Evidence of noise-induced subclinical hearing loss using auditory brainstem responses and objective measures of noise exposure in humans.

Exposure to loud sound places the auditory system at considerable risk, especially when the exposure is routine. The current study examined the impact of routine auditory overexposure in young human adults with clinically-normal audiometric thresholds by measuring the auditory brainstem response (ABR), an electrophysiological measure of peripheral and central auditory processing. Sound exposure was measured objectively with body-worn noise dosimeters over a week. Participants were divided into low-exposure and high-exposure groups, with the low-exposure group having an average daily noise exposure dose of ∼11% of the recommended exposure limit compared to the high-exposure group average of nearly 500%. Compared to the low-exposure group, the high-exposure group had delayed ABRs to suprathreshold click stimuli and this prolongation was evident at ABR waves I and III but strongest for V. When peripheral differences were corrected using the I-V interpeak latency, the high-exposure group showed greater taxation at faster stimulus presentation rates than the low-exposure group, suggestive of neural conduction inefficiencies within central auditory structures. Our findings are consistent with the hypothesis that auditory overexposure affects peripheral and central auditory structures even before changes are evident on standard audiometry. We discuss our findings within the context of the larger debate on the mechanisms and manifestations of subclinical hearing loss.

Frequency-dependent fine structure in the frequency-following response: The byproduct of multiple generators.

The frequency-following response (FFR) is an auditory-evoked response recorded at the scalp that captures the spectrotemporal properties of tonal stimuli. Previous investigations report that the amplitude of the FFR fluctuates as a function of stimulus frequency, a phenomenon thought to reflect multiple neural generators phase-locking to the stimulus with different response latencies. When phase-locked responses are offset by different latencies, constructive and destructive phase interferences emerge in the volume-conducted signals, culminating in an attenuation or amplification of the scalp-recorded response in a frequency-specific manner. Borrowing from the literature on the audiogram and otoacoustic emissions (OAEs), we refer to this frequency-specific waxing and waning of the FFR amplitude as fine structure. While prior work on the human FFR was limited by small sets of stimulus frequencies, here, we provide the first systematic investigation of FFR fine structure using a broad stimulus set (90 + frequencies) that spanned the limits of human pitch perception. Consistent with predictions, the magnitude of the FFR response varied systematically as a function of stimulus frequency between 16.35 and 880 Hz. In our dataset, FFR high points (local maxima) emerged at ∼44, 87, 208, and 415 Hz with FFR valleys (local minima) emerging ∼62, 110, 311, and 448 Hz. To investigate whether these amplitude fluctuations are the result of multiple neural generators with distinct latencies, we created a theoretical model of the FFR that included six putative generators. Based on the extant literature on the sources of the FFR, our model adopted latencies characteristic of the cochlear microphonic (0 ms), cochlear nucleus (∼1.25 ms), superior olive (∼3.7 ms), and inferior colliculus (∼5 ms). In addition, we included two longer latency putative generators (∼13 ms, and ∼25 ms) reflective of the characteristic latencies of primary and non-primary auditory cortical structures. Our model revealed that the FFR fine structure observed between 16.35 and 880 Hz can be explained by the phase-interaction patterns created by six generators with relative latencies spaced between 0 and 25 ms. In addition, our model provides confirmatory evidence that both subcortical and cortical structures are activated by low-frequency (<100 Hz) tones, with the cortex being less sensitive to frequencies > 100 Hz. Collectively, these findings highlight (1) that the FFR is a composite response; (2) that the FFR at any given frequency can reflect activity from multiple generators; (3) that the fine-structure pattern between 16.35 and 880 Hz is the collective outcome of short- and long-latency generators; (4) that FFR fine structure is epiphenomenal in that it reflects how volume-conducted electrical potentials originating from different sources with different latencies interact at scalp locations, not how these different sources actually interact in the brain; and (5) that as a byproduct of these phase-interaction patterns low-amplitude responses will emerge at some frequencies, even when the underlying generators are fully functioning. We believe these findings call for a re-examination of how FFR amplitude is interpreted in both clinical and experimental contexts.

