Olivocochlear Efferent Suppression in Classical Musicians

Transcription

1 Olivocochlear Efferent Suppression in Classical Musicians Shanda M. Brashears* Thierry G. Morlet* Charles I. Berlin* Linda J. Hood* Abstract Suppression of transient-evoked otoacoustic emissions was recorded from 29 members of the Louisiana Philharmonic Orchestra and 28 non-musician control subjects matched for age and gender. Binaural broad band noise was used as the suppressor stimulus in a forward masking paradigm. Results showed musicians to have significantly more suppression than non-musicians for both the right and left ears. Two possible explanations for this functional difference between groups are that moderately loud music serves as a sound conditioning stimulus and that music can be a mechanism for strengthening central auditory pathways which may influence the olivocochlear reflex arc. Possible explanations for this are discussed and ear, gender, and age differences within each group are examined. Additionally, middle-ear muscle reflex thresholds were found to be higher in musicians than non-musicians at some frequencies in some conditions. Key Words: Human, middle-ear muscle reflex, musicians, otoacoustic emission, suppression of otoacoustic emission, transient-evoked otoacoustic emission Abbreviations: OHC = outer hair cell, OAE = otoacoustic emission, MOCS = medial olivocochlear system, TEOAE = transient-evoked otoacoustic emission, LPO = Louisiana Philharmonic Orchestra, KEM = Kresge EchoMaster, MEMR = middle ear muscle reflex, TTS = temporary threshold shift, PTS = permanent threshold shift Sumario: Se registró la supresión de las emisiones otoacústicas evocadas por transitorios a 29 miembros de la Orquesta Filarmónica de Louisiana, y a un grupo de 28 sujetos control, no músicos, equiparados por edad y género. Se utilizó un ruido binaural de banda ancha como el estímulo supresor, en un paradigma de enmascaramiento anterógrado. Los resultados mostraron que los músicos tenían mayor supresión que los no músicos, tanto para el oído derecho como para el izquierdo. Dos posibles explicaciones para esta diferencia funcional entre los grupos son que la exposición a música moderadamente fuerte sirve como estímulo condicionante al sonido, y que la música puede ser un mecanismo para fortalecer las vías auditivas centrales, las cuales pueden influir en el arco reflejo olivococlear. Se discuten explicaciones posibles para los resultados y se examinan las diferencias de oído, género y edad dentro de cada grupo. Además, se encontró que los umbrales para el reflejo *Kresge Hearing Research Laboratory, Department of Otorhinolaryngology, Louisiana State University Health Sciences Center Reprint requests: Shanda M. Brashears, Kresge Hearing Research Laboratory, 533 Bolivar St., 5th Floor, New Orleans, Louisiana 70112; Ph: ; Fax: ; sbrash@lsuhsc.edu 314

2 Olivocochlear Efferent Suppression in Classical Musicians/Brashears et al. muscular del oído medio son más altos en los músicos que en los no músicos, en algunas frecuencias, bajo determinadas condiciones. Palabras Clave: Emisión otoacústica; emisión otoacústicas evocada por transitorios; supresión de la emisión otoacústica; reflejo muscular del oído medio, humano, músicos. Abreviaturas: OHC = células ciliadas externas; OAE = emisión otoacústica; MOCS = sistema olivococlear medial; TEAOE = emisión otoacústica evocada por transitorios; LPO = Orquesta Filarmónica de Louisiana; KEM = EchoMaster de Kresge; MEMR = reflejo muscular del oído medio; TTS = cambio temporal de umbral; PTS = cambio permanente de umbral. The auditory efferent system includes neural pathways that transmit information from the lower brainstem to the cochlea (Warr and Guinan, 1978). The medial component consists of large, myelinated fibers that originate around the medial nuclei of the superior olivary complex and terminate beneath the outer hair cells (OHCs) of the organ of Corti (Warr and Guinan, 1978; Warr et al., 1986). Some medial olivocochlear neurons project contralaterally and some project ipsilaterally, with most OHCs having binaural inputs (Liberman, 1988). When activated acoustically, the medial olivocochlear system (MOCS) inhibits activity of the OHCs as shown by a decrease in the level of otoacoustic emissions (OAEs) in normally functioning ears (Collet et al., 1990; Veuillet et al., 1991; Hood et al., 1996). The amount of suppression is quantitatively measured by subtracting the level of the emission in the presence of the suppressor stimulus from the level without the suppressor. The function and purpose of the MOCS is not completely understood. In attempts to further understand its function, various psychoacoustic measures such as the ability to detect signals in noise and loudness adaptation have been studied in relation to MOCS strength (Micheyl and Collet, 1995; Micheyl et al., 1995a, b). Another approach to uncovering its functionality has been to study MOCS differences among different subject populations. Research has shown that musicians have a greater degree of suppression in response to contralateral noise than non-musicians (Micheyl et al., 1995a, 