The 25th anniversary of the discovery of otoacoustic emissions (OAEs)-sounds that can be measured in the external ear canal following the presentation of an acoustic stimulus-was celebrated in 2003. The key interests following the original descriptions of the four types of OAEs-the click- or transient-evoked OAE (TEOAE), the distortion product OAE (DPOAE), the stimulus frequency OAE (SFOAE), and the spontaneous OAE (SOAE)-primarily concerned basic research issues.
At that time, existing models of cochlear function were modified significantly to acknowledge the reality of active processing as supported by the mere existence of OAEs. Also, some efforts were made to relate OAEs to parallel neural and psychoacoustical phenomena. Finally, emitted responses were described in a number of experimental species commonly used as research models of hearing impairment including monkeys, gerbils, guinea pigs, and chinchillas, and, most recently, mice.
Exactly how OAEs arise and how they are propagated in the cochlea is still being debated. Recent experimental and theoretical findings suggest that there may be two mechanisms of OAE generation. Thus, SOAEs, TEOAEs, and SFOAEs may arise from linear reflections from impedance discontinuities (e.g., out of place hair-cell receptors) distributed along the cochlear partition, whereas DPOAEs likely result from nonlinear distortion. The bulk of evidence now suggests that outer hair cells (OHCs) are capable of motile activity, and the current consensus is that OHC motility is due to the receptor-potential initiated micromovements of "motor" molecules called "prestin" embedded in the lateral membrane of the OHC. Our present understanding is that OAEs are in some way generated as a by-product of these electromotile vibrations of the OHCs.
The existence of OAEs provides evidence that the cochlea is an active participant in the processing of acoustic signals, because movements of the OHCs probably act to enhance the sensitivity and frequency tuning of the vibration of the cochlear partition. In current theories of cochlear function, "active" OHCs are considered to act as a "cochlear amplifier" in the form of a biomechanical-feedback system that sharpens the peak of the mechanical traveling wave. With OHC damage, the sensitivity and sharp tuning of basilar membrane vibration are greatly reduced and the passive mechanical analysis and poor tuning of the traveling wave predominate.
OAEs then are either produced or influenced as a byproduct of this amplification process. It is well established that if the OHCs are damaged, the sharp tuning and sensitivity of the cochlea is compromised and OAEs are reduced or absent. In the case of reflection emissions, the peak of the traveling wave may play an important role as a source of reflection and filtering for TEOAEs, SFOAEs, and SOAEs. Hence OHC damage greatly affects this type of OAE.
On the other hand, DPOAEs are probably generated in the nonlinear aspects of the OHC transduction process that likely involves their stereocilia. This explains why, following the administration of certain ototoxins such as furosemide, DPOAEs evoked by high-level primaries persist. In this situation the OHC nonlinearity is not damaged, but sufficient gain and associated basilar-membrane vibration that normally stimulate the nonlinearity located in stereocilia of the OHCs are absent due to the drug-induced reduction of the driving voltage across the OHC. However, for high-level stimuli this lack of gain is overcome and DPOAEs can again be observed. A recent genetics study using mutant mice lacking prestin (i.e., as noted above, the molecular motor responsible for OHC motility) showed that OHC motility is not necessary for the production of high-level DPOAEs.
Testing Benefits and Uses
As the initial basic studies on OAEs proceeded, researchers recognized the significant benefits of emissions as a clinical test. Thus, early on, the three major applications of OAE testing in clinical settings became apparent including the differential diagnosis of hearing loss, hearing screening in difficult-to-test patients such as newborns, and the serial monitoring of progressive hearing-impairment conditions.
The rationale for using OAEs in each of these major applications is based on a significant beneficial feature of emitted responses including their specificity for testing the functional status of OHCs, which represent the most fragile sensory receptors for hearing. This attribute in particular makes OAEs an ideal measure for determining the sensory component of a sensorineural hearing loss. In addition, mainly because the OAE is an objective response that is non-invasively and quickly measured from the outer ear canal, it makes an ideal screening test, especially for identifying hearing impairment in new borns. Finally, because OAEs are stable and reliably measured over lengthy time intervals, they make excellent monitors for detecting pathological changes in cochlear function, which occurs with regular exposure to either ototoxic drugs or excessive sounds.
Since this recognition of the major clinical applications of OAEs, other uses have emerged including resolving the legitimacy of medico-legal claims involving compensatory payments for hearing loss based on the sensitivity of emitted responses to the intactness of the OHC system and its susceptibility to noise-induced damage. Another relatively new application of OAEs over the past decade has been the use of emissions to measure the functional intactness of the descending auditory nervous system. This capability is based on the knowledge that the suppressive effects of cochlear efferents mainly affect OHC activity, since these receptors are the primary targets of the descending neural system. Indeed, recent research in experimental models of noise-induced hearing loss indicates that the susceptibility of the ear to the harmful effects of, for example, intense noise may be determined by the amount of indigenous efferent activity. That is, the more robust the efferent activity, the more resistant the ear is to the damaging effects of loud sounds, and vice versa.
