Garreth Prendergast

Perceptual consequences of "hidden" hearing loss

Dramatic results from recent animal experiments show that noise exposure can cause a selective loss of high-threshold auditory nerve fibers without affecting absolute sensitivity permanently. This cochlear neuropathy has been described as hidden hearing loss, as it is not thought to be detectable using standard measures of audiometric threshold. It is possible that hidden hearing loss is a common condition in humans and may underlie some of the perceptual deficits experienced by people with clinically normal hearing. There is some evidence that a history of noise exposure is associated with difficulties in speech discrimination and temporal processing, even in the absence of any audiometric loss. There is also evidence that the tinnitus experienced by listeners with clinically normal hearing is associated with cochlear neuropathy, as measured using Wave I of the auditory brainstem response. To date, however, there has been no direct link made between noise exposure, cochlear neuropathy, and perceptual difficulties. Animal experiments also reveal that the aging process itself, in the absence of significant noise exposure, is associated with loss of auditory nerve fibers. Evidence from human temporal bone studies and auditory brainstem response measures suggests that this form of hidden loss is common in humans and may have perceptual consequences, in particular, regarding the coding of the temporal aspects of sounds. Hidden hearing loss is potentially a major health issue, and investigations are ongoing to identify the causes and consequences of this troubling condition.

Tinnitus with a normal audiogram: Relation to noise exposure but no evidence for cochlear synaptopathy

&NA; In rodents, exposure to high‐level noise can destroy synapses between inner hair cells and auditory nerve fibers, without causing hair cell loss or permanent threshold elevation. Such “cochlear synaptopathy” is associated with amplitude reductions in wave I of the auditory brainstem response (ABR) at moderate‐to‐high sound levels. Similar ABR results have been reported in humans with tinnitus and normal audiometric thresholds, leading to the suggestion that tinnitus in these cases might be a consequence of synaptopathy. However, the ABR is an indirect measure of synaptopathy and it is unclear whether the results in humans reflect the same mechanisms demonstrated in rodents. Measures of noise exposure were not obtained in the human studies, and high frequency audiometric loss may have impacted ABR amplitudes. To clarify the role of cochlear synaptopathy in tinnitus with a normal audiogram, we recorded ABRs, envelope following responses (EFRs), and noise exposure histories in young adults with tinnitus and matched controls. Tinnitus was associated with significantly greater lifetime noise exposure, despite close matching for age, sex, and audiometric thresholds up to 14 kHz. However, tinnitus was not associated with reduced ABR wave I amplitude, nor with significant effects on EFR measures of synaptopathy. These electrophysiological measures were also uncorrelated with lifetime noise exposure, providing no evidence of noise‐induced synaptopathy in this cohort, despite a wide range of exposures. In young adults with normal audiograms, tinnitus may be related not to cochlear synaptopathy but to other effects of noise exposure. HighlightsTinnitus participants matched with controls for age, sex, & audiogram up to 14 kHz.Tinnitus participants more noise exposed, despite close audiometric matching.No ABR or EFR evidence for cochlear synaptopathy in tinnitus participants.No association between ABR or EFR measures and lifetime noise exposure.

Effects of noise exposure on young adults with normal audiograms I: Electrophysiology