1997; Perrot et al., 1999). Micheyl and colleagues (1995a), in studying the right ears of a mixed group of musicians and non-musicians, found a positive correlation between contralateral suppression and the ability to maintain accurate loudness perception across a broad range of frequencies. Additionally, they found that both efferent suppression and loudness adaptation were stronger in musicians than non-musicians. In a subsequent experiment, these researchers again compared contralateral suppression between musicians and non-musicians in the right ear and found that musicians had significantly more suppression of transient-evoked otoacoustic emissions (TEOAEs) in response to contralateral stimulation than non-musicians (Micheyl et al., 1997). Perrot et al. (1999) found the same result for right and left ears with both groups having a right ear suppression advantage, a phenomenon noted by previous researchers (Khalfa and Collet, 1996; Khalfa et al., 1998), with no difference in this advantage between musicians and non-musicians. These experiments all measured efferent suppression with contralateral broad-band noise (BBN) as the suppressor stimulus using a method developed by Collet and colleagues (1990). This method was used in many other germinal human suppression studies (Giraud et al., 1995; Graham and Hazell, 1994; Micheyl and Collet, 1995; Micheyl et al., 1995a, b; Veuillet et al., 1991; Williams et al., 1994), and because it is the simplest way to elicit a suppression effect non-invasively, it is still commonly used (Maison et al., 2001; Quaranta et al., 2001). However, because most OHCs have inputs from both the ipsilateral and contralateral superior olivary complex, more fibers can be stimulated when the suppressor stimulus is presented binaurally. Berlin and colleagues (1994, 315

3 1996) developed methods to measure suppression to bilateral and ipsilateral stimuli as well as contralateral stimuli using a forward masking paradigm. This was accomplished for the ILO systems in collaboration with David Kemp and also resulted in the development of a custom designed Labview system (Kresge EchoLab). As the physiology would predict, binaural stimulation produces the strongest efferent effect followed by ipsilateral and then contralateral stimuli (Berlin et al., 1995). Suppression that is measured using binaural stimuli is referred to here as binaural suppression. All of the studies to date comparing the efferent suppression of musicians to nonmusicians were conducted by the same team and used the mode Lyon method of stimulation and recording that compares TEOAEs with and without a continuous contralateral suppressor stimulus. To better understand this phenomenon, binaural suppression, as well as pure-tone and middleear muscle reflex (MEMR) thresholds and TEOAEs were compared between musicians and non-musicians. Suppression was also analyzed for ear, gender, and age differences within and between these two groups. Subjects METHOD Forty-four members of the Louisiana Philharmonic Orchestra (LPO), 21 females and 23 males, participated in a hearing conservation program set up by the Kresge Hearing Research Laboratory. All members of the LPO who participated in the hearing conservation program also enrolled in this suppression study. Of these 44 participants, eight were dropped for the following reasons: two had complicated middle ear histories and mild conductive hearing losses that precluded emission recording, five subjects had no emissions due to bilateral sensorineural hearing loss, one with a noise notch, and one subject had a unilateral, sensorineural hearing loss with no emissions bilaterally. Of the remaining 36 normal hearing participants, six were recorded using an ILO92 system. The timing parameters used to run these six subjects were later discovered to be different from the parameters used to run subjects on the Labview system. Because of this difference, these six subjects were also eliminated from the final suppression analysis. Finally, both ears of one subject and the left ear of an additional subject were eliminated from the final analysis due to a lack of emissions in the absence of pure-tone hearing loss leaving 29 right ears and 28 left ears. Emission criteria are discussed in the next section. A detailed case history was obtained from each participating musician in which information concerning level of training in music and weekly exposure to music was acquired. All but one of the experimental subjects have a bachelors degree or higher in music, and years of study in music vary from 22 to 55 years. The exception was a 24-yearold undergraduate music student with 13 years of formal music training. String, brass, percussion, and woodwind instrumentalists were all represented in this population. All the musicians had negative case histories of non-musical noise exposure. Weekly exposure to classical music for each subject included h/wk of LPO practice and performances, with summers off. Personal practice varied from 2-30 h/wk. Typically, subjects reported practicing h weekly and, in addition, many members also taught private lessons and/or played in smaller