Distortion-product otoacoustic-emission suppression tuning in human infants and adults using absorbed sound power

The greatest difference in distortion product otoacoustic emission (DPOAE) suppression tuning curves (STCs) in infant and adult ears occurs at a stimulus frequency of 6 kHz. These infant and adult STCs are much more similar when constructed using the absorbed power level of the stimulus and suppressor tones rather than using sound pressure level. This procedure incorporates age-related differences in forward and reverse transmission of sound power through the ear canal and middle ear. These results support the theory that the cochlear mechanics underlying DPOAE suppression are substantially mature in full-term infants.     

Distortion product otoacoustic emission suppression tuning and acoustic admittance in human infants: birth through 6 months

Previous work has reported non-adultlike distortion product otoacoustic emission (DPOAE) suppression in human newborns at f2=6000 Hz, indicating an immaturity in peripheral auditory function. In this study, DPOAE suppression tuning curves (STCs) were recorded as a measure of cochlear function and acoustic admittance/reflectance (YR) in the ear canal recorded as a measure of middle-ear function, in the same 20 infants at birth and through 6 months of age. DPOAE STCs changed little from birth through 6 months, showing excessively narrow and sharp tuning throughout the test period. In contrast, several middle-ear indices at corresponding frequencies shifted systematically with increasing age, although they also remained non-adultlike at 6 months. Linear correlations were conducted between YR and DPOAE suppression features. Only two correlations out of 76 were significant, and all but three YR variables accounted for <10% of the variance in DPOAE suppression tuning. The strongest correlation was noted between admittance phase at 5700 Hz and STC tip-to-tail (R=0.49). The association between middle-ear variables and DPOAE suppression may be stronger during other developmental time periods. Study of older infants and children is needed to fully define postnatal immaturity of human peripheral auditory function.     

Theory of forward and reverse middle-ear transmission applied to otoacoustic emissions in infant and adult ears

The purpose of this study is to understand why otoacoustic emission (OAE) levels are higher in normal-hearing human infants relative to adults. In a previous study, distortion product (DP) OAE input/output (I/O) functions were shown to differ at f2 = 6 kHz in adults compared to infants through 6 months of age. These DPOAE I/0 functions were used to noninvasively assess immaturities in forward/reverse transmission through the ear canal and middle ear [Abdala, C., and Keefe, D. H., (2006). J. Acoust Soc. Am. 120, 3832-3842]. In the present study, ear-canal reflectance and DPOAEs measured in the same ears were analyzed using a scattering-matrix model of forward and reverse transmission in the ear canal, middle ear, and cochlea. Reflectance measurements were sensitive to frequency-dependent effects of ear-canal and middle-ear transmission that differed across OAE type and subject age. Results indicated that DPOAE levels were larger in infants mainly because the reverse middle-ear transmittance level varied with ear-canal area, which differed by more than a factor of 7 between term infants and adults. The forward middle-ear transmittance level was -16 dB less in infants, so that the conductive efficiency was poorer in infants than adults.     

Distortion product otoacoustic emission (2f1-f2) suppression in 3-month-old infants: evidence for postnatal maturation of human cochlear function?

The complete timeline for maturation of human cochlear function has not been defined. Distortion product otoacoustic emission (DPOAE)-based measures of cochlear function show non-adult-like responses from premature and term-born neonates at high f2 frequencies; however, older infants were not included in these studies. In the present experiment, previously collected DPOAE ipsilateral suppression data from premature neonates were combined with new data collected from adults, term-born neonates, and 3-month-old infants to further examine the time course for maturation of cochlear function. DPOAE suppression tuning curves (STC) and suppression growth patterns were measured in the three age groups at f2 = 6000 Hz, L1 = 65, L2 = 55 dB SPL, with an f2/f1 of 1.2. Results indicate that term-born neonates and 3-month-old infants have non-adult-like STC width, slope on the low-frequency flank, and tip features. However, the two infant groups are not significantly different from one another. Suppression growth patterns for low-frequency suppressor tones show a clear developmental progression. In general, the younger the infant, the more shallow and compressive the suppression growth for the lowest suppressor frequencies. These findings suggest a high-frequency postnatal immaturity in cochlear function as measured by DPOAE suppression. Results may have been influenced by noncochlear factors, such as middle-ear immaturity. These factors are reviewed and considered.     

