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A rich history of comparative research in the auditory field has afforded a synthetic view of sound information processing by ears and brains. Some organisms have proven to be powerful models for human hearing due to fundamental similarities (e.g., well-matched hearing ranges), while others feature intriguing differences (e.g., atympanic ears) that invite further study. Work across diverse "non-traditional" organisms, from small mammals to avians to amphibians and beyond, continues to propel auditory science forward, netting a variety of biomedical and technological advances along the way. In this brief review, limited primarily to tetrapod vertebrates, we discuss the continued importance of comparative studies in hearing research from the periphery to central nervous system with a focus on outstanding questions such as mechanisms for sound capture, peripheral and central processing of directional/spatial information, and non-canonical auditory processing, including efferent and hormonal effects., Competing Interests: Declaration of Competing Interest The authors declare no competing interests, (Copyright © 2023 The Author(s). Published by Elsevier B.V. All rights reserved.)

The auditory brain stem response (ABR) is an evoked potential that indexes a cascade of neural events elicited by sound. In the present study we evaluated the influence of sound frequency on a derived component of the ABR known as the binaural interaction component (BIC). Specifically, we evaluated the effect of acoustic interaural (between-ear) frequency mismatch on BIC amplitude. Goals were to 1 ) increase basic understanding of sound features that influence this long-studied auditory potential and 2 ) gain insight about the persistence of the BIC with interaural electrode mismatch in human users of bilateral cochlear implants, presently a limitation on the prospective utility of the BIC in audiological settings. Data were collected in an animal model that is audiometrically similar to humans, the chinchilla ( Chinchilla lanigera ; 6 females). Frequency disparities and amplitudes of acoustic stimuli were varied over broad ranges, and associated variation of BIC amplitude was quantified. Subsequently, responses were simulated with the use of established models of the brain stem pathway thought to underlie the BIC. Collectively, the data demonstrate that at high sound intensities (≥85 dB SPL), the acoustically elicited BIC persisted with interaurally disparate stimulation (click frequencies ≥1.5 octaves apart). However, sharper tuning emerged at moderate sound intensities (65 dB SPL), with the largest BIC occurring for stimulus frequencies within ~0.8 octaves, equivalent to ±1 mm in cochlear place. Such responses were consistent with simulated responses of the presumed brain stem generator of the BIC, the lateral superior olive. The data suggest that leveraging focused electrical stimulation strategies could improve BIC-based bilateral cochlear implant fitting outcomes. NEW & NOTEWORTHY Traditional hearing tests evaluate each ear independently. Diagnosis and treatment of binaural hearing dysfunction remains a basic challenge for hearing clinicians. We demonstrate in an animal model that the prospective utility of a noninvasive electrophysiological signature of binaural function, the binaural interaction component (BIC), depends strongly on the intensity of auditory stimulation. Data suggest that more informative BIC measurements could be obtained with clinical protocols leveraging stimuli restricted in effective bandwidth.

Hypothesis: Intracochlear pressures (PIC) and stapes velocity (Vstap) elicited by bilaterally placed bone-anchored hearing devices (BAHD) will be systematically modulated by imposed interaural time (ITD) and level differences (ILD), demonstrating the potential for users of bilateral BAHD to access these binaural cues., Background: BAHD are traditionally implanted unilaterally under the assumption that transcranial cross-talk limits interaural differences. Recent studies have demonstrated improvements in binaural and spatial performance with bilateral BAHD; however, objective measures of binaural cues from bilateral BAHDs are lacking., Methods: Bone-conduction transducers were coupled to both mastoids of cadaveric specimens via implanted titanium abutments. PIC and Vstap were measured using intracochlear pressure probes and laser Doppler vibrometry, respectively, during stimulation with pure-tone stimuli of varied frequency (250-4000 Hz) under ipsilateral, contralateral, and bilateral ITD (-1 to 1 ms) and ILD (-20 to 20 dB) conditions., Results: Bilateral stimulation produced constructive and destructive interference patterns that varied dramatically with ITD and stimulus frequency. Variation of ITD led to large variation of PIC and Vstap, with opposing effects in ipsilateral and contralateral ears expected to lead to "ITD to ILD conversion." Variation of ILD produced more straightforward (monotonic) variations of PIC and Vstap, with ipsilateral-favoring ILD producing higher PIC and Vstap than contralateral-favoring., Conclusion: Variation of ITDs and ILDs conveyed by BAHDs systematically modulated cochlear inputs. While transcranial cross-talk leads to complex interactions that depend on cue type and stimulus frequency, binaural disparities potentiate binaural benefit, providing a basis for improved sound localization and speech-in-noise perception.