&NA; Noise‐induced cochlear synaptopathy has been demonstrated in numerous rodent studies. In these animal models, the disorder is characterized by a reduction in amplitude of wave I of the auditory brainstem response (ABR) to high‐level stimuli, whereas the response at threshold is unaffected. The aim of the present study was to determine if this disorder is prevalent in young adult humans with normal audiometric hearing. One hundred and twenty six participants (75 females) aged 18–36 were tested. Participants had a wide range of lifetime noise exposures as estimated by a structured interview. Audiometric thresholds did not differ across noise exposures up to 8 kHz, although 16‐kHz audiometric thresholds were elevated with increasing noise exposure for females but not for males. ABRs were measured in response to high‐pass (1.5 kHz) filtered clicks of 80 and 100 dB peSPL. Frequency‐following responses (FFRs) were measured to 80 dB SPL pure tones from 240 to 285 Hz, and to 80 dB SPL 4 kHz pure tones amplitude modulated at frequencies from 240 to 285 Hz (transposed tones). The bandwidth of the ABR stimuli and the carrier frequency of the transposed tones were chosen to target the 3–6 kHz characteristic frequency region which is usually associated with noise damage in humans. The results indicate no relation between noise exposure and the amplitude of the ABR. In particular, wave I of the ABR did not decrease with increasing noise exposure as predicted. ABR wave V latency increased with increasing noise exposure for the 80 dB peSPL click. High carrier‐frequency (envelope) FFR signal‐to‐noise ratios decreased as a function of noise exposure in males but not females. However, these correlations were not significant after the effects of age were controlled. The results suggest either that noise‐induced cochlear synaptopathy is not a significant problem in young, audiometrically normal adults, or that the ABR and FFR are relatively insensitive to this disorder in young humans, although it is possible that the effects become more pronounced with age. HighlightsLarge study on the effects of lifetime noise exposure in normal‐hearing young adults.No clear evidence for noise‐induced cochlear synaptopathy in ABR or FFR measures.Noise exposure associated with elevated 16‐kHz audiometric thresholds in females.

The role of phase-locking to the temporal envelope of speech in auditory perception and speech intelligibility

The temporal envelope of speech is important for speech intelligibility. Entrainment of cortical oscillations to the speech temporal envelope is a putative mechanism underlying speech intelligibility. Here we used magnetoencephalography (MEG) to test the hypothesis that phase-locking to the speech temporal envelope is enhanced for intelligible compared with unintelligible speech sentences. Perceptual “pop-out” was used to change the percept of physically identical tone-vocoded speech sentences from unintelligible to intelligible. The use of pop-out dissociates changes in phase-locking to the speech temporal envelope arising from acoustical differences between un/intelligible speech from changes in speech intelligibility itself. Novel and bespoke whole-head beamforming analyses, based on significant cross-correlation between the temporal envelopes of the speech stimuli and phase-locked neural activity, were used to localize neural sources that track the speech temporal envelope of both intelligible and unintelligible speech. Location-of-interest analyses were carried out in a priori defined locations to measure the representation of the speech temporal envelope for both un/intelligible speech in both the time domain (cross-correlation) and frequency domain (coherence). Whole-brain beamforming analyses identified neural sources phase-locked to the temporal envelopes of both unintelligible and intelligible speech sentences. Crucially there was no difference in phase-locking to the temporal envelope of speech in the pop-out condition in either the whole-brain or location-of-interest analyses, demonstrating that phase-locking to the speech temporal envelope is not enhanced by linguistic information.

Toward a Diagnostic Test for Hidden Hearing Loss

Cochlear synaptopathy (or hidden hearing loss), due to noise exposure or aging, has been demonstrated in animal models using histological techniques. However, diagnosis of the condition in individual humans is problematic because of (a) test reliability and (b) lack of a gold standard validation measure. Wave I of the transient-evoked auditory brainstem response is a noninvasive electrophysiological measure of auditory nerve function and has been validated in the animal models. However, in humans, Wave I amplitude shows high variability both between and within individuals. The frequency-following response, a sustained evoked potential reflecting synchronous neural activity in the rostral brainstem, is potentially more robust than auditory brainstem response Wave I. However, the frequency-following response is a measure of central activity and may be dependent on individual differences in central processing. Psychophysical measures are also affected by intersubject variability in central processing. Differential measures may help to reduce intersubject variability due to unrelated factors. A measure can be compared, within an individual, between conditions that are affected differently by cochlear synaptopathy. Validation of the metrics is also an issue. Comparisons with animal models, computational modeling, auditory nerve imaging, and human temporal bone histology are all potential options for validation, but there are technical and practical hurdles and difficulties in interpretation. Despite the obstacles, a diagnostic test for hidden hearing loss is a worthwhile goal, with important implications for clinical practice and health surveillance.