Music training improves speech-in-noise perception: Longitudinal evidence from a community-based music program.

Music training may strengthen auditory skills that help children not only in musical performance but in everyday communication. Comparisons of musicians and non-musicians across the lifespan have provided some evidence for a "musician advantage" in understanding speech in noise, although reports have been mixed. Controlled longitudinal studies are essential to disentangle effects of training from pre-existing differences, and to determine how much music training is necessary to confer benefits. We followed a cohort of elementary school children for 2 years, assessing their ability to perceive speech in noise before and after musical training. After the initial assessment, participants were randomly assigned to one of two groups: one group began music training right away and completed 2 years of training, while the second group waited a year and then received 1 year of music training. Outcomes provide the first longitudinal evidence that speech-in-noise perception improves after 2 years of group music training. The children were enrolled in an established and successful community-based music program and followed the standard curriculum, therefore these findings provide an important link between laboratory-based research and real-world assessment of the impact of music training on everyday communication skills.

Impairments in musical abilities reflected in the auditory brainstem: evidence from congenital amusia.

Congenital amusia is a neurogenetic condition, characterized by a deficit in music perception and production, not explained by hearing loss, brain damage or lack of exposure to music. Despite inferior musical performance, amusics exhibit normal auditory cortical responses, with abnormal neural correlates suggested to lie beyond auditory cortices. Here we show, using auditory brainstem responses to complex sounds in humans, that fine-grained automatic processing of sounds is impoverished in amusia. Compared with matched non-musician controls, spectral amplitude was decreased in amusics for higher harmonic components of the auditory brainstem response. We also found a delayed response to the early transient aspects of the auditory stimulus in amusics. Neural measures of spectral amplitude and response timing correlated with participants' behavioral assessments of music processing. We demonstrate, for the first time, that amusia affects how complex acoustic signals are processed in the auditory brainstem. This neural signature of amusia mirrors what is observed in musicians, such that the aspects of the auditory brainstem responses that are enhanced in musicians are degraded in amusics. By showing that gradients of music abilities are reflected in the auditory brainstem, our findings have implications not only for current models of amusia but also for auditory functioning in general.

Auditory brainstem's sensitivity to human voices.

Differentiating between voices is a basic social skill humans acquire early in life. The current study aimed to understand the subcortical mechanisms of voice processing by focusing on the two most important acoustical voice features: the fundamental frequency (F0) and harmonics. We measured frequency following responses in a group of young adults to a naturally produced speech syllable under two linguistic contexts: same-syllable and multiple-syllable. Compared to the same-syllable context, the multiple-syllable context contained more speech cues to aid voice processing. We analyzed the magnitude of the response to the F0 and harmonics between same-talker and multiple-talker conditions within each linguistic context. Results establish that the human auditory brainstem is sensitive to different talkers as shown by enhanced harmonic responses under the multiple-talker compared to the same-talker condition, when the stimulus stream contained multiple syllables. This study thus provides the first electrophysiological evidence of the auditory brainstem's sensitivity to human voices.

Continued maturation of the click-evoked auditory brainstem response in preschoolers.