DPOAE suppression tuning: cochlear immaturity in premature neonates or auditory aging in normal-hearing adults?

Previous work has shown that distortion product otoacoustic emission (DPOAE) suppression tuning curves (STCs) recorded from premature neonates are narrower than adult STCs at both low and high frequencies. This has been interpreted to indicate an immaturity in cochlear function prior to term birth. However, an alternative explanation for this finding is that adult DPOAE STCs are broadened and reflect cochlear hair cell loss in normal-hearing adults due to aging, and natural exposure to noise and ototoxins. This alternative hypothesis can be tested by studying suppression tuning in normal-hearing school-aged children. If normal-hearing children, who have not aged significantly or been exposed to noise/ototoxins, have DPOAE suppression tuning similar to adults, the auditory aging hypothesis can be ruled out. However, if children have tuning similar to premature neonates and dissimilar from adults, it implicates aging or other factors intrinsic to the adult cochlea. DPOAE STCs were recorded at 1500, 3000, and 6000 Hz using optimal parameters in normal-hearing children and adults. DPOAE STCs collected previously from premature neonates were used for age comparisons. In general, results indicate that tuning curves from children are comparable to adult STCs and significantly different from neonatal STCS at 1500 and 6000 Hz. Only the growth of suppression was not adultlike in children and only at 6000 Hz. These findings do not strongly support the auditory aging hypothesis as a primary explanation for previously observed neonatal-adult differences in DPOAE suppression tuning. It suggests that these age differences are most likely due to immaturities in the neonatal cochlea. However, nonadultlike suppression growth observed in children at 6000 Hz warrants further attention and may be indicative of subtle alternations in the adult cochlea at high frequencies.     

Distortion product otoacoustic emissions for hearing threshold estimation and differentiation between middle-ear and cochlear disorders in neonates

Our aim in the present study was to apply extrapolated DPOAE I/O-functions [J. Acoust. Soc. Am. 111, 1810-1818 (2002); 113, 3275-3284 (2003)] in neonates in order to investigate their ability to estimate hearing thresholds and to differentiate between middle-ear and cochlear disorders. DPOAEs were measured in neonates after birth (mean age = 3.2 days) and 4 weeks later (follow-up) at 11 test frequencies between f2 = 1.5 and 8 kHz and compared to that found in normal hearing subjects and cochlear hearing loss patients. On average, in a single ear hearing threshold estimation was possible at about 2/3 of the test frequencies. A sufficient test performance of the approach is therefore suggested. Thresholds were higher at the first measurement compared to that found at the follow-up measurement. Since thresholds varied with frequency, transitory middle ear dysfunction due to amniotic fluid instead of cochlear immaturity is suggested to be the cause for the change in thresholds. DPOAE behavior in the neonate ears differed from that found in the cochlear hearing loss ears. From a simple model it was concluded that the difference between the estimated DPOAE threshold and the DPOAE detection threshold is able to differentiate between sound conductive and cochlear hearing loss.     

The breaking of cochlear scaling symmetry in human newborns and adults

Scaling symmetry appears to be a fundamental property of the cochlea as evidenced by invariant distortion product otoacoustic emission (DPOAE) phase above ～1-1.5 kHz when using frequency-scaled stimuli. Below this frequency demarcation, phase steepens. Cochlear scaling and its breaking have been described in the adult cochlea but have not been studied in newborns. It is not clear whether immaturities in cochlear mechanics exist at birth in the human neonate. In this study, DPOAE phase was recorded with a swept-tone protocol in three, octave-wide segments from 0.5 to 4 kHz. The lowest-frequency octave was targeted with increased signal averaging to enhance signal-to-noise ratio (SNR) and focus on the apical half of the newborn cochlea where breaks from scaling have been observed. The results show: (1) the ear canal DPOAE phase was dominated by the distortion-source component in the low frequencies; thus, the reflection component cannot explain the steeper slope of phase; (2) DPOAE phase-frequency functions from adults and infants showed an unambiguous discontinuity around 1.4 and 1 kHz when described using two- and three-segment fits, respectively, and (3) newborns had a significantly steeper slope of phase in the low-frequency portion of the function which may suggest residual immaturities in the apical half of the newborn cochlea.     