The auditory brainstem response (ABR) is a sound-evoked noninvasively measured electrical potential representing the sum of neuronal activity in the auditory brainstem and midbrain. ABR peak amplitudes and latencies are widely used in human and animal auditory research and for clinical screening. The binaural interaction component (BIC) of the ABR stands for the difference between the sum of the monaural ABRs and the ABR obtained with binaural stimulation. The BIC comprises a series of distinct waves, the largest of which (DN1) has been used for evaluating binaural hearing in both normal hearing and hearing-impaired listeners. Based on data from animal and human studies, the authors discuss the possible anatomical and physiological bases of the BIC (DN1 in particular). The effects of electrode placement and stimulus characteristics on the binaurally evoked ABR are evaluated. The authors review how interaural time and intensity differences affect the BIC and, analyzing these dependencies, draw conclusion about the mechanism underlying the generation of the BIC. Finally, the utility of the BIC for clinical diagnoses are summarized.

The interaural level difference (ILD) cue to sound location is first encoded in the lateral superior olive (LSO). ILD sensitivity results because the LSO receives excitatory input from the ipsilateral cochlear nucleus and inhibitory input indirectly from the contralateral cochlear nucleus via glycinergic neurons of the ipsilateral medial nucleus of the trapezoid body (MNTB). It is hypothesized that in order for LSO neurons to encode ILDs, the sound spectra at both ears must be accurately encoded via spike rate by their afferents. This spectral-coding hypothesis has not been directly tested in MNTB, likely because MNTB neurons have been mostly described and studied recently in regards to their abilities to encode temporal aspects of sounds, not spectral. Here, we test the hypothesis that MNTB neurons and their inputs from the cochlear nucleus and auditory nerve code sound spectra via discharge rate. The Random Spectral Shape (RSS) method was used to estimate how the levels of 100-ms duration spectrally stationary stimuli were weighted, both linearly and non-linearly, across a wide band of frequencies. In general, MNTB neurons, and their globular bushy cell inputs, were found to be well-modeled by a linear weighting of spectra demonstrating that the pathways through the MNTB can accurately encode sound spectra including those resulting from the acoustical cues to sound location provided by head-related directional transfer functions (DTFs). Together with the anatomical and biophysical specializations for timing in the MNTB-LSO complex, these mechanisms may allow ILDs to be computed for complex stimuli with rapid spectrotemporally-modulated envelopes such as speech and animal vocalizations and moving sound sources.

While much is known about the metrics and kinematics of gaze shifts to visual targets in cats, little is known about gaze shifts to auditory targets. Here, cats were trained to localize auditory and visual targets via gaze shifts. Five properties of gaze shifts to sounds were observed. First, gaze shifts were accomplished primarily by large head movements. Unlike primates, the head movement in cats often preceded eye movement though the relative timing of eye in head and head latencies depended upon the target modality and gaze shift magnitude. Second, gaze shift latencies to auditory targets tended to be shorter than equivalent shifts to visual targets for some conditions. Third, the main sequences relating gaze amplitude to maximum gaze velocity for auditory and visual targets were comparable. However, head movements to auditory and visual targets were less consistent than gaze shifts and tended to undershoot the targets by 30 % for both modalities. Fourth, at the end of gaze movement, the proportion of the gaze shift accomplished by the eye-in-head movement was greater to visual than auditory targets. On the other hand, at the end of head movement, the proportion of the gaze shift accomplished by the head was greater to auditory than visual targets. Finally, gaze shifts to long-duration auditory targets were accurate and precise and were similar to accuracy of gaze shifts to long-duration visual targets. Because the metrics of gaze shifts to visual and auditory targets are nearly equivalent, as well as their accuracy, we conclude that both sensorimotor tasks use primarily the same neural substrates for the execution of movement.