Of the two general classes of OAEs, SOAEs have not been as clinically useful as the evoked OAE s for several reasons. First, as assessed by commonly available commercial equipment, their prevalence at only about 50% of normal-hearing individuals and, second, the individually based uniqueness of their frequencies and levels both make it difficult to develop SOAEs into a standardized test. However, earlier studies showed that some SOAEs are linked to tinnitus in a subset of patients, who have near-normal hearing. Thus, in patients with SOAE-induced tinnitus, suppressing the associated SOAEs eliminates the annoying tinnitus. Interestingly and contrary to expectations, since excessive aspirin produces tinnitus in normal-hearing individuals, high-dose aspirin suffices as a palliative in patients with SOAE-induced tinnitus.
Concerning the three subclasses of evoked OAEs, only the TEOAEs and DPOAEs have proven clinically useful. The SFOAE can be reliably measured only by using expensive phase-tracking devices, since the emission must be extracted from the ear-canal sound at a time that the eliciting stimulus is present at the identical frequency. Fortunately, the SFOAE is essentially the long-lasting version of the TEOAE, which is more straightforward to measure and interpret. However, SFOAEs serve as a useful investigative tool for studying cochlear function.
Within a decade after the discovery of TEOAEs, commercial equipment based on procedures used for evoking auditory brainstem responses became available. Because the TEOAE is measured after the transient stimulus occurs, ears from different individuals produce a response that exhibits a unique spectral pattern. This idiosyncratic property makes it difficult to develop a set of metrics that describe the average TEOAE for normal-hearing individuals. Because of this difficulty in determining "normal" TEOAEs in terms of frequencies and level values, they are most often described as being either present or absent. Thus, one of the most popular uses of TEOAEs clinically is as a test for screening auditory function in newborns.
In normal adult ears, the click-elicited TEOAE typically falls off for frequencies more than 2 kHz, and is seldom present over 4 kHz, because of both technical limitations in the ear-speaker at higher frequencies and the physical features of adult ear canals. For newborns and older infants, the TEOAE is much more robust by about 10 dB and typically can be measured out to about 6 kHz indicating that smaller ear canals influence the acoustic characteristics of standard click stimuli much differently than do adult ears.
Distortion product OAEs are elicited by presenting two long-lasting pure tonebursts at f1 (lower frequency) and f2 (higher frequency) simultaneously to the ear. This emission arises because of the nonlinear aspects of the OHC transduction process in which new frequencies are generated that are not present in the input signal. The frequencies and levels of the tone-bursts or primary tones are important in that the largest DPOAEs are elicited by f1 and f2 primaries that are within one-half octave of each other (i.e., f2/f1=1.22), with levels, L1 and L2, that are offset. For example, typical clinical protocols measure the 2f1-f2 DPOAE, which is the largest DPOAE in human ears, in response to relatively low-level primary tones of L1=65 and L2=55 dB SPL.
DPOAE level as a function of test frequency-that is, the DP-gram-is typically measured from about 800 Hz to 8 kHz, in 6ÿ10 points/octave steps. Test frequency is characteristically represented by the f2 frequency, which is assumed to correspond to the frequency region on the basilar membrane at which the primary tones maximally overlap. This assumption is based on a combination of theoretical considerations, experimental studies, and observations of the generation of DPOAEs in pathological ears. However, further e xperimental work suggests that the DPOAE source is level-dependent, with the primary generation site in response to higher-level primaries of equal level (L1=L2) occurring around the geometric-mean frequency representing the logarithmic average of the f1 and f2 primaries. In contrast, for lower-level primaries that are often offset in level, the primary generation site is closer to f2.
The Present and Future
Relatively recently, a number of experimental outcomes have further demonstrated that the DPOAE-frequency region also contributes to emission magnitude through reflection processes. Indeed, some forms of commercially available equipment, which deliberately suppress the DPOAE-reflection emission using a third f3 or suppressor tone, produce detection "threshold" values that are typically closer to corresponding hearing thresholds than those measured with routine instrumentation.
Currently, research on OAEs is uncovering even more benefits of these tests including the possibility that the SFOAE, which had previously been neglected clinically, may be more predictive of behavioral hearing thresholds than either TEOAEs or DPOAEs. Other benefits of suprathreshold OAEs involve promising future applications. For example, their utility in determining optimal amplification patterns for digital hearing-aid users has yet to be established. In addition, further screening applications may involve their inclusion in hearing-conservation programs and in screening for hearing loss in both school-aged children and the elderly.
It is clear that applications of OAEs in the hearing sciences and clinical audiology are wide-ranging. Without a doubt, OAEs are useful experimentally for evaluating and/or monitoring the status of cochlear function in animal models. Moreover, clinically they contribute toward determining the differential diagnosis of cochlear versus retrocochlear disorders. Further, their practical features make them helpful in the hearing screening of newborns worldwide.
OAEs have also proven useful in monitoring the effects of agents, such as ototoxins and loud sounds, on cochlear function. In fact, there is accumulating evidence that it is possible to detect such adverse effects of drugs or noise or a progressive familial hearing disorder on OHC function using OAEs before a related hearing loss can be detected by pure-tone audiometry. And OAEs are providing a non-invasive means for assessing the integrity of the cochlear-efferent pathway.
In general, OAEs supply unique information about cochlear function in the presence of hearing problems. It is this capability that continues to make them valuable response measures in both the clinical and basic hearing sciences and that promises to contribute further useful tests to the audiometric-test battery.