Ipsilateral distortion product otoacoustic emission (2f1-f2) suppression in children with sensorineural hearing loss

Distortion product otoacoustic emission (DPOAE) ipsilateral suppression has been applied to study cochlear function and maturation in laboratory animals and humans. Although DPOAE suppression appears to be sensitive to regions of specialized cochlear function and to cochlear immaturity, it is not known whether it reflects permanent cochlear damage, i.e., sensorineural hearing loss (SNHL), in a reliable and systematic manner in humans. Eight school-aged children with mild-moderate SNHL and 20 normal-hearing children served as subjects in this study. DPOAE (2f1-f2) suppression data were collected at four f2 frequencies (1500, 3000, 4000, and 6000 Hz) using moderate-level primary tones. Features of the DPOAE iso-suppression tuning curves and suppression growth were analyzed for both subject groups. Results show that DPOAE suppression tuning curves from hearing-impaired subjects can be reliably recorded. DPOAE suppression tuning curves were generally normal in appearance and shape for six out of eight hearing-impaired subjects but showed subtle abnormalities in at least one feature. There was not one single trend or pattern of abnormality that characterized all hearing-impaired subjects. The most prominent patterns of abnormality included: broadened tuning, elevated tip, and downward shift of tip frequency. The unique patterns of atypical DPOAE suppression in subjects with similar audiograms may suggest different patterns of underlying sensory cell damage. This speculation warrants further investigation.     

Distortion product otoacoustic emission (2f1-f2) amplitude growth in human adults and neonates

Distortion product otoacoustic emissions (DPOAEs) are thought to be by-products of an active amplification process in the cochlea and thus serve as a metric for evaluating the integrity of this process. Because the cochlear amplifier functions in a level-dependent fashion, DPOAEs recorded as a function of stimulus level (i.e., a DPOAE growth function) may provide important information about the range and operational characteristics of the cochlear amplifier. The DPOAE growth functions recorded in human adults and neonates may provide information about the maturation of these active cochlear processes. Two experiments were conducted. Experiment I included normal-hearing adults and term-born neonates. The 2f1-f2 DPOAE growth functions were recorded for both age groups at three f2 frequencies. Experiment II was an extension of the first experiment but added a subject group of premature neonates. The results of these studies indicate that DPOAE growth functions most often show amplitude saturation and nonmonotonic growth for all age groups. However, premature neonates show monotonic growth and the absence of amplitude saturation more often than adults. Those premature neonates who do show saturation also show an elevated threshold for amplitude saturation relative to adults. In contrast, term neonates are adultlike for most measures except that they show a larger percentage of nonsaturating growth functions than adults. These results may indicate immaturity in cochlear amplifier function prior to term birth in humans. Outer hair cell function and/or efferent regulation of outer hair cell function are hypothesized sources of this immaturity, although some contribution from the immature middle ear cannot be ruled out.     

Ear asymmetries in middle-ear, cochlear, and brainstem responses in human infants

In 2004, Sininger and Cone-Wesson examined asymmetries in the signal-to-noise ratio (SNR) of otoacoustic emissions (OAE) in infants, reporting that distortion-product (DP)OAE SNR was larger in the left ear, whereas transient-evoked (TE)OAE SNR was larger in the right. They proposed that cochlear and brainstem asymmetries facilitate development of brain-hemispheric specialization for sound processing. Similarly, in 2006 Sininger and Cone-Wesson described ear asymmetries mainly favoring the right ear in infant auditory brainstem responses (ABRs). The present study analyzed 2640 infant responses to further explore these effects. Ear differences in OAE SNR, signal, and noise were evaluated separately and across frequencies (1.5, 2, 3, and 4 kHz), and ABR asymmetries were compared with cochlear asymmetries. Analyses of ear-canal reflectance and admittance showed that asymmetries in middle-ear functioning did not explain cochlear and brainstem asymmetries. Current results are consistent with earlier studies showing right-ear dominance for TEOAE and ABR. Noise levels were higher in the right ear for OAEs and ABRs, causing ear asymmetries in SNR to differ from those in signal level. No left-ear dominance for DPOAE signal was observed. These results do not support a theory that ear asymmetries in cochlear processing mimic hemispheric brain specialization for auditory processing.     

