|Year : 2017 | Volume
| Issue : 2 | Page : 89-93
Test-retest reliability of contralateral suppression of acoustic middle ear muscle reflex
Sandeep Maruthy, G Nike Gnanateja, M Shamantha, M Nayana
Department of Audiology, All India Institute of Speech and Hearing, Mysuru, Karnataka, India
|Date of Web Publication||14-Jun-2017|
G Nike Gnanateja
Department of Audiology, All India Institute of Speech and Hearing, Mysore - 570 006, Karnataka
Source of Support: None, Conflict of Interest: None
Background and Objective: The role of efferent system in auditory perception is very important. To assess this, a reliable measure of efferent functioning is necessary. The efferent suppression of otoacoustic emission lacks good test-retest reliability, and there is a need to look for the reliability of other measures of efferent auditory functioning. The current study evaluated the test-retest reliability of contralateral suppression of acoustically evoked middle ear muscle reflexes (MEMR). Method: Nineteen normal hearing adults in the age range of 18–24 years participated in the study. A Repeated measures design was used to establish the reliability of the contralateral suppression of MEMR. Measurements were spaced 1 h and 1 day apart. Results: The results showed acceptable test-retest reliability of contralateral suppression of acoustically evoked MEMR in terms of its Cronbach's alpha. However, inspection of the individual data did not support the impression to call it a reliable tool to assess efferent auditory functioning. The findings of the study are discussed in light of its clinical utility. Conclusion: Contralateral suppression of acoustically evoked MEMR has questionable reliability to be used as a clinical tool.
Keywords: Efferent suppression, middle ear muscle reflexes, test-retest reliability
|How to cite this article:|
Maruthy S, Gnanateja G N, Shamantha M, Nayana M. Test-retest reliability of contralateral suppression of acoustic middle ear muscle reflex. Indian J Otol 2017;23:89-93
|How to cite this URL:|
Maruthy S, Gnanateja G N, Shamantha M, Nayana M. Test-retest reliability of contralateral suppression of acoustic middle ear muscle reflex. Indian J Otol [serial online] 2017 [cited 2020 Jan 24];23:89-93. Available from: http://www.indianjotol.org/text.asp?2017/23/2/89/208017
| Introduction|| |
The efferent auditory neurons, like any other efferent pathways, have inhibitory influence on the afferent auditory pathway. Of the three efferent auditory pathways that have been described; olivocochlear bundle (OCB),,,,,,, corticofugal pathway ,,,,,,, and the corticocortical pathways,,, the role of OCB has been more clearly understood. OCB that originates from the superior olivary complex is divided into medial olivocochlear (MOC) and lateral olivocochlear (LOC) efferent bundles.,, The medial and the lateral efferent auditory pathways, between the brainstem and the cochlea, have been shown to modify the auditory input before it reaches the brain., Of the two, the MOC neurons are myelinated and terminate mostly at outer hair cells, and their role has been documented using contralateral suppression of otoacoustic emissions (CSOAE).
Certain functions have been attributed to the MOC system, based on both human and animal research, which include localization of sound source,,, auditory attention,, protection of cochlea against acoustic injury, improved detection of acoustic signals in the presence of noise,, and improved speech perception in noise.,, It has been shown using various approaches ,,,, that acoustic stimulation of one cochlea modifies afferent fiber responses in the contralateral cochlea. Berlin et al. reported frequency-specific decrease in otoacoustic emissions (OAEs), in the presence of contralateral acoustic stimulation, attributable to the MOC system.
In the last decade, the mechanisms underlying auditory processing disorders in various developmental disorders such as autism, learning disability, and auditory neuropathy spectrum disorders  have been found to be closely linked to the efferent auditory system. As a result, clinicians have realized the need for assessing the efferent auditory system in the diagnostic audiological evaluation. Among various techniques, CSOAE has been the most frequently used and investigated tool for the purpose.
Contralateral suppression of both transient evoked OAEs and distortion product OAEs (DPOAEs) have been attempted., In both of them, suppression magnitude ranges between 1 and 3 dB  and is primarily in the region of 1–3 kHz. The efferent-mediated changes are also reported to be frequency specific. The reduction or absence of suppression magnitude is used as a clinical sign of the damaged or dysfunctional efferent auditory neurons.