Magnified neural envelope coding predicts deficits in speech perception in noise

Verbal communication in noisy backgrounds is challenging. Understanding speech in background noise that fluctuates in intensity over time is particularly difficult for hearing-impaired listeners with a sensorineural hearing loss (SNHL). The reduction in fast-acting cochlear compression associated with SNHL exaggerates the perceived fluctuations in intensity in amplitude-modulated sounds. SNHL-induced changes in the coding of amplitude-modulated sounds may have a detrimental effect on the ability of SNHL listeners to understand speech in the presence of modulated background noise. To date, direct evidence for a link between magnified envelope coding and deficits in speech identification in modulated noise has been absent. Here, magnetoencephalography was used to quantify the effects of SNHL on phase locking to the temporal envelope of modulated noise (envelope coding) in human auditory cortex. Our results show that SNHL enhances the amplitude of envelope coding in posteromedial auditory cortex, whereas it enhances the fidelity of envelope coding in posteromedial and posterolateral auditory cortex. This dissociation was more evident in the right hemisphere, demonstrating functional lateralization in enhanced envelope coding in SNHL listeners. However, enhanced envelope coding was not perceptually beneficial. Our results also show that both hearing thresholds and, to a lesser extent, magnified cortical envelope coding in left posteromedial auditory cortex predict speech identification in modulated background noise. We propose a framework in which magnified envelope coding in posteromedial auditory cortex disrupts the segregation of speech from background noise, leading to deficits in speech perception in modulated background noise. SIGNIFICANCE STATEMENT People with hearing loss struggle to follow conversations in noisy environments. Background noise that fluctuates in intensity over time poses a particular challenge. Using magnetoencephalography, we demonstrate anatomically distinct cortical representations of modulated noise in normal-hearing and hearing-impaired listeners. This work provides the first link among hearing thresholds, the amplitude of cortical representations of modulated sounds, and the ability to understand speech in modulated background noise. In light of previous work, we propose that magnified cortical representations of modulated sounds disrupt the separation of speech from modulated background noise in auditory cortex.

Effects of noise exposure on young adults with normal audiograms II: Behavioral measures

ABSTRACT An estimate of lifetime noise exposure was used as the primary predictor of performance on a range of behavioral tasks: frequency and intensity difference limens, amplitude modulation detection, interaural phase discrimination, the digit triplet speech test, the co‐ordinate response speech measure, an auditory localization task, a musical consonance task and a subjective report of hearing ability. One hundred and thirty‐eight participants (81 females) aged 18–36 years were tested, with a wide range of self‐reported noise exposure. All had normal pure‐tone audiograms up to 8 kHz. It was predicted that increased lifetime noise exposure, which we assume to be concordant with noise‐induced cochlear synaptopathy, would elevate behavioral thresholds, in particular for stimuli with high levels in a high spectral region. However, the results showed little effect of noise exposure on performance. There were a number of weak relations with noise exposure across the test battery, although many of these were in the opposite direction to the predictions, and none were statistically significant after correction for multiple comparisons. There were also no strong correlations between electrophysiological measures of synaptopathy published previously and the behavioral measures reported here. Consistent with our previous electrophysiological results, the present results provide no evidence that noise exposure is related to significant perceptual deficits in young listeners with normal audiometric hearing. It is possible that the effects of noise‐induced cochlear synaptopathy are only measurable in humans with extreme noise exposures, and that these effects always co‐occur with a loss of audiometric sensitivity. HIGHLIGHTSLarge study on the effects of lifetime noise exposure in normal‐hearing young adults.Performance on a range of behavioral tasks unrelated to noise exposure history.Effects of cochlear synaptopathy not evident in young audiometrically normal cohort.

MEG Adaptation Resolves the Spatiotemporal Characteristics of Face-Sensitive Brain Responses

