WHAT MAKES HUMAN HEARING SPECIAL?

Humans and many other animals can hear a wide range of sounds. We can hear low and high notes and both quiet and loud sounds. We are also very good at telling the difference between sounds that are similar, like the speech sounds "argh" and "ah," and picking apart sounds that are mixed together, like when an orchestra is playing. But how do human hearing abilities compare to those of other animals? In this article, we discover how the inner ear determines hearing abilities. Many other mammals can hear very high notes that we cannot, and some can hear quiet sounds that we cannot. However, humans may be better than any other species at distinguishing similar sounds. We know this because, milliseconds after the sounds around us go into our ears, other sounds come out: sounds that are actually produced by those same ears!

Overtone focusing in biphonic tuvan throat singing.

Khoomei is a unique singing style originating from the republic of Tuva in central Asia. Singers produce two pitches simultaneously: a booming low-frequency rumble alongside a hovering high-pitched whistle-like tone. The biomechanics of this biphonation are not well-understood. Here, we use sound analysis, dynamic magnetic resonance imaging, and vocal tract modeling to demonstrate how biphonation is achieved by modulating vocal tract morphology. Tuvan singers show remarkable control in shaping their vocal tract to narrowly focus the harmonics (or overtones) emanating from their vocal cords. The biphonic sound is a combination of the fundamental pitch and a focused filter state, which is at the higher pitch (1-2 kHz) and formed by merging two formants, thereby greatly enhancing sound-production in a very narrow frequency range. Most importantly, we demonstrate that this biphonation is a phenomenon arising from linear filtering rather than from a nonlinear source.

The republic of Tuva, a remote territory in southern Russia located on the border with Mongolia, is perhaps best known for its vast mountainous geography and the unique cultural practice of "throat singing". These singers simultaneously create two different pitches: a low-pitched drone, along with a hovering whistle above it. This practice has deep cultural roots and has now been shared more broadly via world music performances and the 1999 documentary Genghis Blues. Despite many scientists being fascinated by throat singing, it was unclear precisely how throat singers could create two unique pitches. Singing and speaking in general involves making sounds by vibrating the vocal cords found deep in the throat, and then shaping those sounds with the tongue, teeth and lips as they move up the vocal tract and out of the body. Previous studies using static images taken with magnetic resonance imaging (MRI) suggested how Tuvan singers might produce the two pitches, but a mechanistic understanding of throat singing was far from complete. Now, Bergevin et al. have better pinpointed how throat singers can produce their unique sound. The analysis involved high quality audio recordings of three Tuvan singers and dynamic MRI recordings of the movements of one of those singers. The images showed changes in the singer's vocal tract as they sang inside an MRI scanner, providing key information needed to create a computer model of the process. This approach revealed that Tuvan singers can create two pitches simultaneously by forming precise constrictions in their vocal tract. One key constriction occurs when tip of the tongue nearly touches a ridge on the roof of the mouth, and a second constriction is formed by the base of the tongue. The computer model helped explain that these two constrictions produce the distinctive sounds of throat singing by selectively amplifying a narrow set of high frequency notes that are made by the vocal cords. Together these discoveries show how very small, targeted movements of the tongue can produce distinctive sounds.

Evidence supporting synchrony between two active ears due to interaural coupling.

Motivated by recent developments suggesting that interaural coupling in non-mammals allows for the two active ears to effectively synchronize, this report describes otoacoustic measurements made in the oral cavity of lizards. As expected from that model, spontaneous otoacoustic emissions (SOAEs) were readily measurable in the mouth, which is contiguous with the interaural airspace. Additionally, finite element model calculations were made to simulate the interaural acoustics based upon SOAE-related tympanic membrane vibrational data. Taken together, these data support the notion of two active ears synchronizing by virtue of acoustic coupling and have potential implications for sound localization at low-levels.

Mammalian behavior and physiology converge to confirm sharper cochlear tuning in humans.

Frequency analysis of sound by the cochlea is the most fundamental property of the auditory system. Despite its importance, the resolution of this frequency analysis in humans remains controversial. The controversy persists because the methods used to estimate tuning in humans are indirect and have not all been independently validated in other species. Some data suggest that human cochlear tuning is considerably sharper than that of laboratory animals, while others suggest little or no difference between species. We show here in a single species (ferret) that behavioral estimates of tuning bandwidths obtained using perceptual masking methods, and objective estimates obtained using otoacoustic emissions, both also employed in humans, agree closely with direct physiological measurements from single auditory-nerve fibers. Combined with human behavioral data, this outcome indicates that the frequency analysis performed by the human cochlea is of significantly higher resolution than found in common laboratory animals. This finding raises important questions about the evolutionary origins of human cochlear tuning, its role in the emergence of speech communication, and the mechanisms underlying our ability to separate and process natural sounds in complex acoustic environments.

