and predict response strength. Altogether, the results of this study can guide stimulus choice for future EFR research and practical applications.

The effect of stimulus envelope shape on the auditory steady-state response.

Auditory steady-state responses (ASSRs) are auditory evoked potentials that reflect phase-locked neural activity to periodic stimuli. ASSRs are often evoked by tones with a modulated envelope, with sinusoidal envelopes being most common. However, it is unclear if and how the shape of the envelope affects ASSR responses. In this study, we used various trapezoidal modulated tones to evoke ASSRs (modulation frequency = 40 Hz) and studied the effect of four envelope parameters: attack time, hold time, decay time and off time. ASSR measurements in 20 normal hearing subjects showed that envelope shape significantly influenced responses: increased off time and/or increased decay time led to responses with a larger signal-to-noise-ratio (SNR). Response phase delay was significantly influenced by attack time and to a lesser degree by off time. We also simulated neural population responses that approximate ASSRs with a model of the auditory periphery (Bruce et al. 2018). The modulation depth of the simulated responses, i.e. the difference between maximum and minimum firing rate, correlated highly with the response SNRs found in the ASSR measurements. Longer decay time and off time enhanced the modulation depth both by decreasing the minimum firing rate and by increasing the maximum firing rate. In conclusion, custom envelopes with long decay and off time provide larger response SNRs and the benefit over the commonly used sinusoidal envelope was in the range of several dB.