For over a century, the Duplex theory has posited that low- and ­high-frequency sounds are localized using two different acoustical cues, interaural time (ITDs) and level (ILDs) differences, respectively. Psychophysical data have generally supported the theory for pure tones. Anatomically, ITDs and ILDs are separately encoded in two parallel brainstem pathways. Acoustically ILDs are a function of location and frequency such that lower and higher frequencies exhibit smaller and larger ILDs, respectively. It is well established that neurons throughout the auditory neuraxis encode high-frequency ILDs. Acoustically, low-frequency ILDs are negligible (∼1–2 dB); however, humans are still sensitive to them and physiological studies often report low-frequency ILD-sensitive neurons. These ­latter findings are at odds with the Duplex theory. We suggest that these discrepancies arise from an inadequate characterization of the acoustical environment. We hypothesize that low-frequency ILDs become large and useful when sources are located near the head. We tested this hypothesis by making measurements of the ILDs in chinchillas as a function of source distance and the sensitivity to ILDs in 103 neurons in the inferior colliculus (IC). The ILD sensitivity of IC neurons was found to be frequency independent even though far-field acoustical ILDs were frequency dependent. However, as source distance was decreased, the magnitudes of low-frequency ILDs increased. Using information theoretic methods, we ­demonstrate that a population of IC neurons can encode the full range of acoustic ILDs across frequency that would be experienced as a joint function of source location and distance.

The lateral superior olive (LSO) is one of the earliest sites in the auditory pathway involved in processing acoustical cues to sound location. LSO neurons encode the interaural level difference (ILD) cue to azimuthal location. Here we investigated the effect of variations in the overall stimulus levels of sounds at the two ears on the sensitivity of LSO neurons to small differences in ILDs of pure tones. The neuronal firing rate versus ILD functions were found to depend greatly on the overall stimulus level, typically shifting along the ILD axis toward the excitatory ear and attaining greater maximal firing rates as stimulus level increased. Seventy-five percent of neurons showed significant shifts with changes in overall sound level. The range of ILDs corresponding to best neural acuity for ILDs shifted accordingly. In a simulation using the empirical data, when the overall stimulus level was randomly changed from one trial to the next, the neural discrimination thresholds for ILD, or ILD acuities, were worsened by 50-60% across the population of neurons relative to fixed stimulus levels whether ILD acuity was measured at the azimuthal midline or the ILD pedestal producing the best acuity. The impairment in ILD discrimination was attributed to the increased neural response variance imparted by varying the stimulus level. These results contrast to those observed in psychophysical studies where ILD discrimination thresholds under similar experimental conditions are invariant to overall changes in stimulus level. A simple computational model that incorporated the antagonistic inputs of bilateral LSO nuclei as well as the dorsal nuclei of the lateral lemniscus to the inferior colliculus produced a more robust encoding of ILD even in the setting of roving stimulus level. Testable predictions of this model and comparison to other computational models addressing stimulus invariance were considered.

Although there have been many anatomical, physiological, and psychophysical studies of auditory development in cat, there have been no comparable studies of the development of the sound pressured transformations by the cat head and pinnae. Because the physical dimensions of the head and pinnae determine the spectral and temporal transformations of sound, as head and pinnae size increase during development, the magnitude and frequency ranges of these transformations are hypothesized to systematically change. This hypothesis was tested by measuring directional transfer functions (DTFs), the directional components of head-related transfer functions, and the linear dimensions of the head and pinnae in cats from the onset of hearing ( approximately 1.5 weeks) through adulthood. Head and pinnae dimensions increased by factors of approximately 2 and approximately 2.5, respectively, reaching adult values by approximately 23 and approximately 16 weeks, respectively. The development of the spectral notch cues to source location, the spatial- and frequency-dependent distributions of DTF amplitude gain (acoustic directionality), maximum gain, and the acoustic axis, and the resonance frequency and associated gain of the ear canal and concha were systematically related to the dimensions of the head and pinnae. These monaural acoustical properties of the head and pinnae in the cat are mature by 16 weeks.