No otoacoustic evidence for a peripheral basis of absolute pitch.

Absolute pitch (AP) is the ability to identify the perceived pitch of a sound without an external reference. Relatively rare, with an incidence of approximately 1/10,000, the mechanisms underlying AP are not well understood. This study examined otoacoustic emissions (OAEs) to determine if there is evidence of a peripheral (i.e., cochlear) basis for AP. Two OAE types were examined: spontaneous emissions (SOAEs) and stimulus-frequency emissions (SFOAEs). Our motivations to explore a peripheral foundation for AP were several-fold. First is the observation that pitch judgment accuracy has been reported to decrease with age due to age-dependent physiological changes cochlear biomechanics. Second is the notion that SOAEs, which are indirectly related to perception, could act as a fixed frequency reference. Third, SFOAE delays, which have been demonstrated to serve as a proxy measure for cochlear frequency selectivity, could indicate tuning differences between groups. These led us to the hypotheses that AP subjects would (relative to controls) exhibit a. greater SOAE activity and b. sharper cochlear tuning. To test these notions, measurements were made in normal-hearing control (N = 33) and AP-possessor (N = 20) populations. In short, no substantial difference in SOAE activity was found between groups, indicating no evidence for one or more strong SOAEs that could act as a fixed cue. SFOAE phase-gradient delays, measured at several different probe levels (20-50 dB SPL), also showed no significant differences between groups. This observation argues against sharper cochlear frequency selectivity in AP subjects. Taken together, these data support the prevailing view that AP mechanisms predominantly arise at a processing level in the central nervous system (CNS) at the brainstem or higher, not within the cochlea.

Salient features of otoacoustic emissions are common across tetrapod groups and suggest shared properties of generation mechanisms.

Otoacoustic emissions (OAEs) are faint sounds generated by healthy inner ears that provide a window into the study of auditory mechanics. All vertebrate classes exhibit OAEs to varying degrees, yet the biophysical origins are still not well understood. Here, we analyzed both spontaneous (SOAE) and stimulus-frequency (SFOAE) otoacoustic emissions from a bird (barn owl, Tyto alba) and a lizard (green anole, Anolis carolinensis). These species possess highly disparate macromorphologies of the inner ear relative to each other and to mammals, thereby allowing for novel insights into the biomechanical mechanisms underlying OAE generation. All ears exhibited robust OAE activity, and our chief observation was that SFOAE phase accumulation between adjacent SOAE peak frequencies clustered about an integral number of cycles. Being highly similar to published results from human ears, we argue that these data indicate a common underlying generator mechanism of OAEs across all vertebrates, despite the absence of morphological features thought essential to mammalian cochlear mechanics. We suggest that otoacoustic emissions originate from phase coherence in a system of coupled oscillators, which is consistent with the notion of "coherent reflection" but does not explicitly require a mammalian-type traveling wave. Furthermore, comparison between SFOAE delays and auditory nerve fiber responses for the barn owl strengthens the notion that most OAE delay can be attributed to tuning.

External and middle ear sound pressure distribution and acoustic coupling to the tympanic membrane.

Sound energy is conveyed to the inner ear by the diaphanous, cone-shaped tympanic membrane (TM). The TM moves in a complex manner and transmits sound signals to the inner ear with high fidelity, pressure gain, and a short delay. Miniaturized sensors allowing high spatial resolution in small spaces and sensitivity to high frequencies were used to explore how pressure drives the TM. Salient findings are: (1) A substantial pressure drop exists across the TM, and varies in frequency from ∼10 to 30 dB. It thus appears reasonable to approximate the drive to the TM as being defined solely by the pressure in the ear canal (EC) close to the TM. (2) Within the middle ear cavity (MEC), spatial variations in sound pressure could vary by more than 20 dB, and the MEC pressure at certain locations/frequencies was as large as in the EC. (3) Spatial variations in pressure along the TM surface on the EC-side were typically less than 5 dB up to 50 kHz. Larger surface variations were observed on the MEC-side.

Obtaining reliable phase-gradient delays from otoacoustic emission data.