BACKGROUND: Click-evoked auditory brainstem responses (ABRs) are a valuable tool for probing auditory system function and development. Although it has long been thought that the human auditory brainstem is fully mature by age 2 yr, recent evidence indicates a prolonged developmental trajectory. PURPOSE: The purpose of this study was to determine the time course of ABR maturation in a preschool population and fill a gap in the knowledge of development. RESEARCH DESIGN: Using a cross-sectional design, we investigated the effect of age on absolute latencies, interwave latencies, and amplitudes (waves I, III, V) of the click-evoked ABR. STUDY SAMPLE: A total of 71 preschoolers (ages 3.12-4.99 yr) participated in the study. All had normal peripheral auditory function and IQ. DATA COLLECTION AND ANALYSIS: ABRs to a rarefaction click stimulus presented at 31/sec and 80 dB SPL (73 dB nHL) were recorded monaurally using clinically-standard recording and filtering procedures while the participant sat watching a movie. Absolute latencies, interwave latencies, and amplitudes were then correlated to age. RESULTS: Developmental changes were restricted to absolute latencies. Wave V latency decreased significantly with age, whereas wave I and III latencies remained stable, even in this restricted age range. CONCLUSIONS: The ABR does not remain static after age 2 yr, as seen by a systematic decrease in wave V latency between ages 3 and 5 yr. This finding suggests that the human brainstem has a continued developmental time course during the preschool years. Latency changes in the age 3-5 yr range should be considered when using ABRs as a metric of hearing health.

Stability and plasticity of auditory brainstem function across the lifespan.

The human auditory brainstem is thought to undergo rapid developmental changes early in life until age ∼2 followed by prolonged stability until aging-related changes emerge. However, earlier work on brainstem development was limited by sparse sampling across the lifespan and/or averaging across children and adults. Using a larger dataset than past investigations, we aimed to trace more subtle variations in auditory brainstem function that occur normally from infancy into the eighth decade of life. To do so, we recorded auditory brainstem responses (ABRs) to a click stimulus and a speech syllable (da) in 586 normal-hearing healthy individuals. Although each set of ABR measures (latency, frequency encoding, response consistency, nonstimulus activity) has a distinct developmental profile, across all measures developmental changes were found to continue well past age 2. In addition to an elongated developmental trajectory and evidence for multiple auditory developmental processes, we revealed a period of overshoot during childhood (5-11 years old) for latency and amplitude measures, when the latencies are earlier and the amplitudes are greater than the adult value. Our data also provide insight into the capacity for experience-dependent auditory plasticity at different stages in life and underscore the importance of using age-specific norms in clinical and experimental applications.

The impoverished brain: disparities in maternal education affect the neural response to sound.

Despite the prevalence of poverty worldwide, little is known about how early socioeconomic adversity affects auditory brain function. Socioeconomically disadvantaged children are underexposed to linguistically and cognitively stimulating environments and overexposed to environmental toxins, including noise pollution. This kind of sensory impoverishment, we theorize, has extensive repercussions on how the brain processes sound. To characterize how this impoverishment affects auditory brain function, we compared two groups of normal-hearing human adolescents who attended the same schools and who were matched in age, sex, and ethnicity, but differed in their maternal education level, a correlate of socioeconomic status (SES). In addition to lower literacy levels and cognitive abilities, adolescents from lower maternal education backgrounds were found to have noisier neural activity than their classmates, as reflected by greater activity in the absence of auditory stimulation. Additionally, in the lower maternal education group, the neural response to speech was more erratic over repeated stimulation, with lower fidelity to the input signal. These weaker, more variable, and noisier responses are suggestive of an inefficient auditory system. By studying SES within a neuroscientific framework, we have the potential to expand our understanding of how experience molds the brain, in addition to informing intervention research aimed at closing the achievement gap between high-SES and low-SES children.

A little goes a long way: how the adult brain is shaped by musical training in childhood.

Playing a musical instrument changes the anatomy and function of the brain. But do these changes persist after music training stops? We probed this question by measuring auditory brainstem responses in a cohort of healthy young human adults with varying amounts of past musical training. We show that adults who received formal music instruction as children have more robust brainstem responses to sound than peers who never participated in music lessons and that the magnitude of the response correlates with how recently training ceased. Our results suggest that neural changes accompanying musical training during childhood are retained in adulthood. These findings advance our understanding of long-term neuroplasticity and have general implications for the development of effective auditory training programs.

Subcortical encoding of sound is enhanced in bilinguals and relates to executive function advantages.