The acoustical cues for sound location are generated by spatial- and frequency-dependent filtering of propagating sound waves by the head and external ears. Although rats have been a common model system for anatomy, physiology, and psychophysics of localization, there have been few studies of the acoustical cues available to rats. Here, directional transfer functions (DTFs), the directional components of the head-related transfer functions, were measured in six adult rats. The cues to location were computed from the DTFs. In the frontal hemisphere, spectral notches were present for frequencies from approximately 16 to 30 kHz; in general, the frequency corresponding to the notch increased with increases in source elevation and in azimuth toward the ipsilateral ear. The maximum high-frequency envelope-based interaural time differences (ITDs) were 130 mus, whereas low-frequency (<3.5 kHz) fine-structure ITDs were 160 mus; both types of ITDs were larger than predicted from spherical head models. Interaural level differences (ILDs) strongly depended on location and frequency. Maximum ILDs were <10 dB for frequencies <8 kHz and were as large as 20-40 dB for frequencies >20 kHz. Removal of the pinna eliminated the spectral notches, reduced the acoustic gain and ILDs, altered the acoustical axis, and reduced the ITDs.

The lateral superior olive (LSO) is believed to encode differences in sound level at the two ears, a cue for azimuthal sound location. Most high-frequency-sensitive LSO neurons are binaural, receiving inputs from both ears. An inhibitory input from the contralateral ear, via the medial nucleus of the trapezoid body (MNTB), and excitatory input from the ipsilateral ear enable level differences to be encoded. However, the classical descriptions of low-frequency-sensitive neurons report primarily monaural cells with no contralateral inhibition. Anatomical and physiological evidence, however, shows that low-frequency LSO neurons receive low-frequency inhibitory input from ipsilateral MNTB, which in turn receives excitatory input from the contralateral cochlear nucleus and low-frequency excitatory input from the ipsilateral cochlear nucleus. Therefore, these neurons would be expected to be binaural with contralateral inhibition. Here, we re-examined binaural interaction in low-frequency (less than approximately 3 kHz) LSO neurons and phase locking in the MNTB. Phase locking to low-frequency tones in MNTB and ipsilaterally driven LSO neurons with frequency sensitivities <1.2 kHz was enhanced relative to the auditory nerve. Moreover, most low-frequency LSO neurons exhibited contralateral inhibition: ipsilaterally driven responses were suppressed by raising the level of the contralateral stimulus; most neurons were sensitive to interaural time delays in pure tone and noise stimuli such that inhibition was nearly maximal when the stimuli were presented to the ears in-phase. The data demonstrate that low-frequency LSO neurons of cat are not monaural and can exhibit contralateral inhibition like their high-frequency counterparts.

Our objective was to examine the effects of hearing aid amplification on auditory detection and discrimination in infants who were hard of hearing (IHH) using a physiological measure of auditory perception. We recorded EEG from 41 sleeping IHH aged 1.04 to 5.62 months while presenting auditory stimuli in a mismatch response paradigm. Responses were recorded during two listening conditions for each participant: aided and unaided. Temporal envelopes of the mismatch response in the EEG alpha band (6–12 Hz) were extracted from the latent, time-frequency transformed data. Aided alpha band responses were greater than unaided responses for the deviant trials but were not different for the standard trials. Responses to the deviant trials were greater than responses to the standard trials for the aided conditions but were not different for the unaided conditions. These results suggest that the alpha band mismatch can be used to examine both detection and discrimination of speech and non-speech sounds in IHH. With further study, the alpha band mismatch could expand and refine our abilities to validate hearing aid fittings at younger ages than current clinical protocols allow. [ABSTRACT FROM AUTHOR]

