Backward Propagation of Otoacoustic Emissions

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Backward Propagation of Otoacoustic Emissions HE Wenxuan,1, 2 REN Tianying,1, 2 1. Oregon Hearing Research Center, Department of Otolaryngology and Head & Neck Surgery, Oregon Health & Science University, 3181 SW Sam Jackson Park Road, NRC04, Portland, Oregon 97239 USA; 2. School of Medicine, Xi’ an Jiaotong University, Xi’ an, Shaanxi 710061 China Abstract Normal mammalian ears not only detect but also generate sounds. The ear-generated sounds, i.e., otoacoustic emissions (OAEs), can be measured in the external ear canal using a tiny sensitive microphone. In spite of wide applications of OAEs in diagnosis of hearing disorders and in studies of cochlear functions, the question of how the cochlea emits sounds remains unclear. The current dominating theory is that the OAE reaches the cochlear base through a backward traveling wave. However, recently published works, including experimental data on the spatial pattern of basilar membrane vibrations at the emission frequency, demonstrated only forward traveling waves and no signs of backward traveling waves. These new findings indicate that the cochlea emits sounds through cochlear fluids as compression waves rather than through the basilar membrane as backward traveling waves. This article reviews different mechanisms of the backward propagation of OAEs and summarizes recent experimental results. Key words otoacoustic emissions; cochlea; basilar membrane vibration; cochlear traveling wave

Introductions Sounds impinging the eardrum are transmitted via middle ear ossicles to the oval window. Stapes vibration creates pressure difference between the scala tympani and the scala vestibuli. This pressure difference causes a movement of cochlear partition and adjacent cochlear fluids. Basilar membrane vibrations result in deflection of hair cell stereocilia, which gate ion channels on their tips. This mechanical-to-electrical transduction process converts mechanical vibrations into electrical impulses, which encode acoustical information and are transmitted to the brain by the auditory nerve. In order to understand how the ear processes sounds, Gold proposed that there was a reverse (i.e., electrical-to-mechanical) transduction process in the cochlea(Gold, 1948). He predicted the existence of ear-generated sounds but failed to detect them due to the poor sensitivity of his microphones. Little attention was given to Gold’s hypothesis until Kemp successfulCorresponding author: Dr. Ren Tianying, Oregon Hearing Research Center, Department of Otolaryngology and Head & Neck Surgery, Oregon Health & Science University, 3181 SW Sam Jackson Park Road, NRC04, Portland, Oregon, 97239, USA. E-mail: [email protected]

ly recorded otoacoustic emissions (OAEs) in the human ear canal (Kemp, 1978). There are two types of OAEs: spontaneous OAEs (SOAEs) and evoked OAEs. SOAEs can be detected in the external ear canal without external stimuli, and the evoked OAEs are the OAEs elicited by external stimuli. Evoked emissions can be subclassified into (1) transiently evoked otoacoustic emissions (TEOAEs), elicited by transient acoustic stimuli, such as clicks or tonepips; (2) stimulus-frequency otoacoustic emissions (SFOAEs), elicited by a single continuous pure tone; (3) electrically evoked otoacoustic emissions (EEOAEs), evoked by electrical stimulation of the cochlear partition; and(4) distortion-product otoacoustic emissions (DPOAEs), evoked by two continuous pure tones at different frequencies. When a pair of pure tones at frequencies of f1 and f2 (f1＜f2) are simultaneously presented into the external ear canal, distortion products at frequencies of mf1 + nf2(where m and n are integers) are generated in the inner ear by the cochlear nonlinearity. Among different DPOAEs, the most prominent one is the cubic difference tone (CDT) at the frequency 2f1-f2, and it has been commonly used in clinics for testing hearing (Probst et al, 1991). Applications of OAEs include universal newborn hearing screening,

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monitoring the effects of treatment, selecting of hearing aids, and studying cochlear mechanical mechanisms (Kemp 1988, Robles and Ruggero, 2001). Kemp concluded that OAEs are caused by cochlear nonlinear processes(Kemp, 1978). Cochlear nonlinearity exists only in normal ears, and results from the cochlear amplifier(Robles et al, 2001). The cochlear amplifier is believed to be a local feedback mechanism, which uses metabolic energies to amplify basilar membrane vibrations (Dallos, 1992). Outer hair cells can convert the mechanical energy into electrical currents (Gillespie et al, 2001), which result in power production via somatic motility (Brownell et al, 1985; Zenner et al, 1987) and/or active hair bundle motion (Martin et al, 1999; Martin et al, 2000). Thus, OAEs have been believed to be generated by the cochlear amplifier and outer hair cells. In the literature, OAEs have been used to estimate the cochlear amplifier gain or the integrity of outer hair cells (Mills, 1998). Because OAEs result from cochlear nonlinearity, their generation locations should overlap with locations of the latter. Regarding how OAEs are transmitted to the cochlear base from their generation places, there are two different theories: the reverse traveling-wave theory(Kemp, 1986) and compression-wave mechanism theory(Wilson, 1980). Backward traveling wave According to the backward-traveling-wave theory, the OAE propagates from the generation site to the cochlear base as a transverse vibration along the cochlear partition at the same speed as a forward traveling wave. This theory was originally proposed by Kemp in 1986, based on the observation that cochlear-generated sound can be measured in the ear canal (Kemp, 1978) and a mathematical demonstration of the theoretical feasibility of backward propagation (de Boer et al, 1986). Kemp noted that the idea of backward traveling wave contradicts the well-known observations of Békésy that basilar membrane vibration travels only in a forward direction from base to apex (von Békésy, 1960). He thought, however, that Békésy‘s observation was true only for external sound-induced cochlear vibration, not for internal sound sources, such as otoacoustic emissions. The backward traveling wave theory has been comprehensively studied mathematically and experimentally and has become widely accepted in the literature (Knight et al, 2001; Lukashkin et al, 2002; Schneider et al, 1999; Schoonhoven et al, 2001; Shera et al, 1999; Tubis et al, 2000; Withnell et al,