Reflection-source otoacoustic emission phase-gradient delays are widely used to obtain noninvasive estimates of cochlear function and properties, such as the sharpness of mechanical tuning and its variation along the length of the cochlear partition. Although different data-processing strategies are known to yield different delay estimates and trends, their relative reliability has not been established. This paper uses in silico experiments to evaluate six methods for extracting delay trends from reflection-source otoacoustic emissions (OAEs). The six methods include both previously published procedures (e.g., phase smoothing, energy-weighting, data exclusion based on signal-to-noise ratio) and novel strategies (e.g., peak-picking, all-pass factorization). Although some of the methods perform well (e.g., peak-picking), others introduce substantial bias (e.g., phase smoothing) and are not recommended. In addition, since standing waves caused by multiple internal reflection can complicate the interpretation and compromise the application of OAE delays, this paper develops and evaluates two promising signal-processing strategies, the first based on time-frequency filtering using the continuous wavelet transform and the second on cepstral analysis, for separating the direct emission from its subsequent reflections. Altogether, the results help to resolve previous disagreements about the frequency dependence of human OAE delays and the sharpness of cochlear tuning while providing useful analysis methods for future studies.

Probing cochlear tuning and tonotopy in the tiger using otoacoustic emissions.

Otoacoustic emissions (sound emitted from the ear) allow cochlear function to be probed noninvasively. The emissions evoked by pure tones, known as stimulus-frequency emissions (SFOAEs), have been shown to provide reliable estimates of peripheral frequency tuning in a variety of mammalian and non-mammalian species. Here, we apply the same methodology to explore peripheral auditory function in the largest member of the cat family, the tiger (Panthera tigris). We measured SFOAEs in 9 unique ears of 5 anesthetized tigers. The tigers, housed at the Henry Doorly Zoo (Omaha, NE), were of both sexes and ranged in age from 3 to 10 years. SFOAE phase-gradient delays are significantly longer in tigers--by approximately a factor of two above 2 kHz and even more at lower frequencies--than in domestic cats (Felis catus), a species commonly used in auditory studies. Based on correlations between tuning and delay established in other species, our results imply that cochlear tuning in the tiger is significantly sharper than in domestic cat and appears comparable to that of humans. Furthermore, the SFOAE data indicate that tigers have a larger tonotopic mapping constant (mm/octave) than domestic cats. A larger mapping constant in tiger is consistent both with auditory brainstem response thresholds (that suggest a lower upper frequency limit of hearing for the tiger than domestic cat) and with measurements of basilar-membrane length (about 1.5 times longer in the tiger than domestic cat).

Interrelationships between spontaneous and low-level stimulus-frequency otoacoustic emissions in humans.

It has been proposed that OAEs be classified not on the basis of the stimuli used to evoke them, but on the mechanisms that produce them (Shera and Guinan, 1999). One branch of this taxonomy focuses on a coherent reflection model and explicitly describes interrelationships between spontaneous emissions (SOAEs) and stimulus-frequency emissions (SFOAEs). The present study empirically examines SOAEs and SFOAEs from individual ears within the context of model predictions, using a low stimulus level (20 dB SPL) to evoke SFOAEs. Emissions were recorded from ears of normal-hearing young adults, both with and without prominent SOAE activity. When spontaneous activity was observed, SFOAEs demonstrated a localized increase about the SOAE peaks. The converse was not necessarily true though, i.e., robust SFOAEs could be measured where no SOAE peaks were observed. There was no significant difference in SFOAE phase-gradient delays between those with and without observable SOAE activity. However, delays were larger for a 20 dB SPL stimulus level than those previously reported for 40 dB SPL. The total amount of SFOAE phase accumulation occurring between adjacent SOAE peaks tended to cluster about an integral number of cycles. Overall, the present data appear congruous with predictions stemming from the coherent reflection model and support the notion that such comparisons ideally are made with emissions evoked using relatively lower stimulus levels.

Frequency selectivity in Old-World monkeys corroborates sharp cochlear tuning in humans.

Frequency selectivity in the inner ear is fundamental to hearing and is traditionally thought to be similar across mammals. Although direct measurements are not possible in humans, estimates of frequency tuning based on noninvasive recordings of sound evoked from the cochlea (otoacoustic emissions) have suggested substantially sharper tuning in humans but remain controversial. We report measurements of frequency tuning in macaque monkeys, Old-World primates phylogenetically closer to humans than the laboratory animals often taken as models of human hearing (e.g., cats, guinea pigs, chinchillas). We find that measurements of tuning obtained directly from individual auditory-nerve fibers and indirectly using otoacoustic emissions both indicate that at characteristic frequencies above about 500 Hz, peripheral frequency selectivity in macaques is significantly sharper than in these common laboratory animals, matching that inferred for humans above 4-5 kHz. Compared with the macaque, the human otoacoustic estimates thus appear neither prohibitively sharp nor exceptional. Our results validate the use of otoacoustic emissions for noninvasive measurement of cochlear tuning and corroborate the finding of sharp tuning in humans. The results have important implications for understanding the mechanical and neural coding of sound in the human cochlea, and thus for developing strategies to compensate for the degradation of tuning in the hearing-impaired.