Life underground often leads to animals having specialized auditory systems to accommodate the constraints of acoustic transmission in tunnels. Despite living underground, naked mole-rats use a highly vocal communication system, implying that they rely on central auditory processing. However, little is known about these animals' central auditory system, and whether it follows a similar developmental time course as other rodents. Naked mole-rats show slowed development in the hippocampus suggesting they have altered brain development compared to other rodents. Here, we measured morphological characteristics and voltage-gated potassium channel Kv3.3 expression and protein levels at different key developmental time points (postnatal days 9, 14, 21 and adulthood) to determine whether the auditory brainstem (lateral superior olive and medial nucleus of the trapezoid body) develops similarly to two common auditory rodent model species: gerbils and mice. Additionally, we measured the hearing onset of naked mole-rats using auditory brainstem response recordings at the same developmental timepoints. In contrast with other work in naked mole-rats showing that they are highly divergent in many aspects of their physiology, we show that naked mole-rats have a similar hearing onset, between postnatal day (P) 9 and P14, to many other rodents. On the other hand, we show some developmental differences, such as a unique morphology and Kv3.3 protein levels in the brainstem. [ABSTRACT FROM AUTHOR]

Temporary conductive hearing loss (CHL) can lead to hearing impairments that persist beyond resolution of the CHL. In particular, unilateral CHL leads to deficits in auditory skills that rely on binaural input (e.g., spatial hearing). Here, we asked whether single neurons in the auditory midbrain, which integrate acoustic inputs from the two ears, are altered by a temporary CHL. We introduced 6 weeks of unilateral CHL to young adult chinchillas via foam earplug. Following CHL removal and restoration of peripheral input, single-unit recordings from inferior colliculus (ICC) neurons revealed the CHL decreased the efficacy of inhibitory input to the ICC contralateral to the earplug and increased inhibitory input ipsilateral to the earplug, effectively creating a higher proportion of monaural responsive neurons than binaural. Moreover, this resulted in a ∼10 dB shift in the coding of a binaural sound location cue (interaural-level difference, ILD) in ICC neurons relative to controls. The direction of the shift was consistent with a compensation of the altered ILDs due to the CHL. ICC neuron responses carried ∼37% less information about ILDs after CHL than control neurons. Cochlear peripheral-evoked responses confirmed that the CHL did not induce damage to the auditory periphery. We find that a temporary CHL altered auditory midbrain neurons by shifting binaural responses to ILD acoustic cues, suggesting a compensatory form of plasticity occurring by at least the level of the auditory midbrain, the ICC. [ABSTRACT FROM AUTHOR]

Sound localization accuracy in elevation can be affected by sound spectrum alteration. Correspondingly, any stimulus manipulation that causes a change in the peripheral representation of the spectrum may degrade localization ability in elevation. The present study examined the influence of sound duration and level on localization performance in cats with the head unrestrained. Two cats were trained using operant conditioning to indicate the apparent location of a sound via gaze shift, which was measured with a search-coil technique. Overall, neither sound level nor duration had a notable effect on localization accuracy in azimuth, except at near-threshold levels. In contrast, localization accuracy in elevation improved as sound duration increased, and sound level also had a large effect on localization in elevation. For short-duration noise, the performance peaked at intermediate levels and deteriorated at low and high levels; for long-duration noise, this "negative level effect" at high levels was not observed. Simulations based on an auditory nerve model were used to explain the above observations and to test several hypotheses. Our results indicated that neither the flatness of sound spectrum (before the sound reaches the inner ear) nor the peripheral adaptation influences spectral coding at the periphery for localization in elevation, whereas neural computation that relies on "multiple looks" of the spectral analysis is critical in explaining the effect of sound duration, but not level. The release of negative level effect observed for long-duration sound could not be explained at the periphery and, therefore, is likely a result of processing at higher centers. [ABSTRACT FROM AUTHOR]

Mammals localize sound sources in azimuth based on two binaural cues, interaural differences in the time of arrival and level of the sounds at the ears. In contrast, the cue for elevation is based on patterns of the broadband power spectra at each ear that result from the direction-dependent acoustic filtering properties of the head and pinnae. Although the exact form of this "spectral shape" cue is unknown, most attention has been directed toward a prominent direction-dependent energy minimum, or "notch," because its location in frequency, for both humans and cats, moves predictably from low to high as a source is moved from low to high elevations. However, there is little direct evidence that these spectral notches are important elevational cues in animals other than humans. Here we demonstrate a striking illusion in the localization of sounds in elevation by cats using stimulus configurations that elicit summing localization and the precedence effect that can be explained by spectral shape cues. [ABSTRACT FROM AUTHOR]