Although studies considering the group data show a clear difference between normal and disordered population, for CSOAEs to be proved as a good clinical tool, it should possess good test-retest reliability among other diagnostically relevant features such as sensitivity and specificity. Kumar et al. measured contralateral suppression of DPOAEs in the right ear of 24 adult male participants. Both intra- and inter-session, reliability was assessed in the study. The intra-session reliability was assessed by repeating the contralateral suppression of DPOAEs without altering the position of the DPOAE probe (single-probe-fit), whereas, the intersession reliability was assessed through repeated measurements on 8 different days (multiple-probe-fit). Reliability of inhibition of DPOAE magnitudes was evaluated by Cronbach's alpha, interclass correlations, standard error of measurement and its 95% confidence interval and smallest detectable difference. Results showed that the test/retest reliability coefficients of DPOAE inhibition magnitudes were less than satisfactory for all the frequencies, in both single-probe-fit and multiple-probe-fit modes. Therefore, although CSOAE is a quick, noninvasive estimate of the efferent auditory function, its poor reliability suggests that it should not be used clinically.
Furthermore, evaluating the medial efferent system using CSOAE warrants normal cochlear functioning and cannot be used in individuals with even a mild degree of hearing loss. In such instances, there is a need for a test of the efferent functioning which is more resistant to the effects of hearing loss and has good test-retest reliability. There is very sparse literature on the evaluation of efferent functioning using the contralateral suppression of middle ear muscle reflexes (MEMR)., Kumar and Barman  showed evidence that MEMRs can be used for assessing the functioning of efferent auditory system. Unlike CSOAE, the efferent-induced suppression of the MEMR reflex might be mediated by both efferent neurons originating in the medial as well as lateral olivary complexes. In addition, the MEMRs are resistant up to 60 dB of sensorineural hearing loss and therefore have application in broader clinical population than that with OAEs. However, its test-retest reliability has not been examined till date. If proven to be reliable, in future, contralateral suppression of MEMRs shall replace the suppression of OAEs in being an objective index of efferent auditory functioning.
The objective of the present study is to assess the test-retest reliability of contralateral suppression of MEMR and in turn to assess if it is a feasible clinical tool for the assessment of efferent auditory functioning.
| Methods|| |
Nineteen normal hearing adults in the age range of 18–24 years participated in the study. Normal hearing was ensured on pure tone audiometry, and all of them had hearing thresholds within 15 dB HL at octave frequencies between 250 and 8000 Hz. All the participants had Type-A tympanogram, and had acoustic reflexes present bilaterally which indicated normal middle ear function. They did not have any complaint/history of relevant neurological and otological dysfunctions. Perception of bisyllabic phonemically balanced words in the presence of speech noise at 0 dB SNR was above 60% in all the participants. The participants were either bachelors or masters students of speech and hearing and geographically from different parts of the country. After completely explaining the objectives and the testing procedure, a written consent was taken from all of them before their participation. All the procedures used were approved by the Institutional Ethical Guidelines and conformed to the Declaration of Helsinki.
After ensuring that all the participants met the necessary qualifications, the contralateral suppression of MEMRs was measured in them. The test procedure involved, recording of ipsilateral MEMR threshold in two conditions; without and with contralateral broadband noise (BBN). Acoustic reflexes were measured using a calibrated GSI-TympStar middle ear analyzer while the BBN presented from a calibrated Piano plus audiometer. Audiological assessment was carried out in a sound-treated room without ambient noise levels as per the ANSI guidelines. [Figure 1] shows the illustration of the apparatus used.
|Figure 1: Illustration of the apparatus used for measuring the contralateral suppression of acoustic reflexes|
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The participants were positioned in a comfortable chair. They were instructed to avoid head movements, swallowing, and speaking during the testing. Before starting the actual measurements, probe assembly of the immittance meter was inserted into the right ear while the insert receiver of the audiometer was inserted into the left ear. In each of them, ipsilateral MEMRs were measured at 500, 1000, and 2000 Hz in intensity steps of 5 dB to track the acoustic reflex thresholds. Reflex threshold was defined as the minimum intensity in dB HL at which repeatable acoustic reflex of amplitude 0.03 ml is obtained. Initially, the thresholds were measured in the absence of contralateral BBN and were designated as baseline thresholds. The acoustic reflex thresholds were always recorded from the right ear.
Efferent suppression was triggered by presenting BBN to the contralateral ear (invariably the left ear) through insert receiver of the Piano plus audiometer. The noise was continuously presented to the contralateral ear at 40 dB SL (ref: Threshold of BBN). The thresholds thus obtained were designated as suppression thresholds. The baseline thresholds and suppression thresholds were then compared as below to infer on the efferent inhibition.
