Christopher Bergevin

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.

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.

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.

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.

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 ears 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.

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.

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.

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

Significance Healthy ears not only detect sound but can emit it as well. These sounds can occur either spontaneously and continuously or in response to acoustic stimulation. Evoked emissions are increasingly used as clinical diagnostic tools. The mechanisms underlying their generation, however, are incompletely understood. In particular, otoacoustic emissions occur in a wide variety of species, from frogs to humans, suggesting basic, shared principles. Here, we analyzed both spontaneous and evoked otoacoustic emissions from a bird and a lizard. We relate these data to those from humans and suggest that otoacoustic emissions originate from similar biomechanical principles despite gross differences in the underlying anatomy of the ear. 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.

Coupled, Active Oscillators and Lizard Otoacoustic Emissions

The present study empirically explores the relationship between spontaneous otoacoustic emissions (SOAEs) and stimulus‐frequency emissions (SFOAEs) in lizards, an ideal group for such research given their relatively simple inner ear (e.g., lack of basilar membrane traveling waves), diverse morphology across species/families (e.g., tectorial membrane structure) and robust emissions. In a nutshell, our results indicate that SFOAEs evoked using low‐level tones are intimately related to underlying SOAE activity, and appear to represent the entrained response of active oscillators closely tuned to the probe frequency. The data described here indicate several essential features that are desirable to capture in theoretical models for auditory transduction in lizards, and potentially represent generic properties at work in many different classes of “active” ears.

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.