Level dependence of distortion product otoacoustic emission phase is attributed to component mixing

Distortion product otoacoustic emissions (DPOAEs) measured in the ear canal represent the vector sum of components produced at two regions of the basilar membrane by distinct cochlear mechanisms. In this study, the effect of stimulus level on the 2f(1)?- f(2) DPOAE phase was evaluated in 22 adult subjects across a three-octave range. Level effects were examined for the mixed DPOAE signal measured in the ear canal and after unmixing components to assess level effects individually on the distortion (generated at the f(1), f(2) overlap) and reflection (at f(dp)) sources. Results show that ear canal DPOAE phase slope becomes steeper with decreasing level; however, component analysis further explicates this result, indicating that interference between DPOAE components (rather than a shift in mechanics related to distortion generation) drives the level dependence of DPOAE phase measured in the ear canal. The relative contribution from the reflection source increased with decreasing level, producing more component interference and, at times, a reflection-dominated response at the lowest stimulus levels. These results have implications for the use of DPOAE phase to study cochlear mechanics and for the potential application of DPOAE phase for clinical purposes.     

Cochlear compression estimates from measurements of distortion-product otoacoustic emissions

Evidence of the compressive growth of basilar-membrane displacement can be seen in distortion-product otoacoustic emission (DPOAE) levels measured as a function of stimulus level. When the levels of the two stimulus tones (f1 and f2) are related by the formula L1 = 39 dB + 0.4 x L2 [Kummer et al., J. Acoust. Soc. Am. 103, 3431-3444 (1998)] the shape of the function relating DPOAE level to L2 is similar (up to an L2 of 70 dB SPL) to the classic Fletcher and Munson [J. Acoust. Soc. Am. 9, 1-10 (1933)] loudness function when plotted on a logarithmic scale. Explicit estimates of compression have been derived based on recent DPOAE measurements from the laboratory. If DPOAE growth rate is defined as the slope of the DPOAE I/O function (in dB/dB), then a cogent definition of compression is the reciprocal of the growth rate. In humans with normal hearing, compression varies from about 1 at threshold to about 4 at 70 dB SPL. With hearing loss, compression is still about 1 at threshold, but grows more slowly above threshold. Median DPOAE I/O data from ears with normal hearing, mild loss, and moderate loss are each well fit by log functions. When the I/O function is logarithmic, then the corresponding compression is a linear function of stimulus level. Evidence of cochlear compression also exists in DPOAE suppression tuning curves, which indicate the level of a third stimulus tone (f3) that reduces DPOAE level by 3 dB. All three stimulus tones generate compressive growth within the cochlea; however, only the relative compression (RC) of the primary and suppressor responses is observable in DPOAE suppression data. An RC value of 1 indicates that the cochlear responses to the primary and suppressor components grow at the same rate. In normal ears, RC rises to 4, when f3 is an octave below f2. The similarities between DPOAE and loudness compression estimates suggest the possibility of predicting loudness growth from DPOAEs; however, intersubject variability makes such predictions difficult at this time.     

Breaking away: violation of distortion emission phase-frequency invariance at low frequencies

The phase versus frequency function of the distortion product otoacoustic emission (DPOAE) at 2f(1) - f(2) is approximately invariant at frequencies above 1.5 kHz in human subjects when recorded with a constant f(2)/f(1). However, a secular break from this invariance has been observed at lower frequencies where the phase-gradient becomes markedly steeper. Apical DPOAEs, such as 2f(1)?- f(2), are known to contain contributions from multiple sources. This experiment asked whether the phase behavior of the ear canal DPOAE at low frequencies is driven by the phase of the component from the distortion product (DP) region at 2f(1)?- f(2), which exhibits rapid phase accumulation. Placing a suppressor tone close in the frequency to 2f(1)?- f(2) reduced the contribution of this component to the ear canal DPOAE in normal-hearing adult human ears. When the contribution of this component was reduced, the phase behavior of the ear canal DPOAE was not altered, suggesting that the breaking from DPOAE phase invariance at low frequencies is an outcome of apical-basal differences in cochlear mechanics. The deviation from DPOAE phase invariance appears to be a manifestation of the breaking from approximate scaling symmetry in the human cochlear apex.     

An empirical bound on the compressibility of the cochlea.