ensembles. Inclusion Criteria Criteria for inclusion in the suppression study for experimental and control subjects were normal pure-tone thresholds, defined as 25 db HL or better, at 250, 500, 1000, 2000, 3000, 4000, 6000, and 8000 Hz, normal ipsilateral and contralateral MEMR at 500, 1000, and 2000 Hz, normal tympanometry, and normal TEOAEs. Normal TEOAEs were defined as having a stimulus stability exceeding 80%, an overall wave reproducibility exceeding 70%, and a signalto-noise amplitude in the frequency bands centered at 1000 and 2000 Hz exceeding 4 db. Additionally, subjects had no history of middle ear disease, ototoxic drugs, familial hearing impairment, or non-musical noise exposure. One normal hearing, experimental subject who was recorded on the Labview system for suppression was eliminated completely from the suppression study on 316

4 Olivocochlear Efferent Suppression in Classical Musicians/Brashears et al. the basis of TEOAE criteria leaving 29 subjects (17 females and 12 males). Another subject s left ear only was eliminated because of poor emissions leaving 29 right ears and 28 left ears for the musician group. Their ages ranged from (mean age of 39.3 ± 11.5 yr; median age of 34 yr). Experimental subjects were matched for age and gender to 28 normal hearing, non-musician control subjects, 17 females and 11 males. Control subjects ranged in age from (mean age of 38.1 ± 10.1 yr; median age of 35.5 yr). Non-musicians were defined as having no formal training in music and no formal music experience within the 7 yr prior to the onset of the study. Apparatus Pure-tone audiometry was completed for each subject using a clinical audiometer (GSI- 10). Tympanometry and middle-ear muscle reflex testing was performed using a clinical immittance bridge (GSI-33). Ipsilateral and contralateral MEMRs were measured in response to 500, 1000, 2000, and 4000 Hz tones. Ipsilateral and contralateral reflexes were also measured in response to broadband noise (BBN) for a subset of seven subjects. TEOAEs were recorded to determine if inclusion criteria were met using a commercial instrument (Otodynamics ILO88, v5.6) with the standard 80 db peak sound pressure non-linear click default protocol with a commercially available OAE probe (Otodynamics SGD-type) in the ear canal. In the non-linear mode, click trains of four clicks each consist of three 80 db pespl clicks of one polarity and a fourth 90 db pespl click of the opposite polarity. This method of adding out-of-phase stimuli serves to minimize the stimulus artifact. Two hundred sixty sweeps of four clicks per sweep were performed in each ear. Pure-tone, emission, and suppression testing took place in a sound treated booth. Binaural suppression using the Labview system was measured using ER10-C probe microphones / transducers in both ears with an 80 us linear click calibrated to the test ear canal to be 65 db pespl prior to data acquisition, and the binaural noise bursts were presented at 70 db pespl. This noise / click relationship at these levels was chosen because Hood and colleagues (1996) showed them to elicit emissions and a substantial suppression effect. Four hundred ms BBN bursts were presented binaurally at 70 db peak SPL in a forward masking paradigm with an interstimulus interval of 10 ms separating the noise from the click. Sweeps exceeding the noise reject level set at 45 db SPL were eliminated from the final sample. One hundred sweeps were averaged for each condition and each ear. Two without-noise and two with-noise conditions were presented to each test ear in an interleaved fashion. Data Analysis Like conditions (i.e., with or without noise) were added together, and the sum of the withnoise conditions was subtracted from the sum of the without-noise conditions. The root mean square (RMS) amplitude difference between the two tracings was compared using custom software [Kresge EchoMaster (KEM) v4.0 developed by Wen et al. (1993)]. A value for the overall RMS suppression was derived for the time window between 8 and 18 ms. This is the time window within which the most suppression occurs (Veuillet et al., 1991; Berlin et al., 1993). In addition to the overall RMS amplitude difference, values were derived to represent RMS suppression across nine 2-ms time bands from 2 20 ms and in the spectral domain across 32 frequency bands. For pure-tone thresholds, OAE level, and MEMR thresholds, comparisons between musicians and non-musicians were made for the right and left ears separately with two way repeated measures analysis of variance (ANOVA) using SigmaStat version 2.03 software with frequency (for pure-tone thresholds), frequency band (for OAE level), and frequency and condition (for MEMR, i.e., 500 Hz ipsilateral, 500 Hz contralateral, etc.) as the repeated measures, respectively. Additionally, a linear regression was performed to investigate any possible correlation between emission level and suppression. Finally, for the seven musician subjects who underwent BBN MEMR threshold testing, a linear regression was performed to investigate the possibility of any correlation between BBN reflex thresholds and suppression. For overall suppression from 8 to 18 ms, a two way repeated measures ANOVA was used to compare the two groups with ear as the repeated measure. One way ANOVA was used to analyze each groups right and left 317