Bilingualism profoundly affects the brain, yielding functional and structural changes in cortical regions dedicated to language processing and executive function [Crinion J, et al. (2006) Science 312:1537-1540; Kim KHS, et al. (1997) Nature 388:171-174]. Comparatively, musical training, another type of sensory enrichment, translates to expertise in cognitive processing and refined biological processing of sound in both cortical and subcortical structures. Therefore, we asked whether bilingualism can also promote experience-dependent plasticity in subcortical auditory processing. We found that adolescent bilinguals, listening to the speech syllable [da], encoded the stimulus more robustly than age-matched monolinguals. Specifically, bilinguals showed enhanced encoding of the fundamental frequency, a feature known to underlie pitch perception and grouping of auditory objects. This enhancement was associated with executive function advantages. Thus, through experience-related tuning of attention, the bilingual auditory system becomes highly efficient in automatically processing sound. This study provides biological evidence for system-wide neural plasticity in auditory experts that facilitates a tight coupling of sensory and cognitive functions.

Harmonic relationships influence auditory brainstem encoding of chords.

The cortical processing of musical sounds is influenced by listeners' sensitivity to the structural regularities of music, and particularly by sensitivity to harmonic relationships. As subcortical and cortical processing dynamically interact to shape auditory perception in an experience-dependent manner, we asked whether subcortical processing of musical sounds would be sensitive to harmonic relationships. We examined auditory brainstem responses to a chord that was preceded either by a harmonically related chord, by an unrelated chord, or was repeated. We observed higher spectral response magnitudes in the related than in the unrelated or repeated conditions, for both musician and nonmusician listeners. Our results suggest that listeners' implicit knowledge of musical regularities influences subcortical auditory processing.

Perception of speech in noise: neural correlates.

The presence of irrelevant auditory information (other talkers, environmental noises) presents a major challenge to listening to speech. The fundamental frequency (F(0)) of the target speaker is thought to provide an important cue for the extraction of the speaker's voice from background noise, but little is known about the relationship between speech-in-noise (SIN) perceptual ability and neural encoding of the F(0). Motivated by recent findings that music and language experience enhance brainstem representation of sound, we examined the hypothesis that brainstem encoding of the F(0) is diminished to a greater degree by background noise in people with poorer perceptual abilities in noise. To this end, we measured speech-evoked auditory brainstem responses to /da/ in quiet and two multitalker babble conditions (two-talker and six-talker) in native English-speaking young adults who ranged in their ability to perceive and recall SIN. Listeners who were poorer performers on a standardized SIN measure demonstrated greater susceptibility to the degradative effects of noise on the neural encoding of the F(0). Particularly diminished was their phase-locked activity to the fundamental frequency in the portion of the syllable known to be most vulnerable to perceptual disruption (i.e., the formant transition period). Our findings suggest that the subcortical representation of the F(0) in noise contributes to the perception of speech in noisy conditions.

Brainstem correlates of speech-in-noise perception in children.

Children often have difficulty understanding speech in challenging listening environments. In the absence of peripheral hearing loss, these speech perception difficulties may arise from dysfunction at more central levels in the auditory system, including subcortical structures. We examined brainstem encoding of pitch in a speech syllable in 38 school-age children. In children with poor speech-in-noise perception, we find impaired encoding of the fundamental frequency and the second harmonic, two important cues for pitch perception. Pitch, an essential factor in speaker identification, aids the listener in tracking a specific voice from a background of voices. These results suggest that the robustness of subcortical neural encoding of pitch features in time-varying signals is a key factor in determining success with perceiving speech in noise.

Stimulus rate and subcortical auditory processing of speech.