·41· 2005). Besides numerous modeling studies, main experimental evidence supporting the backward-traveling-wave theory is that the roundtrip delay of an emission measured as phase-frequency slope (i.e., group delay) in the human or animal ear canal is approximately twice the forward delay (Kimberley et al, 1993; Mahoney et al, 1995; Schneider et al, 1999). Group delay is defined as a phase change as a function of frequency. It is described by the following equation: D = Δɸ/Δω, where D is the group delay in seconds, Δɸ is the phase difference in radians, Δω is the angular frequency change. For a linear system, the group delay can be used to indicate the time delay. However, cochlear nonlinearity, filtering, and dispersion complicate the interpretation of group-delay measurements. It is a common belief that the group delay of OAEs includes the propagation delay and the cochlear“filter”delay (Avan et al, 1998; Ruggero,2004). Because sharpness of the cochlear filter varies with cochlear longitudinal location, stimulus intensity, and cochlear condition, there is no simple means to estimate cochlear-filter delay based on the phase data. Due to the unknown cochlear-filter delay, it is difficult to derive the propagation delay of OAEs from group delay measured in the external ear canal. In spite of the difficulties in data interpretation, group delay has been commonly used to estimate the delay of OAEs because of the lack of other methods. Kimberley et al(1993) estimated the traveling wave delay through measurement of group delays of DPOAEs. These authors assumed that the generation site of DPOAE was at the f2 place on the basilar membrane, and the emission delay was two times of the forward delay. Group delays of DPOAEs were measured at eight different f2 frequencies from 10 to 0.78 kHz in 36 human ears. It was found that the phase of emissions decreased as a function of the frequency. Estimates of the traveling wave delay from the ear canal to the f2 place varied from about 1 ms for 10 kHz place to 3.5 ms for the 0.78 kHz place. This finding apparently agrees with the previous estimates using electrocochleography. Cooper and Shera measured basilar membrane vibration, stimulus-frequency(SFOAEs), and DPOAEs from anaesthetized guinea pigs (Cooper et al, 2004). These authors found that phase characteristics of SFOAEs and DPOAEs showed group delays well in excess of those measured for forward traveling waves on the basilar membrane. By modeling analysis of the basilar membrane vibration at the emission frequency, Cooper and Shera showed that forward-traveling waves dominated the basilar membrane response in the

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near best-frequency(BF) region. Backward-traveling waves were only evident well below the BF. This result is consistent with modelling prediction that OAEs couple to the middle ear via traveling pressure-difference wave in the cochlea(Talmadge et al, 1998; Zweig et al, 1995). The above data have been interpreted to be consistent with the hypothesis that OAEs propagate away from hair cells via backward-traveling waves, and inconsistent with the hypothesis that OAEs reach the stapes directly via fluid-borne compression wave. In addition to phase-based group delay measurements, OAE delays have also been measured in time domain in several studies(Konrad-Martin et al, 2003; Shaffer et al, 2003; Withnell et al, 2005). These studies have provided additional supporting data for the backward-traveling wave theory. However, OAE delays measured in time domain are also subject to effects of the cochlear filter and dispersion, and cannot be considered as propagation delay or the signal front delay (Ruggero, 2004) in the cochlea. Backward compression wave The compression-wave theory posits that OAEs propagate to the cochlear base via longitudinal waves in the cochlear fluids at the speed of sound in water. The concept of the cochlear compression wave was first implied in a sensory outer-hair-cell swelling model by Wilson(Wilson, 1980), in which hair cell volume changes displaced the stapes footplate and resulted in the emission. Although the hair cell-swelling mechanism is no longer considered likely, due to the required speed of volume changes, this theory implies that a pressure wave in cochlear fluids directly produces an otoacoustic emission. Compression-wave theories have subsequently been advanced by a number of studies (Avan et al, 1998; Ren, 2004; Robles et al. , 1997; Ruggero, 2004; Siegel et al, 2005). Avan et al.(1998) measured OAE pressures in the scalae vestibuli and tympani at the first and second turn of the guinea-pig cochlea. Frequencies of 2f1-f2 were varied from 0.75 to 9 kHz and pressures were measured with a miniature piezoresistive transducer. It was observed that pressures of DPOAEs in the scala vestibuli at the first turn were similar to those at the second turn. Phase data showed that forward and backward travel times from one turn to the other were shorter than 0.2 ms, which was shorter than the emission group delay measured in the ear canal by about five folds. The authors believed that local filtering process-