5 ears separately (i.e., non-musicians right ear, non-musicians left ear, musicians right ear, musicians left ear) for age and gender differences. Subjects were separated into younger and older with younger defined as less than 34 years, 7 months chronological age and older defined as greater than 34 years, 7 months chronological age. There were 16 younger musician subjects (4 men and 12 women), 13 older musician subjects (8 men and 5 women), 13 younger non-musician subjects (4 men and 9 women), and 15 older non-musician subjects (7 men and 8 women). For suppression across time periods, two way repeated measures ANOVAs were used to compare the two groups, examine each group for ear differences, and to analyze each groups right and left ears separately for age and gender differences all with time period as the repeated measure. The same was performed across these measures for spectral suppression with frequency band as the repeated measure. All post hoc pairwise multiple comparison procedures were performed using the Tukey test. The authors adopted p < 0.05 as the desired level of statistical significance. Data in the figures are presented as the mean + 1 SD as in Figure 1 or the mean ± 1 SD as in Figures 2 and 3. RESULTS Pure-Tone Thresholds, TEOAE Level, and MEMR Thresholds No difference was evident between the musician and non-musician groups for puretone thresholds or TEOAE level. The average difference in the mean pure-tone thresholds across frequency between musicians and nonmusicians was 0.83 db HL for the right ear and 0.67 db HL for the left (ranging from 0.17 db HL to 4.26 db HL). The average difference in TEOAE level without efferent stimulation across frequency was 0.72 db SPL for the right ear and 0.38 db SPL for the left (ranging from 0.37 db SPL to 2.73 db SPL). Figure 1. The average and + 1 SD for the middle-ear muscle reflex thresholds for left and right ipsilateral and contralateral stimuli at.5, 1, 2 and 4 KHz of 29 non-musicians and 29 musicians. 318

6 Olivocochlear Efferent Suppression in Classical Musicians/Brashears et al. However, as indicated in panels A-D of Figure 1, MEMR thresholds were higher for musicians than non-musicians, especially for the following conditions: left contralateral (Fig. 1C) 500 Hz stimulation and right contralateral (Fig. 1D) 500 Hz stimulation and 2000 Hz stimulation ms Overall RMS Suppression A comparison of overall RMS suppression from 8 18 ms for musicians versus nonmusicians revealed a nearly significant difference between groups (p < 0.058; musician mean = 4.447; non-musician mean = 3.542; standard error = 0.332). While women tended to have more suppression than men, and younger subjects tended to have more suppression than older subjects, no significant differences were discovered within either group in either ear. As previously established by Hood et al. (1996), no correlation was found between suppression and TEOAE level. Likewise, no correlation was established between suppression and MEMR thresholds to BBN stimuli. RMS Suppression across Time When musicians were compared to nonmusicians on RMS suppression across nine 2- ms time bands as seen in Figure 2, musiciansure showed more suppression effect than nonmusicians for the right and left ears with greater differences in the later time bands between 8 and 20 ms. Differences were only significant for the right ear, however (p < 0.012; Fig. 2B). When ear differences were analyzed across time, a nearly significant right ear advantage was discovered for musicians (p < 0.067) but not for non-musicians. No large gender differences were found within either ear of either group. However, within the group of musicians younger subjects showed significantly more suppression than older subjects for the left (p < 0.046) and right (p < 0.032) ears. There was a nearly significant age difference for the left ears of nonmusicians subjects as well (p < 0.074). No age differences were seen within the nonmusician group for the right ear. Spectral Suppression across Frequency Spectral suppression was analyzed across 32 frequency bands from khz to 6.25 khz, revealing, as shown in Figure 3, significant differences between musicians and non-musicians for the left (p < 0.008; Fig. 3A) and right (p < 0.011; Fig. 3B) ears. The greatest difference between groups was seen between 1 and 4 khz for the left and between.5 and 3.5 khz for the right ear. This type of analysis did not reveal ear or gender differences within either group. Figure 2. The average RMS suppression and ± 1 SD over time between 2 and 20 ms for the left and right ears of 29 non-musicians and 28 left ears and 29 right ears of musicians. While musicians show more suppression than non-musicians for both ears, only the right ear difference was statistically significant using this analysis paradigm (p = 0.012). For both ears, differences were more pronounced in the later time bands. 319