Suppression of MEMR = Baseline thresholds − Suppression thresholds
The measurement of baseline thresholds and the suppression thresholds was repeated after 1 h and after 1 day, i.e., the thresholds were totally measured on three occasions. The test-retest reliability of contralateral suppression of MEMRs was determined by statistically comparing the difference in thresholds between the two conditions, across the three sessions. A schematic block diagram of the test procedure is shown in [Figure 2]. All the procedures used are noninvasive and are cleared by the Institutional Ethical Review Board.
| Results|| |
The mean and standard deviation of the baseline thresholds and suppression thresholds are shown in [Table 1]. The mean data showed that the MEMR thresholds were elevated in the presence of contralateral noise. This was true in all three recording sessions and for all three frequencies. The individual elevation in the thresholds ranged from 2.5 to 4.5 dB. On comparing thresholds across sessions, there was negligible difference in the mean thresholds at 500 and 1 kHz while there was a difference of up to 4 dB at 2 kHz.
|Table 1: Mean and standard deviation of the acoustic middle ear muscle reflexes in baseline, in the presence of |
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The effect of condition (baseline vs. with contralateral noise) on thresholds along with the effect of session was statistically verified using 2 × 3 repeated measures ANOVA. Results showed a significant main effect of condition (F(3,13) = 9.767, P= 0.001) on the MEMR thresholds. However, there was no main effect of session on the MEMR thresholds (F(3,13) = 0.652, P= 0.689), and there was no significant interaction between condition and sessions.
The across session comparison of contralateral suppression of MEMRs being the primary objective of the study, the data were further tested for reliability. The magnitude of suppression was used for this purpose. The magnitude of suppression was derived by subtracting suppression thresholds from baseline thresholds. The Mean and standard deviation of the magnitude of suppression, in the three sessions, for the three frequencies is given in [Table 1]. The mean suppression was more in Session 3 compared to Session 1 and 2.
The magnitude of suppression was tested for its test-retest reliability on intraclass correlation. [Figure 3] shows the MEMR suppression magnitude among the three sessions. The standardized Cronbach's alpha was 0.5750 at 500 Hz, 0.5817 at 1000 Hz, and 0.0219 at 2000 Hz.
|Figure 3: Plots showing the variations of acoustic reflex suppression magnitude across sessions in individual participants|
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| Discussion|| |
The results of the present study showed elevated MEMR thresholds in the presence of contralateral noise. Considering that the contralateral noise was presented at 40 dB SL in normal hearing individuals, elevated thresholds cannot be attributed to any other physiological mechanism but for the participation of efferent auditory system. The contralateral noise would have triggered the efferent auditory system which in turn would have inhibited the afferent auditory neurons, thereby elevating the acoustic reflex thresholds. Kumar and Barman  attributed the suppression of acoustic reflex thresholds to efferent-induced mechanical inhibition of basilar membrane motion  and change in the firing of auditory nerve fibers by an electrical effect.
Although efferent-induced contralateral suppression can be studied either through OAEs or acoustic reflexes, acoustic reflexes have an advantage over OAEs as they can be recorded even in individuals with cochlear hearing loss (up-to moderate-severe degree). Further, CSOAEs were found to be not reliable on intra class correlation by Kumar et al. Therefore in the present study, contralateral suppression was assessed for its test-retest reliability. Results showed that there was an acceptable reliability of contralateral suppression of MEMRs at 500 Hz and 1 kHz. However, it was not reliable at 2 kHz. Therefore, it can be inferred that contralateral suppression of acoustic reflexes can be used to reliably document the functioning of the efferent auditory system. However, one should only use reflexes elicited by 500 Hz and 1 kHz pure tones. The exact reason for the lower reliability at 2 kHz is not clear. One could speculate that it is linked to the adaptation of auditory neurons. Adaptation of auditory neurons is known to be greater at higher frequencies, and probably, this could have contributed to the lower reliability of contralateral suppression of MEMRs at 2 kHz.
For any test to qualify as a clinically useful one, apart from its reliability, it should be present in most of the normal individuals, i.e., if contralateral suppression is to be designated as a good test for assessing efferent auditory inhibition, it should show suppression in majority of the individuals. A close analysis of [Figure 3] shows that contralateral suppression of MEMRs was absent in a considerable number of participants. This was true for all three sessions and all three frequencies. This feature makes it difficult to differentiate between normal and efferent damaged individuals based on contralateral suppression of MEMRs. Therefore, although it possesses good reliability, the authenticity of using contralateral suppression of MEMRs for clinical use to identify efferent damage is questionable due to its low prevalence.
