The 25th anniversary of the discovery of otoacoustic emissions (OAEs), the acoustic energy produced by the cochlea, was celebrated in 2003. Following Kemp's (1978, 1979a, 1979b) breakthrough descriptions of the four types of OAEs in humans—the click-or transient-evoked OAE (TEOAE), the distortion product OAE (DPOAE), the stimulus frequency OAE (SFOAE), and the spontaneous OAE (SOAE)—interest turned to basic research issues. Existing models of cochlear function were modified to reflect the existence of active processing as implied by the mere reality of OAEs. Also, efforts were made to relate OAEs to parallel neural and psychoacoustical phenomena, and to describe emitted responses in species used as research models, including monkeys, gerbils, guinea pigs, and chinchillas (Zurek, 1985).

During the early years of OAE study, another great advance in the hearing sciences occurred when Brownell et al. (1985) discovered electromotility in isolated outer hair cells. The current consensus is that outer hair cell motility is due to the receptor-potential initiated movements of atomic-sized “motor” molecules called prestin (Zheng et al., 2002) that are embedded in the lateral membrane of the outer hair cell. Our present understanding is that OAEs are generated as a by-product of these electromotile vibrations of outer hair cells (Brownell, 1990).

As the initial basic studies on OAEs were ongoing, the significant benefits of OAEs as a clinical test were being recognized. Thus, early on, four major applications of OAE testing in clinical settings became apparent: the differential diagnosis of hearing loss, hearing screening in difficult to test patients, serial monitoring of progressive hearing impairment conditions, and determining the legitimacy of medicolegal claims involving compensatory payments for hearing loss. The rationale for using OAEs in each of these major applications is based on a significant beneficial feature of the measure, including its specificity for testing the functional status of outer hair cells, 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 noninvasively measured from the outer ear canal and thus can be rapidly obtained, it is an ideal screening test for identifying hearing impairment in newborns. Finally, because OAEs are stable and reliably measured over long time intervals, they are excellent for monitoring pathological changes in cochlear function, particularly in individuals regularly exposed to ototoxic drugs or excessive sounds.

One relatively new application of OAEs over the past decade has been the use of emissions to measure the intactness of the entire ascending and descending auditory pathway (Collet et al., 1990). This capability is based on the knowledge that the suppressive effects of cochlear efferents mainly affect outer hair cell activity, since these sensory cells are the primary targets of the descending auditory system. Indeed, recent research indicates that the susceptibility of the ear to the harmful effects of, for example, intense noise is likely determined by the amount of indigenous efferent activity (Luebke, Foster, and Stagner, 2002). 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 OAEs, for several reasons. Their prevalence in only about 50% of normal-hearing individuals and the individually based uniqueness of their frequencies and levels make it difficult to develop SOAEs into a standardized test. However, SOAEs have been linked to tinnitus in a subset of tinnitus patients with near-normal hearing (Penner, 1992). 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 persons with SOAE-induced tinnitus (Penner and Coles, 1992).

Concerning the three subclasses of evoked OAEs, only TEOAEs and DPOAEs have proved to be clinically useful. SFOAEs can be reliably measured only 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.

Within a decade after the discovery of TEOAEs, commercial equipment based on procedures used for evoking auditory brainstem responses was available (Bray and Kemp, 1987). Figure 1 shows the results of pure-tone audiometry (A) and tests of click-evoked TEOAEs (B) and DPOAEs (C) in a 37-year-old patient receiving the ototoxic antitumor drug cisplatin. In this case, following a single infusion (Fig. 1A), a moderate high-frequency hearing loss was evident bilaterally for frequencies over 4 kHz. The associated TEOAE spectrum (Fig. 1B) illustrates the commonly measured properties for this emitted response, including its level, frequency content and extent, and reliability, according to automatically computed reproducibility factors for five representative frequencies at 1, 2, 3, 4, and 5 kHz.

Figure 1..  

Audiometric and evoked OAE findings in a 37-year-old man who had received intravenous infusions of cisplatin for testicular carcinoma. A, Pure-tone clinical audiogram for left (solid circles) and right (open circles) ear showing normal to near-normal hearing thresholds from 250 Hz to 4 kHz, after which hearing levels fell to 35–65 dB HL at 6 and 8 kHz. B, A TEOAE spectrum for the left ear showing relatively normal click-evoked emissions up to about 3.5 kHz. Note the progressive decrement in TEOAE levels above 1.5 kHz, which is a pattern typically observed for normal-hearing adults. The “repro by frequency” values indicate excellent test-retest results over the short recording session for frequencies up to 3 kHz. C, DP-gram showing DPOAE levels for left (solid circles) and right (open circles) ears in response to moderate, equilevel primary tones, i.e., L₁ = L₂ = 65 dB SPL, from 800 Hz to 8 kHz, at 10 points per octave. The bold dashed curves at the top of the plot represent the ±1 SD of DPOAE values in response to identical primaries for 100 ears from normal-hearing subjects; the bold dotted curves at the bottom of the plot indicate the counterpart distribution of noise-floor values for the same subjects. Note that the patient was exceptionally quiet, as his noise-floor curves (bold line = left ear; stippled line = right ear) tracked the lower distribution trajectory of the control population. In this example, the ototoxic drug caused outer hair cell dysfunction for frequencies above about 2.5 kHz for the left ear and 4 kHz for the right ear.

Because the TEOAE is measured after the transient stimulus occurs, each ear produces 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. Owing to 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 (Norton et al., 2000).

In the example of Figure 1B, representing the left ear of the patient, even in the presence of a drug-induced high-frequency hearing loss, the TEOAE pattern appears fairly normal in that the click-elicited emission typically falls off for frequencies greater than 2 kHz, and is seldom present at frequencies above 4 kHz in adult ears. 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. The frequencies and levels of the tonebursts 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 primary-tone levels of L₁ = 65 and L₂ = 55 dB SPL (Gorga, Neely, and Dorn, 1999).

Figure 1C shows a DP-gram, i.e., DPOAE level as a function of test frequency, from about 800 Hz to 8 kHz, in response to equilevel primary tones (L₁ = L₂ = 65 dB SPL). In this example, test frequency is represented by the geometric or logarithmic mean of f₁ and f₂, although it could also be represented by the f₂ frequency. That is, based on a combination of theoretical considerations, experimental studies, and observations of the generation of DPOAEs in pathological ears, it is clear that these emissions are produced in the region of the primary tones. Based on further experimental work, it is likely 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. In contrast, for lower level primaries, which are often offset in level, the primary generation site is closer to f₂.

As illustrated in Figure 1C, the patient's emissions were relatively normal, as compared to the ±1 SD distribution of DPOAE levels for normal-hearing adults, until about 3 kHz for the left ear (solid circles) and 4 kHz for the right ear (open circles). In this case, because DPOAEs are typically tested out to 8 kHz, they detected the developing high-frequency hearing loss associated with the ototoxic antitumor therapy.

It is clear that applications of OAEs in the hearing sciences and clinical audiology are varied. Without a doubt, OAEs are useful experimentally for evaluating and monitoring the status of cochlear function in animal models, and clinically in distinguishing cochlear from retrocochlear disorders. Moreover, their practical features make them helpful in the hearing screening of newborns. Additionally, they have proved 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 on outer hair cell function using OAEs before a related hearing loss can be detected by pure-tone audiometry. In addition, OAEs provide a noninvasive 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, and this capability makes them ideal response measures in both the clinical and basic hearing sciences.