7 Figure 3. The average spectral suppression and ± 1 SD across 32 frequency bands for the left and right ears of 29 non-musicians and 28 left ears and 29 right ears of musicians. Suppression was significantly stronger among musicians as compared to non-musicians for the right (p = 0.011) and left (p = 0.008) ears with the largest differences seen between 1 and 4 khz for the left ear and between.5 and 3.5 khz for the right ear. However, younger musician subjects showed significantly more suppression than older musician subjects for the right ear (p < 0.013). This younger ear advantage for musicians was nearly significant for the left ear (p < 0.054). Age differences were not seen within the non-musician group. DISCUSSION The main finding of the current study is congruent with previous findings (Micheyl et al., 1995a, 1997; Perrot et al., 1999) that musicians have a larger measurable efferent suppression effect than non-musicians. The current study compliments previous studies by demonstrating the effect of binaural acoustic stimulation on efferent pathways between musicians and non-musicians. While the typical trends of stronger suppression for women and younger subjects were noted for both groups, the present study only found significant gender and age differences within the musician group. Supposedly the large degree of variability among the non-musician subjects is the reason. Similarly, the right ear advantage previously observed by Khalfa and Collet (1996) and Khalfa et al. (1998) was only observed here within the musician group. The lack of any clear-cut ear advantage seen in the non-musician group is again explained by the large degree of variability within this particular group of non-musicians. The unexpected finding that musicians have higher MEMR thresholds than nonmusicians uncovers another auditory variation in this population, the mechanisms of which are unclear and may give rise to further investigation. The rest of this discussion will focus on possible explanations for our finding that musicians have stronger binaural efferent suppression and higher middle-ear muscle reflex thresholds than non-musicians. Links between the MEMR and the MOCS Middle-ear muscle reflex (MEMR) threshold data were acquired on the subjects in this suppression study because the MEMR arc represents an efferent pathway similar in some ways to that of the MOCS. The possibility that the MEMR confounds the ability to use emission recordings to evaluate the MOCS has long been under scrutiny. The MOCS and the MEMR both alter auditory input to the cochlea in the presence of acoustic stimulation, thus decreasing OAE level in the ear canal and subsequently afferent eighth nerve firing. The MOCS does this via efferent eighth nerve innervation of the OHCs and the MEMR via the seventh nerve innervation of the stapedius muscle. Activation of the MEMR arc causes a contraction of the stapedius muscle, functionally reducing the amount of low frequency energy that can pass through the 320

8 Olivocochlear Efferent Suppression in Classical Musicians/Brashears et al. middle ear. It has been argued that the suppression of OAEs in response to acoustic stimuli is not a function of the MOCS but simply a function of the MEMR or at least some combination of the two. However, the MOCS is maximally activated at low intensity levels while the MEMR is maximally activated at high intensity levels, and the two responses have differences in their frequency specificity. Additionally, suppression of OAEs has been measured in subjects who have no MEMR at all (Veuillet et al., 1991) and in guinea pigs whose MEMR pathway was chemically relaxed (Cody and Johnstone, 1982). In this experiment, musicians were unexpectedly discovered to have higher MEMR thresholds than non-musicians. This difference, however, is not believed to account for suppression differences seen between the two groups. If MEMRs were accounting for the presence of the larger suppression effect seen in musicians, thresholds would be lower for musicians than for non-musicians. Since the opposite is true, it is highly unlikely that the middle ear s reduction of OAEs in response to BBN can account for the suppression differences seen between these two groups. In addition, seven subjects were examined for their MEMR in response to BBN. No correlation was found between their MEMR threshold and suppression. While the sample size was small for this portion of the experiment, in light of previous findings cited above and the higher MEMR thresholds seen in these musicians, we believe that it is the strength of the MOCS, and not the MEMR, that accounts for the difference in the suppression of musicians. MEMR differences between musicians and non-musicians were neither hypothesized or expected. These differences may be a result of sound conditioning which is discussed in the following section. While the effects of sound conditioning on the MOCS have been explored, the effects of sound conditioning on the MEMR is less documented and needs further investigation. Mechanisms of Improved Suppression The daily and weekly exposure to music experienced by the musicians in this study may serve to provide