Comparison of otoacoustic emissions within gecko subfamilies: morphological implications for auditory function in lizards.

Otoacoustic emissions (OAEs) are sounds emitted by the ear and provide a non-invasive probe into mechanisms underlying peripheral auditory transduction. This study focuses upon a comparison of emission properties in two phylogenetically similar pairs of gecko: Gekko gecko and Hemidactylus turcicus and Eublepharis macularius and Coleonyx variegatus. Each pair consists of two closely related species within the same subfamily, with quantitatively known morphological properties at the level of the auditory sensory organ (basilar papilla) in the inner ear. Essentially, the comparison boils down to an issue of size: how does overall body size, as well as the inner-ear dimensions (e.g., papilla length and number of hair cells), affect peripheral auditory function as inferred from OAEs? Estimates of frequency selectivity derived from stimulus-frequency emissions (emissions evoked by a single low-level tone) indicate that tuning is broader in the species with fewer hair cells/shorter papilla. Furthermore, emissions extend outwards to higher frequencies (for similar body temperatures) in the species with the smaller body size/narrower interaural spacing. This observation suggests the smaller species have relatively improved high-frequency sensitivity, possibly related to vocalizations and/or aiding azimuthal sound localization. For one species (Eublepharis), emissions were also examined in both juveniles and adults. Qualitatively similar emission properties in both suggests that inner-ear function is adult like soon after hatching and that external body size (e.g., middle-ear dimensions and interaural spacing) has a relatively small impact upon emission properties within a species.

Otoacoustic Estimates of Cochlear Tuning: Testing Predictions in Macaque.

Otoacoustic estimates of cochlear frequency selectivity suggest substantially sharper tuning in humans. However, the logic and methodology underlying these estimates remain untested by direct measurements in primates. We report measurements of frequency tuning in macaque monkeys, Old-World primates phylogenetically closer to humans than the small laboratory animals often taken as models of human hearing (e.g., cats, guinea pigs, and chinchillas). We find that measurements of tuning obtained directly from individual nerve fibers and indirectly using otoacoustic emissions both indicate that peripheral frequency selectivity in macaques is significantly sharper than in small laboratory animals, matching that inferred for humans at high frequencies. Our results validate the use of otoacoustic emissions for noninvasive measurement of cochlear tuning and corroborate the finding of sharper tuning in humans.

Tectorial membrane morphological variation: effects upon stimulus frequency otoacoustic emissions.

The tectorial membrane (TM) is widely believed to play an important role in determining the ear's ability to detect and resolve incoming acoustic information. While it is still unclear precisely what that role is, the TM has been hypothesized to help overcome viscous forces and thereby sharpen mechanical tuning of the sensory cells. Lizards present a unique opportunity to further study the role of the TM given the diverse inner-ear morphological differences across species. Furthermore, stimulus-frequency otoacoustic emissions (SFOAEs), sounds emitted by the ear in response to a tone, noninvasively probe the frequency selectivity of the ear. We report estimates of auditory tuning derived from SFOAEs for 12 different species of lizards with widely varying TM morphology. Despite gross anatomical differences across the species examined herein, low-level SFOAEs were readily measurable in all ears tested, even in non-TM species whose basilar papilla contained as few as 50-60 hair cells. Our measurements generally support theoretical predictions: longer delays/sharper tuning features are found in species with a TM relative to those without. However, SFOAEs from at least one non-TM species (Anolis) with long delays suggest there are likely additional micromechanical factors at play that can directly affect tuning. Additionally, in the one species examined with a continuous TM (Aspidoscelis) where cell-to-cell coupling is presumably relatively stronger, delays were intermediate. This observation appears consistent with recent reports that suggest the TM may play a more complex macromechanical role in the mammalian cochlea via longitudinal energy distribution (and thereby affect tuning). Although significant differences exist between reptilian and mammalian auditory biophysics, understanding lizard OAE generation mechanisms yields significant insight into fundamental principles at work in all vertebrate ears.

Coherent reflection without traveling waves: on the origin of long-latency otoacoustic emissions in lizards.