Many sounds in the environment, including speech, are temporally dynamic. The auditory brainstem is exquisitely sensitive to temporal features of the incoming acoustic stream, and by varying the speed of presentation of these auditory signals it is possible to investigate the precision with which temporal cues are represented at a subcortical level. Therefore, to determine the effects of stimulation rate on the auditory brainstem response (ABR), we recorded evoked responses to both a click and a consonant-vowel speech syllable (/da/) presented at three rates (15.4, 10.9 and 6.9 Hz). We hypothesized that stimulus rate affects the onset to speech-evoked responses to a greater extent than click-evoked responses and that subcomponents of the speech- ABR are distinctively affected. While the click response was invariant with changes in stimulus rate, timing of the onset response to /da/ varied systematically, increasing in peak latency as presentation rate increased. Contrasts between the click- and speech-evoked onset responses likely reflect acoustic differences, where the speech stimulus onset is more gradual, has more delineated spectral information, and is more susceptible to backward masking by the subsequent formant transition. The frequency-following response (FFR) was also rate dependent, with response magnitude of the higher frequencies (>400 Hz), but not the frequencies corresponding to the fundamental frequency, diminishing with increasing rate. The selective impact of rate on high-frequency components of the FFR implicates the involvement of distinct underlying neural mechanisms for high- versus low-frequency components of the response. Furthermore, the different rate sensitivities of the speech-evoked onset response and subcomponents of the FFR support the involvement of different neural streams for these two responses. Taken together, these differential effects of rate on the ABR components likely reflect distinct aspects of auditory function such that varying rate of presentation of complex stimuli may be expected to elicit unique patterns of abnormality, depending on the clinical population.

Auditory brain stem response to complex sounds: a tutorial.

This tutorial provides a comprehensive overview of the methodological approach to collecting and analyzing auditory brain stem responses to complex sounds (cABRs). cABRs provide a window into how behaviorally relevant sounds such as speech and music are processed in the brain. Because temporal and spectral characteristics of sounds are preserved in this subcortical response, cABRs can be used to assess specific impairments and enhancements in auditory processing. Notably, subcortical auditory function is neither passive nor hardwired but dynamically interacts with higher-level cognitive processes to refine how sounds are transcribed into neural code. This experience-dependent plasticity, which can occur on a number of time scales (e.g., life-long experience with speech or music, short-term auditory training, on-line auditory processing), helps shape sensory perception. Thus, by being an objective and noninvasive means for examining cognitive function and experience-dependent processes in sensory activity, cABRs have considerable utility in the study of populations where auditory function is of interest (e.g., auditory experts such as musicians, and persons with hearing loss, auditory processing, and language disorders). This tutorial is intended for clinicians and researchers seeking to integrate cABRs into their clinical or research programs.

Emotion and the auditory brainstem response to speech.

Effects of emotion have been reported as early as 20 ms after an auditory stimulus onset for negative valence, and bivalent effects between 30 and 130 ms. To understand how emotional state influences the listener's brainstem evoked responses to speech, subjects looked at emotion-evoking pictures while listening to an unchanging auditory stimulus (danny). The pictures (positive, negative, or neutral valence) were selected from the IAPS database and controlled for dominance and arousal. Utilizing an array of measurements to assess subcortical modulation, we have found that emotion does not substantially alter brainstem alter although there is a subtle effect of background noise suppression in both emotional conditions.

Musical experience limits the degradative effects of background noise on the neural processing of sound.

Musicians have lifelong experience parsing melodies from background harmonies, which can be considered a process analogous to speech perception in noise. To investigate the effect of musical experience on the neural representation of speech-in-noise, we compared subcortical neurophysiological responses to speech in quiet and noise in a group of highly trained musicians and nonmusician controls. Musicians were found to have a more robust subcortical representation of the acoustic stimulus in the presence of noise. Specifically, musicians demonstrated faster neural timing, enhanced representation of speech harmonics, and less degraded response morphology in noise. Neural measures were associated with better behavioral performance on the Hearing in Noise Test (HINT) for which musicians outperformed the nonmusician controls. These findings suggest that musical experience limits the negative effects of competing background noise, thereby providing the first biological evidence for musicians' perceptual advantage for speech-in-noise.

Musician enhancement for speech-in-noise.