their ears with some degree of sound conditioning. Sound conditioning is the beneficial effect of lowintensity, non-damaging sound on subsequent, potentially detrimental levels of noise exposure. Sound conditioning has been shown to ameliorate the damaging effects of noise trauma in various animal models as measured by temporary threshold shift (TTS) (Eldredge et al., 1959; Miller et al., 1963) and permanent threshold shift (PTS) (Canlon et al., 1988). More current research has shown that olivocochlear neurons are plastic and that the MOCS is playing a role in conditioning previously exposed ears to better withstand toxic levels of noise (Kujawa and Liberman, 1997; Brown et al., 1998;). This protective, functional role of the MOCS appears to be shared by the toughening of the OHCs themselves (Kujawa & Liberman, 1999). Our finding of higher MEMR thresholds for musicians may indicate that this auditory system also sustains changes as a result of conditioningtype noise exposures. The constant dose of low-level noise exposure in the form of music may be conditioning the musicians ears and thus providing an increased ability to suppress OAEs and increased MEMR tolerance. In addition to their regular exposure to moderately loud sounds, musicians training and experience in music separates them from their non-musician counterparts. Functional differences may include temporal processing, frequency resolution, and phase perception. These auditory cortical strengths in musicians may be affecting lower pathways such as the MOCS. There are auditory neural fibers that descend from the three cortical auditory fields (first, second, and anterior auditory fields) to the thalamus (Andersen et al., 1980; Rouiller et al., 1991). Although it has been traditionally believed that the MOCS is a fast, reflex-type of pathway that is not influenced by higher brain centers, more recent evidence points to the contrary. Froehlich et al. (1993) found that attention could affect suppression of TEOAEs with a maximum effect between 1 and 2 khz for a visual task and a maximum effect between 2 and 3 khz for an auditory task. Central anesthesia has been shown to reduce MOCS activity in guinea pigs strongly suggesting that there is a central influence on this pathway (Robertson and Gummer, 1985; Gummer et al., 1988). In addition, subjective factors have been shown to affect the detrimental effects of 321

9 noise on hearing. TTS following noise exposure has been shown to exceed TTS following exposure to music of equal energy (Lindgren and Axelsson, 1983; Swanson et al., 1987). The effect of preference on cochlear vulnerability points to an influence of the cerebral cortex on auditory efferent activity. If the temporal lobes and other cortical centers are in fact influencing the MOCS, this may be a mechanism through which training in music and/or the virtue of musicianship itself assert their beneficial effects on the auditory periphery. Benefits of Improved Suppression While music as a source of sound conditioning may be improving mechanisms of the MOCS, it is from music as acoustic trauma that the cochlea needs protection. Protection from noise may be one benefit of having increased suppression for these musicians who do in fact need some cochlear protection. Research shows that the efferent system may play an important role in protecting the cochlea from injury due to acoustic trauma. Cody and Johnstone (1982) found that contralateral acoustic stimulation reduces TTS in guinea pigs; electrical stimulation of efferents also reduces TTS (Rajan, 1991). While these studies show that efferent stimulation reduces acoustic injury, the opposite is also true: efferent inhibition increases acoustic injury. In the aforementioned study (Cody and Johnstone, 1982), TTS increased when efferent activity was blocked by strychnine. Kujawa and Liberman (1997) showed that chronic olivocochlear sectioning in animals results in an increase in PTS. Research in humans shows that there is little or no suppression effect at 4 khz (Veuillet et al., 1992). This frequency area of the cochlea is the first to sustain damage as a result of noise exposure, leading these researchers to suggest that the lack of efferent innervation in this area may contribute to the vulnerability of these frequencies to acoustic injury. Other human research consists of a case study on a subject who underwent a vestibular neurectomy (Scharf et al., 1994), which surgically impairs the efferent system, and an efferent comparison of subjects with noise induced sensorineural hearing loss versus other types of sensorineural hearing loss (Collet et al., 1991). These studies strongly suggested that one major role of the MOCS is in protecting the cochlea from loud sounds. Considering the age of the musicians in this study and the extent of their noise exposure, the incidence of sensorineural hearing loss was quite low (six of 44 subjects). In addition, TEOAE loss in the absence of pure-tone threshold loss has been previously reported (Attias et al., 1995) and was expected to be high in this population. However, it was also surprisingly low with only two normal