An unresolved goal in face perception is to identify brain areas involved in face processing and simultaneously understand the timing of their involvement. Currently, high spatial resolution imaging techniques identify the fusiform gyrus as subserving processing of invariant face features relating to identity. High temporal resolution imaging techniques localize an early latency evoked component—the N/M170—as having a major generator in the fusiform region; however, this evoked component is not believed to be associated with the processing of identity. To resolve this, we used novel magnetoencephalographic beamformer analyses to localize cortical regions in humans spatially with trial-by-trial activity that differentiated faces and objects and to interrogate their functional sensitivity by analyzing the effects of stimulus repetition. This demonstrated a temporal sequence of processing that provides category-level and then item-level invariance. The right fusiform gyrus showed adaptation to faces (not objects) at ∼150 ms after stimulus onset regardless of face identity; however, at the later latency of ∼200–300 ms, this area showed greater adaptation to repeated identity faces than to novel identities. This is consistent with an involvement of the fusiform region in both early and midlatency face-processing operations, with only the latter showing sensitivity to invariant face features relating to identity. SIGNIFICANCE STATEMENT Neuroimaging techniques with high spatial-resolution have identified brain structures that are reliably activated when viewing faces and techniques with high temporal resolution have identified the time-varying temporal signature of the brains response to faces. However, until now, colocalizing face-specific mechanisms in both time and space has proven notoriously difficult. Here, we used novel magnetoencephalographic analysis techniques to spatially localize cortical regions with trial-by-trial temporal activity that differentiates between faces and objects and to interrogate their functional sensitivity by analyzing effects of stimulus repetition on the time-locked signal. These analyses confirm a role for the right fusiform region in early to midlatency responses consistent with face identity processing and convincingly deliver upon magnetoencephalographys promise to resolve brain signals in time and space simultaneously.

Neural mechanisms underlying song and speech perception can be differentiated using an illusory percept.

The issue of whether human perception of speech and song recruits integrated or dissociated neural systems is contentious. This issue is difficult to address directly since these stimulus classes differ in their physical attributes. We therefore used a compelling illusion (Deutsch et al. 2011) in which acoustically identical auditory stimuli are perceived as either speech or song. Deutschs illusion was used in a functional MRI experiment to provide a direct, within-subject investigation of the brain regions involved in the perceptual transformation from speech into song, independent of the physical characteristics of the presented stimuli. An overall differential effect resulting from the perception of song compared with that of speech was revealed in right midposterior superior temporal sulcus/right middle temporal gyrus. A left frontotemporal network, previously implicated in higher-level cognitive analyses of music and speech, was found to co-vary with a behavioural measure of the subjective vividness of the illusion, and this effect was driven by the illusory transformation. These findings provide evidence that illusory song perception is instantiated by a network of brain regions that are predominantly shared with the speech perception network.

The Physiological Bases of Hidden Noise-Induced Hearing Loss: Protocol for a Functional Neuroimaging Study

Background Rodent studies indicate that noise exposure can cause permanent damage to synapses between inner hair cells and high-threshold auditory nerve fibers, without permanently altering threshold sensitivity. These demonstrations of what is commonly known as hidden hearing loss have been confirmed in several rodent species, but the implications for human hearing are unclear. Objective Our Medical Research Council–funded program aims to address this unanswered question, by investigating functional consequences of the damage to the human peripheral and central auditory nervous system that results from cumulative lifetime noise exposure. Behavioral and neuroimaging techniques are being used in a series of parallel studies aimed at detecting hidden hearing loss in humans. The planned neuroimaging study aims to (1) identify central auditory biomarkers associated with hidden hearing loss; (2) investigate whether there are any additive contributions from tinnitus or diminished sound tolerance, which are often comorbid with hearing problems; and (3) explore the relation between subcortical functional magnetic resonance imaging (fMRI) measures and the auditory brainstem response (ABR). Methods Individuals aged 25 to 40 years with pure tone hearing thresholds ≤20 dB hearing level over the range 500 Hz to 8 kHz and no contraindications for MRI or signs of ear disease will be recruited into the study. Lifetime noise exposure will be estimated using an in-depth structured interview. Auditory responses throughout the central auditory system will be recorded using ABR and fMRI. Analyses will focus predominantly on correlations between lifetime noise exposure and auditory response characteristics. Results This paper reports the study protocol. The funding was awarded in July 2013. Enrollment for the study described in this protocol commenced in February 2017 and was completed in December 2017. Results are expected in 2018. Conclusions This challenging and comprehensive study will have the potential to impact diagnostic procedures for hidden hearing loss, enabling early identification of noise-induced auditory damage via the detection of changes in central auditory processing. Consequently, this will generate the opportunity to give personalized advice regarding provision of ear defense and monitoring of further damage, thus reducing the incidence of noise-induced hearing loss.