es rather than propagation delays accounted for the overall emission delay. Robles et al. demonstrated two-tone distortion in basilar-membrane motion using laser-velocimetry technique (Robles et al, 1991). Magnitude and phase characteristics of the basilar membrane vibration at the DP frequency were systematically observed by Robles et al (1997) and Copper and Rhode(1997). Since the forward group delay of sound propagating from the stapes to its BF location can be measured experimentally by the phase transfer function of basilar membrane vibration(Cooper et al, 1992; Khanna et al, 1982; Nuttall et al, 1996; Rhode, 1971; Robles et al, 2001), measuring the OAE group delay and comparing it to the group delay of basilar membrane vibrations has become an important way to distinguish backward traveling waves from fluid compression waves. Narayan et al (1998) measured DPOAEs in the ear canal and basilar membrane vibrations at the f2 place simultaneously in chinchillas and found that the basilar membrane vibration and OAE phases had similar group delays(0.5-0.8 ms), which were similar to the forward delay. Their data indicate that DPOAE group delays largely reflect the cochlear‘filter’ . The findings in their study has been confirmed by a recent study(Gong et al, 2005). Gong et al(2005). found that the group delay of 2f1-f2 DPOAEs was nearly identical to the BM forward delay. Recently, Siegel et al. measured SFOAEs in chinchillas, and compared their group delays to the forward delay of basilar membrane vibrations(Siegel et al, 2005). They found that SFOAE group delays were similar to or shorter than the forward delays. This result contradicts with the“theory of coherent reflection filtering”(Shera et al, 1999; Zweig et al, 1995), and supports the cochlear compression wave mechanism. Ren(2004) measured the longitudinal pattern of basilar membrane vibrations at the emission frequency site using a scanning laser interferometer. The magnitude and phase of basilar membrane vibration were recorded as a function of the longitudinal location. The data showed the maximum vibration at the emission BF site rather than at the f1 and f2 overlapped place. Phase-longitudinal data showed that the phase decreased with the distance from the cochlear base, indicating typical forward traveling waves. The data also showed that the stapes vibration occurred earlier than the basilar membrane vibration. In a separate experiment, Ren et al. (2005) measured DPOAEs at several longitudinal locations on the basilar membrane in gerbils. These authors found that the slope of phase-frequency curve measured from an apical location was al-

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ways steeper than that measured from basal locations. These results from acoustically evoked responses are consistent with those from electrically induced cochlear responses. Ren et al(2004) showed that electrically evoked basilar membrane vibration group delay was significantly shorter than that of a cochlear traveling wave. All experiments by Ren et al. consistently show that the backward transmission of the emission is much faster than that of forward traveling waves. Dong and Olson studied the DPOAE generation mechanism by measuring sound pressure in the cochlear fluids (Dong et al, 2005). They found that the pressure responses near the basilar membrane were consistent with previous observations of two-tone distortion in basilar membrane motion(Cooper et al, 1997; Robles et al, 1997). Distortion product tuning and group delay are similar, but not identical, to single tone response. However, the decay of distortion products with distance from the basilar membrane confirms the feasibility that they could drive the stapes by a direct fluid route as a fluid compression wave (Ren, 2004). In a comprehensive review, Ruggero (2004) compared the group delay of 2f1-f2 distortion product OAEs to the basilar membrane forward delay, and found there were not sufficient data to distinguish the backward traveling theory from the compression wave hypothesis conclusively at that time. Since Ruggero’s review, new experimental data (Gong et al, 2005; Ren et al, 2005; Siegel et al, 2005) supporting the cochlear compression wave mechanism have become available. As Ruggero pointed out, more complete sets of correlated basilar membrane and DPOAE data for the same species are required for reliable comparisons of DPOAE and BM group delays. In addition, other experimental methods, such as measuring backward delay of laser pulse-induced basilar membrane vibration (Fridberger et al, 2006), will likely provide more direct information on the backward propagation of OAEs. In summary, although otoacoustic emissions have been commonly used as a noninvasive method for evaluating hearing and for studying cochlear mechanics, their generation mechanisms remain unclear. It has been widely believed that the cochlea emits sound via backward traveling waves along the cochlear partition. This hypothesis is supported by numerous modeling and experimental studies. However, increasing new data indicate that the emission reaches the stapes at a speed much faster than the traveling waves. These new findings suggest that cochleae emit sounds via the cochlear fluids as compression waves.

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