However, one is cautioned about the generalization of the conclusion. The present study considered only acoustic reflex thresholds while assessing the reliability of the contralateral suppression of MEMRs that too thresholds tracked in 5 dB steps. These findings may not hold good if the thresholds are tracked in 1 or 2 dB steps and if suprathreshold (Ref: Acoustic reflex threshold) reflex amplitude is considered as the response parameter. Therefore, based on the present findings, it can be concluded that contralateral suppression of acoustic reflexes is not advisable as a clinical tool for efferent inhibition, if reflex threshold is considered as the response parameter.
| Conclusions|| |
The stimulation of the auditory system leads to elevation of MEMR thresholds at 500, 1000, and 2000 Hz. The threshold elevation attributable to efferent suppression has poor test-retest reliability and therefore is not very efficient as a clinical tool. However, on comparing the reliability of CSOAEs as reported by Kumar et al. (2013), the reliability of contralateral suppression of MEMRs is better and therefore suggests the use of contralateral suppression of MEMRs as against contralateral suppression of OAEs in evaluating the auditory efferent system. However, the suppression obtained in the MEMR is not a reliable estimate and has limited usefulness in assessing efferent auditory functioning in the clinic. We still need more systematically analyzed strong tools for assessing efferent auditory function in humans.
Contralateral suppression of acoustic MEMR threshold has limited usefulness and reliability in assessing efferent auditory functioning in humans.
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Conflicts of interest
There are no conflicts of interest.
| References|| |
Berlin CI, Hood LJ, Wen H, Szabo P, Cecola RP, Rigby P, et al.
Contralateral suppression of non-linear click-evoked otoacoustic emissions. Hear Res 1993;71:1-11.
Kawase T, Ogura M, Hidaka H, Sasaki N, Suzuki Y, Takasaka T. Effects of contralateral noise on measurement of the psychophysical tuning curve. Hear Res 2000;142:63-70.
Kumar UA, Vanaja CS. Functioning of olivocochlear bundle and speech perception in noise. Ear Hear 2004;25:142-6.
Ameenuddin M, Maruthy S. Effect of Music on Neural Plasticity of Efferent Auditory System. Dissertation Submitted to the University of Mysore, Mysore; 2010.
Mishra SK, Lutman ME. Top-down influences of the medial olivocochlear efferent system in speech perception in noise. PLoS One 2014;9:e85756.
Guinan JJ Jr. Olivocochlear efferents: Anatomy, physiology, function, and the measurement of efferent effects in humans. Ear Hear 2006;27:589-607.
Guinan JJ. The physiology of olivocochlear efferents. In: Dallos PJ, Popper AN, Fay RR, editors. The Cochlea. New York: Springer-Verlag; 1996. p. 435-502.
Suga N, Gao E, Zhang Y, Ma X, Olsen JF. The corticofugal system for hearing: Recent progress. Proc Natl Acad Sci U S A 2000;97:11807-14.
Yan W, Suga N. Corticofugal modulation of the midbrain frequency map in the bat auditory system. Nat Neurosci 1998;1:54-8.
Liu X, Yan Y, Wang Y, Yan J. Corticofugal modulation of initial neural processing of sound information from the ipsilateral ear in the mouse. PLoS One 2010;5:e14038.
Luo F, Wang Q, Kashani A, Yan J. Corticofugal modulation of initial sound processing in the brain. J Neurosci 2008;28:11615-21.
Chandrasekaran B, Hornickel J, Skoe E, Nicol T, Kraus N. Context-dependent encoding in the human auditory brainstem relates to hearing speech in noise: Implications for developmental dyslexia. Neuron 2009;64:311-9.
Parbery-Clark A, Strait DL, Kraus N. Context-dependent encoding in the auditory brainstem subserves enhanced speech-in-noise perception in musicians. Neuropsychologia 2011;49:3338-45.
Gnanateja GN, Ranjan R, Firdose H, Sinha SK, Maruthy S. Acoustic basis of context dependent brainstem encoding of speech. Hear Res 2013;304:28-32.
Strait DL, Hornickel J, Kraus N. Subcortical processing of speech regularities underlies reading and music aptitude in children. Behav Brain Funct 2011;7:44.
Suga N, Xiao Z, Ma X, Ji W. Plasticity and corticofugal modulation for hearing in adult animals. Neuron 2002;36:9-18.
Suga N. Tuning shifts of the auditory system by corticocortical and corticofugal projections and conditioning. Neurosci Biobehav Rev 2012;36:969-88.