Lizard ears produce otoacoustic emissions with characteristics often strikingly reminiscent of those measured in mammals. The similarity of their emissions is surprising, given that lizards and mammals manifest major differences in aspects of inner ear morphology and function believed to be relevant to emission generation. For example, lizards such as the gecko evidently lack traveling waves along their basilar membrane. Despite the absence of traveling waves, the phase-gradient delays of gecko stimulus-frequency otoacoustic emissions (SFOAEs) are comparable to those measured in many mammals. This paper describes a model of emission generation inspired by the gecko inner ear. The model consists of an array of coupled harmonic oscillators whose effective damping manifests a small degree of irregularity. Model delays increase with the assumed sharpness of tuning, reflecting the build-up time associated with mechanical resonance. When tuning bandwidths are chosen to match those of gecko auditory-nerve fibers, the model reproduces the major features of gecko SFOAEs, including their spectral structure and the magnitude and frequency dependence of their phase-gradient delays. The same model with appropriately modified parameters reproduces the features of SFOAEs in alligator lizards. Analysis of the model demonstrates that the basic mechanisms operating in the model are similar to those of the coherent-reflection model developed to describe mammalian emissions. These results support the notion that SFOAE delays provide a noninvasive measure of the sharpness of cochlear tuning.

Towards improving the integration of undergraduate biology and mathematics education.

Arguments have recently asserted the need for change in undergraduate biology education, particularly with regard to the role of mathematics. The crux of these protests is that rapidly developing technology is expanding the types of measurements and subsequent data available to biologists. Thus future generations of biologists will require a set of quantitative and analytic skills that will allow them to handle these types of data in order to tackle relevant questions of interest. In this spirit, we describe here strategies (or lessons learned) for undergraduate educators with regard to better preparing undergraduate biology majors for the new types of challenges that lay ahead. The topics covered here span a broad range, from classroom approaches to the administrative level (e.g., fostering inter-departmental communication, student advising) and beyond. A key theme here is the need for an attitude shift with regard to mathematics education by both students and faculty alike. Such a shift will facilitate the development and implementation of new teaching strategies with regard to improving integration of mathematics and biology pedagogy.

The auditory midbrain of people with tinnitus: abnormal sound-evoked activity revisited.

Sound-evoked fMRI activation of the inferior colliculi (IC) was compared between tinnitus and non-tinnitus subjects matched in threshold (normal), age, depression, and anxiety. Subjects were stimulated with broadband sound in an "on/off" fMRI paradigm with and without on-going sound from the scanner coolant pump. (1) With pump sounds off, the tinnitus group showed greater stimulus-evoked activation of the IC than the non-tinnitus group, suggesting abnormal gain within the auditory pathway of tinnitus subjects. (2) Having pump sounds on reduced activation in the tinnitus, but not the non-tinnitus group. This result suggests response saturation in tinnitus subjects, possibly occurring because abnormal gain increased response amplitude to an upper limit. (3) In contrast to Melcher et al. (2000), the ratio of activation between right and left IC did not differ significantly between tinnitus and non-tinnitus subjects or in a manner dependent on tinnitus laterality. However, new data from subjects imaged previously by Melcher et al. suggest a possible tinnitus subgroup with abnormally asymmetric function of the IC. The present and previous data together suggest elevated responses to sound in the IC are common among those with tinnitus and normal thresholds, while abnormally asymmetric activation is not, even among those with lateralized tinnitus.

Otoacoustic emissions in humans, birds, lizards, and frogs: evidence for multiple generation mechanisms.

Many non-mammalian ears lack physiological features considered integral to the generation of otoacoustic emissions in mammals, including basilar-membrane traveling waves and hair-cell somatic motility. To help elucidate the mechanisms of emission generation, this study systematically measured and compared evoked emissions in all four classes of tetrapod vertebrates using identical stimulus paradigms. Overall emission levels are largest in the lizard and frog species studied and smallest in the chicken. Emission levels in humans, the only examined species with somatic hair cell motility, were intermediate. Both geckos and frogs exhibit substantially higher levels of high-order intermodulation distortion. Stimulus frequency emission phase-gradient delays are longest in humans but are at least 1 ms in all species. Comparisons between stimulus-frequency emission and distortion-product emission phase gradients for low stimulus levels indicate that representatives from all classes except frog show evidence for two distinct generation mechanisms analogous to the reflection- and distortion-source (i.e., place- and wave-fixed) mechanisms evident in mammals. Despite morphological differences, the results suggest the role of a scaling-symmetric traveling wave in chicken emission generation, similar to that in mammals, and perhaps some analog in the gecko.