OBJECTIVE: To investigate the effect of musical training on speech-in-noise (SIN) performance, a complex task requiring the integration of working memory and stream segregation as well as the detection of time-varying perceptual cues. Previous research has indicated that, in combination with lifelong experience with musical stream segregation, musicians have better auditory perceptual skills and working memory. It was hypothesized that musicians would benefit from these factors and perform better on speech perception in noise than age-matched nonmusician controls. DESIGN: The performance of 16 musicians and 15 nonmusicians was compared on clinical measures of speech perception in noise-QuickSIN and Hearing-In-Noise Test (HINT). Working memory capacity and frequency discrimination were also assessed. All participants had normal hearing and were between the ages of 19 and 31 yr. To be categorized as a musician, participants needed to have started musical training before the age of 7 yr, have 10 or more years of consistent musical experience, and have practiced more than three times weekly within the 3 yr before study enrollment. Nonmusicians were categorized by the failure to meet the musician criteria, along with not having received musical training within the 7 yr before the study. RESULTS: Musicians outperformed the nonmusicians on both QuickSIN and HINT, in addition to having more fine-grained frequency discrimination and better working memory. Years of consistent musical practice correlated positively with QuickSIN, working memory, and frequency discrimination but not HINT. The results also indicate that working memory and frequency discrimination are more important for QuickSIN than for HINT. CONCLUSIONS: Musical experience appears to enhance the ability to hear speech in challenging listening environments. Large group differences were found for QuickSIN, and the results also suggest that this enhancement is derived in part from musicians' enhanced working memory and frequency discrimination. For HINT, in which performance was not linked to frequency discrimination ability and was only moderately linked to working memory, musicians still performed significantly better than the nonmusicians. The group differences for HINT were evident in the most difficult condition in which the speech and noise were presented from the same location and not spatially segregated. Understanding which cognitive and psychoacoustic factors as well as which lifelong experiences contribute to SIN may lead to more effective remediation programs for clinical populations for whom SIN poses a particular perceptual challenge. These results provide further evidence for musical training transferring to nonmusical domains and highlight the importance of taking musical training into consideration when evaluating a person's SIN ability in a clinical setting.

Selective subcortical enhancement of musical intervals in musicians.

By measuring the auditory brainstem response to two musical intervals, the major sixth (E3 and G2) and the minor seventh (E3 and F#2), we found that musicians have a more specialized sensory system for processing behaviorally relevant aspects of sound. Musicians had heightened responses to the harmonics of the upper tone (E), as well as certain combination tones (sum tones) generated by nonlinear processing in the auditory system. In music, the upper note is typically carried by the upper voice, and the enhancement of the upper tone likely reflects musicians' extensive experience attending to the upper voice. Neural phase locking to the temporal periodicity of the amplitude-modulated envelope, which underlies the perception of musical harmony, was also more precise in musicians than nonmusicians. Neural enhancements were strongly correlated with years of musical training, and our findings, therefore, underscore the role that long-term experience with music plays in shaping auditory sensory encoding.

Musical experience and neural efficiency: effects of training on subcortical processing of vocal expressions of emotion.

Musicians exhibit enhanced perception of emotion in speech, although the biological foundations for this advantage remain unconfirmed. In order to gain a better understanding for the influences of musical experience on neural processing of emotionally salient sounds, we recorded brainstem potentials to affective human vocal sounds. Musicians showed enhanced time-domain response magnitude to the most spectrally complex portion of the stimulus and decreased magnitude to the more periodic, less complex portion. Enhanced phase-locking to stimulus periodicity was likewise seen in musicians' responses to the complex portion. These results suggest that auditory expertise engenders both enhancement and efficiency of subcortical neural responses that are intricately connected with acoustic features important for the communication of emotional states. Our findings provide the first biological evidence for behavioral observations indicating that musical training enhances the perception of vocally expressed emotion in addition to establishing a subcortical role in the auditory processing of emotional cues.