Rasmussen GL. The olivary peduncle and other fiber projections of the superior olivary complex. J Comp Neurol 1946;84:141-219.
Warr WB, Guinan JJ Jr. Efferent innervation of the organ of corti: Two separate systems. Brain Res 1979;173:152-5.
Warr WB. Olivocochlear and vestibular efferent neurons of the feline brain stem: Their location, morphology and number determined by retrograde axonal transport and acetylcholinesterase histochemistry. J Comp Neurol 1975;161:159-81.
Andéol G, Guillaume A, Micheyl C, Savel S, Pellieux L, Moulin A. Auditory efferents facilitate sound localization in noise in humans. J Neurosci 2011;31:6759-63.
May BJ, Budelis J, Niparko JK. Behavioral studies of the olivocochlear efferent system: Learning to listen in noise. Arch Otolaryngol Head Neck Surg 2004;130:660-4.
Reiss LA, Ramachandran R, May BJ. Effects of signal level and background noise on spectral representations in the auditory nerve of the domestic cat. J Assoc Res Otolaryngol 2011;12:71-88.
de Boer J, Thornton AR. Neural correlates of perceptual learning in the auditory brainstem: Efferent activity predicts and reflects improvement at a speech-in-noise discrimination task. J Neurosci 2008;28:4929-37.
Giard MH, Collet L, Bouchet P, Pernier J. Auditory selective attention in the human cochlea. Brain Res 1994;633:353-6.
Reiter ER, Liberman MC. Efferent-mediated protection from acoustic overexposure: Relation to slow effects of olivocochlear stimulation. J Neurophysiol 1995;73:506-14.
Micheyl C, Collet L. Involvement of the olivocochlear bundle in the detection of tones in noise. J Acoust Soc Am 1996;99:1604-10.
Giraud AL, Wable J, Chays A, Collet L, Chéry-Croze S. Influence of contralateral noise on distortion product latency in humans: Is the medial olivocochlear efferent system involved? J Acoust Soc Am 1997;102:2219-27.
Kumar A, Barman A. Effect of efferent-induced changes on acoustical reflex. Int J Audiol 2002;41:144-7.
Vinay, Moore BC. Effects of activation of the efferent system on psychophysical tuning curves as a function of signal frequency. Hear Res 2008;240:93-101.
Warren EH 3rd
, Liberman MC. Effects of contralateral sound on auditory-nerve responses. I. Contributions of cochlear efferents. Hear Res 1989;37:89-104.
Warren EH 3rd
, Liberman MC. Effects of contralateral sound on auditory-nerve responses. II. Dependence on stimulus variables. Hear Res 1989;37:105-21.
Khalfa S, Bruneau N, Rogé B, Georgieff N, Veuillet E, Adrien JL, et al.
Peripheral auditory asymmetry in infantile autism. Eur J Neurosci 2001;13:628-32.
Garinis AC, Glattke T, Cone-Wesson BK. TEOAE suppression in adults with learning disabilities. Int J Audiol 2008;47:607-14.
Hood LJ, Berlin CI, Bordelon J, Rose K. Patients with auditory neuropathy/dys-synchrony lack efferent suppression of transient evoked otoacoustic emissions. J Am Acad Audiol 2003;14:302-13.
Kujawa SG, Liberman MC. Effects of olivocochlear feedback on distortion product otoacoustic emissions in guinea pig. J Assoc Res Otolaryngol 2001;2:268-78.
Kumar UA, Methi R, Avinash MC. Test/retest repeatability of effect contralateral acoustic stimulation on the magnitudes of distortion product ototacoustic emissions. Laryngoscope 2013;123:463-71.
Higson JM, Morgan N, Stephenson H, Haggard MP. Auditory performance and acoustic reflexes in young adults reporting listening difficulties. Br J Audiol 1996;30:381-7.
Frank T. ANSI update: Maximum permissible ambient noise levels for audiometric test rooms. Am J Audiol 2000;9:3-8.
Nuttall AL, Dolan DF. Comment on “Modulation of the hair cell motor: A possible source of odd-order distortion” [J. Acoust. Soc. Am 96, 2210-2215 (1994)]. J Acoust Soc Am 1994;96:2583-4.
Guinan JJ Jr., Gifford ML. Effects of electrical stimulation of efferent olivocochlear neurons on cat auditory-nerve fibers. III. Tuning curves and thresholds at CF. Hear Res 1988;37:29-45.
Javel E. Long-term adaptation in cat auditory-nerve fiber responses. J Acoust Soc Am 1996;99:1040-52.
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