hearing subjects falling below our emission criteria (one in both ears, and one for the left ear only). Plus, no difference in TEOAE level was seen between the remaining musicians and their age and gender matched controls (Fig. 2). It is possible that the strong MOCSs of these musicians have protected their cochlea from years of acoustic trauma. Another possible benefit of having a strong MOCS is its association with the ability to detect signals in noise and loudness adaptation. Evidence suggests that the efferent system plays a role in improving our ability to detect signals in noise. In some early animal research, Dewson (1968) showed that sectioning the olivocochlear bundle reduced the ability of trained monkeys to discriminate between vowel sounds in noise. More recently, using physiologic measures, Kawase et al. (1993) showed that a contralateral acoustic stimulus increases the afferent auditory nerve firing rate to tones but decreases the firing rate to the noise in which the tones are buried. Scharf et al. (1997) studied patients who had undergone vestibular neuronectomies in their ability to detect signals in noise. It was suggested that their impaired ability to do so was due to a deficit in selective attention caused by the surgical removal of efferent function. Studies showing a positive correlation between the detection threshold of tones in noise and efferent suppression of OAEs also support the theory that the efferent system plays a role in the ability to detect signals in noise (Micheyl and Collet, 1995; Micheyl et al., 1995b). The MOCS is also thought to play a role in loudness adaptation. A positive correlation has been found between suppression and the ability to maintain accurate loudness perception across a broad range of frequencies (Micheyl et al., 1995a). While psychoacoustical measures such as signal detection in noise and loudness adaptation were not investigated in the current study, these and other acute listening skills are considered to 322

10 Olivocochlear Efferent Suppression in Classical Musicians/Brashears et al. be consistent with musicianship. It is possible that training in music and musicianship are not only contributing to improved suppression, but also that the virtue of a stronger MOCS helps to improve auditory skills. SUMMARY The findings of this study confirm the previous findings (Micheyl et al., 1995a, 1997; Perrot et al., 1999) that musicians have a greater degree of auditory efferent suppression than non-musicians. Whereas previous studies investigated differences in contralaterally stimulated suppression, the current study found a suppression difference for binaural suppression. In addition, a difference was found between musicians and non-musicians for MEMR thresholds with musicians having higher thresholds than non-musicians. Further investigation into the differences between the auditory systems of musicians and non-musicians and the mechanisms underlying them can shed light on our understanding of the auditory efferent system and the functional physiology of other auditory systems as well. Acknowledgment. This research was funded by the National Academy of Recording Arts and Sciences. We would also like to thank the Louisiana Philharmonic Orchestra for their participation and enthusiasm as well as the New Orleans Musicians Clinic for their collaborative efforts. REFERENCES Andersen RA, Knight PL, Merzenich MM. (1980). The thalamocortical and corticothalamic connections of AI, AII, and the anterior auditory field (AAF) in the cat: evidence for two largely segregated systems of connections. J Comp Neurol 194: Attias J, Furst M, Furman V, et al. (1995). Noiseinduced otoacoustic emission loss with or without hearing loss. Ear Hear 16: Berlin CI, Hood LJ, Cecola RP, et al. (1993). Does type I afferent neuron dysfunction reveal itself through lack of efferent suppression? Hear Res 65: Berlin CI, Hood LJ, Hurley A, Wen H. (1994). Bilateral and ipsilateral forward masking and TEOAE suppression. Abstr Assoc Res Otolaryngol 17: 52. Berlin CI, Hood LJ, Hurley AE, et al. (1995). Binaural noise suppresses linear click-evoked otoacoustic emissions more than ipsilateral or contralateral noise. Hear Res 87: Berlin CI, Hurley A, Hood LJ, et al. (1996). Binaural efferent suppression of low-level linear click-evoked otoacoustic emissions. Abstr Assoc Res Otolaryngol 19: 24. Brown MC, Kujawa SG, Liberman MC. (1998). Single olivocochlear neurons in the guinea pig. II. Response plasticity due to noise conditioning. J Neurophysiol 79: Canlon B, Borg E, Flock A. (1988). Protection against noise trauma by pre-exposure to a low level acoustic stimulus. Hear Res 34: Cody AR, Johnstone BM. (1982). Temporary threshold shift modified by binaural acoustic stimulation. Hear Res 6: Collet L, Kemp DT, Veuillet E, et al. (1990). Effects of contralateral auditory stimuli on active cochlear micro mechanical properties in human subjects. Hear Res 43: Collet L, Morgon A, Veuillet E, Gartner M. (1991). Noise and medial olivocochlear system in humans. Acta Olaryngol 111: Dewson JH. (1968). Efferent olivocochlear bundle: some relationships to stimulus discrimination