Effects of a possible inner-ear compressibility on middle-ear transfer functions are explored and a small upper bound on the magnitude of that compressibility established. Consequently. the traditional two-port representation of middle-ear mechanics remains valid to within a few percent. If the compressibility of the cochlea is small but finite, a simple phenomenological model of that compressibility correctly predicts hearing thresholds in the "middleless" ear at low frequencies. Experiments to establish the value of cochlear compressibility and to explore further its possible contributions to residual hearing in patients with missing or disarticulated middle-ear ossicles are suggested.     

Input-output functions for stimulus-frequency otoacoustic emissions in normal-hearing adult ears

Input-output (I/O) functions for stimulus-frequency (SFOAE) and distortion-product (DPOAE) otoacoustic emissions were recorded in 30 normal-hearing adult ears using a nonlinear residual method. SFOAEs were recorded at half octaves from 500-8000 Hz in an L1=L2 paradigm with L2=0 to 85 dB SPL, and in a paradigm with L1 fixed and L2 varied. DPOAEs were elicited with primary levels of Kummer et al. [J. Acoust. Soc. Am. 103, 3431-3444 (1998)] at f2 frequencies of 2000 and 4000 Hz. Interpretable SFOAE responses were obtained from 1000-6000 Hz in the equal-level paradigm. SFOAE levels were larger than DPOAEs levels, signal-to-noise ratios were smaller, and I/O functions were less compressive. A two-slope model of SFOAE I/O functions predicted the low-level round-trip attenuation, the breakpoint between linearity and compression, and compressive slope. In ear but not coupler recordings, the noise at the SFOAE frequency increased with increasing level (above 60 dB SPL), whereas noise at adjacent frequencies did not. This suggests the existence of a source of signal-dependent noise producing cochlear variability, which is predicted to influence basilar-membrane motion and neural responses. A repeatable pattern of notched SFOAE I/O functions was present in some ears, and explained using a two-source mechanism of SFOAE generation.     

A comparative study of distortion-product-otoacoustic-emission fine structure in human newborns and adults with normal hearing

Distortion product otoacoustic emissions (DPOAE) measured in human newborns are not adult-like. More than a decade of work from various investigators has created a well-developed body of evidence describing these differences but the putative anatomy or physiology has only been partially explained. Recently, Abdala and Keefe [J. Acoust. Soc. Am. 120, 3832-3842 (2006)] have identified outer and middle ear immaturities that at least partially describe the differences observed between newborn and adult input-output functions and suppression tuning curves. DPOAE fine structure characteristics and their maturation have not been examined to any extent in the literature. Fine structure characteristics in two groups of ten newborns and young adults with normal hearing sensitivity are compared here. Consistent with previous reports, the newborns show higher DPOAE levels; greater fine structure depth and wider fine structure spacing is also observed in the newborns. Differences in fine structure morphology are also observed between the two age groups. While some of these findings are attributable to an immature outer and middle ear system in the newborns, it is argued that some observed differences in fine structure characteristics might be due to remnant immaturities in passive motion of the basilar membrane in the newborn cochlea.     

Suppression of distortion product otoacoustic emissions and hearing threshold

A distortion product otoacoustic emission (DPOAE) suppression tuning curve (STC) shows the minimum level of suppressor tone that is required to reduce DPOAE level by a fixed amount, as a function of suppressor frequency. Several years ago, Mills [J. Acoust. Soc. Am. 103, 507-523 (1998)] derived, theoretically, an approximately linear relationship between the tip-to-tail suppressor level difference on a DPOAE STC, and the gain of the cochlear amplifier, defined as the maximum increase in the active over the passive basilar membrane (BM) response. In this paper, preliminary data from adult human subjects are presented that establish a correlation between this tip-to-tail DPOAE STC difference and the threshold of hearing, the latter measured at the frequency of the f2 primary tone. Assuming that both suppression and the DPOAE are by-products of active, nonlinear BM dynamics, the above result suggests that threshold elevation in mild levels of hearing loss may be attributed, in part, to a reduction of cochlear amplifier gain, which is detectable with the suppression paradigm.     

Simultaneous recording of stimulus-frequency and distortion-product otoacoustic emission input-output functions in human ears

Stimulus frequency otoacoustic emission (SFOAE) input-output (I/O) functions were elicited in normal-hearing adults using unequal-frequency primaries in equal-level and fixed-suppressor level (Ls) conditions. Responses were repeatable and similar across a range of primary frequency ratios in the fixed-Ls condition. In comparison to equal-frequency primary conditions [Schairer, Fitzpatrick, and Keefe, J. Acoust. Soc. Am. 114, 944-966 (2003)], the unequal-frequency, fixed-Ls condition appears to be more useful for characterizing SFOAE response growth and relating it to basilar-membrane response growth, and for testing the ability to predict audiometric thresholds. Simultaneously recorded distortion-product OAE (DPOAE) I/O functions had higher thresholds than SFOAE I/O functions, and they identified the onset of the nonlinear-distortion mechanism in SFOAEs. DPOAE threshold often corresponded to nonmonotonicities in SFOAE I/O functions. This suggests that the level-dependent nonmonotonicities and associated phase shifts in SFOAE I/O functions were due to varying degrees of cancellation of two sources of SFOAE, such as coherent reflection and distortion mechanisms. Level-dependent noise was observed on-band (at the frequencies of the stimuli) but not off-band, or in the DPOAEs. The variability was observed in ears with normal hearing and ears with cochlear implants. In general, these results indicate the source of the variability is biological, possibly from within the middle ear.     

Maturation of medial efferent system function in humans

Otoacoustic emissions are typically reduced in amplitude when broadband noise is presented to the contralateral ear. This contralateral suppression is attributed to activation of the medial olivocochlear system, which has an inhibitory effect on outer hair-cell activity. By studying the effects of contralateral noise on cochlear output at different stages of auditory maturation in human neonates, it is possible to describe the timecourse for development of medial efferent system function in humans. The present study recorded 2 f1-f2 distortion product otoacoustic emissions (DPOAE) in human adults, term and premature neonates at three f2 frequencies: 1500, 3000, and 6000 Hz, using fixed primary tone frequency ratio (f2/f1 = 1.2) and level separation (10 dB, L1 > L2). Average DPOAE growth functions were recorded with and without contralateral broadband noise. Results indicate that contralateral suppression of DPOAEs is absent at 6000 Hz, but present at 1500 and 3000 Hz for all ages. However, DPOAE amplitude from premature neonates was not altered by noise in an adult-like manner; in this age group, DPOAE amplitude was equally likely to by suppressed or enhanced by noise presented contralaterally. Contralateral enhancement may reflect a temporary stage of immaturity in outer hair cell-medial efferent fiber synapses just prior to term birth.     

Suppression tuning in noise-exposed rabbits

Psychophysical, basilar-membrane (BM), and single nerve-fiber tuning curves, as well as suppression of distortion-product otoacoustic emissions (DPOAEs), all give rise to frequency tuning patterns with stereotypical features. Similarities and differences between the behaviors of these tuning functions, both in normal conditions and following various cochlear insults, have been documented. While neural tuning curves (NTCs) and BM tuning curves behave similarly both before and after cochlear insults known to disrupt frequency selectivity, DPOAE suppression tuning curves (STCs) do not necessarily mirror these responses following either administration of ototoxins [Martin et al., J. Acoust. Soc. Am. 104, 972-983 (1998)] or exposure to temporarily damaging noise [Howard et al., J. Acoust. Soc. Am. 111, 285-296 (2002)]. However, changes in STC parameters may be predictive of other changes in cochlear function such as cochlear immaturity in neonatal humans [Abdala, Hear. Res. 121, 125-138 (1998)]. To determine the effects of noise-induced permanent auditory dysfunction on STC parameters, rabbits were exposed to high-level noise that led to permanent reductions in DPOAE level, and comparisons between pre- and postexposure DPOAE levels and STCs were made. Statistical comparisons of pre- and postexposure STC values at CF revealed consistent basal shifts in the frequency region of greatest cochlear damage, whereas thresholds, Q10dB, and tip-to-tail gain values were not reliably altered. Additionally, a large percentage of high-frequency lobes associated with third tone interference phenomena, that were exhibited in some data sets, were dramatically reduced following noise exposure. Thus, previously described areas of DPOAE interference above f2 may also be studied using this type of experimental manipulation [Martin et al., Hear. Res. 136, 105-123 (1999); Mills, J. Acoust. Soc. Am. 107, 2586-2602 (2002)].