in noise. J Neurophysiol 57: Eldredge DH, Covell WP, Gannon RP. (1959). Acoustic trauma following intermittent exposure to tones. Ann Otol Rhinol Laryngol 68: Froehlich P, Collet L, Morgon A. (1993). Transient evoked otoacoustic emission amplitudes change with changes of directed attention. Physiol Behav 53: Giraud AL, Collet L, Chery-Croze S, et al. (1995). Evidence of a medial olivocochlear involvement in contralateral suppression of otoacoustic emissions in humans. Brain Res 705: Graham RL, Hazell JW. (1994) Contralateral suppression of transient evoked otoacoustic emissions: intra-individual variability in tinnitus and normal subjects. Br J Audiol 28: Gummer M, Yates GK, Johnstone BM. (1988) Modulation transfer function of efferent neurons in the guinea pig cochlea. Hear Res 36: Hood LJ, Berlin CI, Hurley A, et al. (1996). Contralateral suppression of transient-evoked otoacoustic emissions in humans: intensity effects. Hear Res 101: Kawase T, Delgutte B, Liberman MC. (1993). Antimasking effects of the olivocochlear reflex. II. Enhancement of auditory-nerve response to masked tones. J Neurophysiol 70: Khalfa S, Collet L. (1996). Functional asymmetry of medial olivocochlear system in humans. Towards a peripheral auditory lateralization. Neuroreport 7:

11 Khalfa S, Micheyl C, Veuillet E, Collet, L. (1998). Peripheral auditory lateralization assessment using TEOAEs. Hear Res 121: Kujawa SG, Liberman MC. (1997). Conditioningrelated protection from acoustic injury: effects of chronic deefferentation and sham surgery. J Neurophysiol 78: Kujawa SG, Liberman MC. (1999). Long-term sound conditioning enhances cochlear sensitivity. J Neurophysiol 82: Liberman MC. (1988). Responses properties of cochlear efferent neurons: monaural vs. binaural stimulation and the effects of noise J Neurophysiol 60: Lindgren F, Axelsson A. (1983). Temporary threshold shift after exposure to noise and music of equal energy. Ear Hear 4: Maison S, Durrant J, Gallineau C, et al. (2001). Delay and temporal integration in medial olivocochlear bundle activation in humans. Ear Hear 22: Micheyl C, Collet L. (1995). Involvement of medial olivocochlear system in the detection of tones in noise. J Acoust Soc Am 99: Micheyl C, Carbonnel O, Collet L. (1995a) Medial olivocochlear system and loudness adaption: Differences between musicians and non-musians. Brain Cogn 29: Micheyl C, Morlet T, Giraud AL, et al. (1995b). Contralateral suppression of evoked otoacoustic emissions and detection of a multi-tone complex in noise. Acta Otolaryngol 115: Micheyl C, Khalfa S, Perrot X, Collet L. (1997). Difference in cochlear efferent activity between musicians and non-musicians. Neuroreport 8: Scharf B, Magnan J, Chays A, et al. (1994). On the role of the olivocochlear bundle in hearing: a case study. Hear Res 75: Scharf B, Magnan J, Chays A. (1997). On the role of the olivocochlear bundle in hearing: 16 case studies. Hear Res 103: Swanson SJ, Dengerink HA, Kondrick P, Miller CL. (1987). The influence of subjective factors on temporary threshold shifts after exposure to music and noise of equal energy. Ear Hear 8: Veuillet E, Collet L, Duclaux R. (1991). Effect of contralateral acoustic stimulation on active cochlear micromechanical properties in human subjects: dependence on stimulus variables. J Neurophysiol 65: Veuillet E, Collet L, Morgan A. (1992). Differential effects of ear canal pressure and contralateral acoustic stimulation on evoked otoacoustic emissions in humans. Hear Res 61: Warr WB, Guinan JJ. (1978). Efferent innervation of the organ of Corti: two different systems. Brain Res 173: Warr WB, Guinan JJ, White JS. (1986). Organization of the efferent fibers: the lateral and medial olivocochlear systems. In: Altshculer RA, Hoffman DW, Bobbin RP, eds. Neurobiology of Hearing: The Cochlea. New York: Raven Press, Wen H, Berlin CI, Hood LJ et al. (1993). A program for the quantification and analysis of t r a n s i e n t evoked otoacoustic emissions. Abstr Assoc Res Otolaryngol 16: 102. Williams EA, Brooks GB, Prasher DK. (1994). Effects of olivocochlear bundle section on otoacoustic emissions in humans: efferent effects in comparison with control subjects. Acta Otolaryngol 114: Miller JD, Watson CS, Covell WP. (1963). Deafening effects of noise on the cat. Acta Otolaryngol Suppl 176: Perrot X, Micheyl C, Khalfa S, Collet L. (1999). Stronger bilateral efferent influences on cochlear biomechanical activity in musicians than in non-musicians. Neurosci Lett 262: Quaranta N, Debole S, DiGirolamo S. (2001). Effect of aging on otoacoustic emissions and efferent suppression in humans. Audiology 40: Rajan R. (1991). Protective functions of the efferent pathways to the mammalian cochlea: a review. In: Dancer AL, Salvi RJ, Hamernick RP, eds. Noise Induced Hearing Loss. St. Louis, MO: Mosby, Robertson D, Gummer M. (1985). Physiological and morphological characterization of efferent neurons in the guinea pig cochlea. Hear Res 20: Rouiller EM, Simm GM, Villa AE, et al. (1991). Auditory coticocortical interconnections in the cat: evidence parallel and hierarchical arrangement of the auditory cortical areas. Exp Brain Res 86: