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No Reduction in the 226-Hz Probe Tone Acoustic Reflex Amplitude Following Severe Inner Hair Cell Loss in Chinchillas

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Abstract

The relationship between the middle ear acoustic reflex (AR) and inner hair cell (IHC) loss is currently unknown. Given that IHC are believed to convey nearly all acoustic information to the central auditory nervous system, it has been assumed that loss of IHC would significantly impact the AR. To evaluate this relationship, we assessed the presence and amplitude of the AR in chinchillas before and after treatment with carboplatin, an anticancer drug that reliably and selectively destroys IHC in this species. Baseline measures of hearing sensitivity, including auditory brainstem response (ABR) thresholds and distortion product otoacoustic emissions (DPOAE), were assessed and then re-evaluated following carboplatin treatment. Post-carboplatin ABR thresholds and DPOAE were found to be unchanged or slightly elevated; results were consistent with published reports. Our main hypothesis was that loss of IHC would abolish the reflex or significantly reduce its amplitude. Contrary to our hypothesis, the ipsilateral 226-Hz AR continued to be reliably elicited following carboplatin treatment. Post-mortem histological analysis confirmed significant IHC loss (65–85 %), but no measurable loss of outer hair cells (OHCs). Given that loss of IHC alone does not significantly reduce the 226-Hz AR, our results suggest that few IHC are needed to maintain the 226-Hz AR response. These results suggest additional studies are needed to better understand the role of IHC in the reflex arc, present opportunities to further study the reflex pathway, and could change how we use the clinical AR as a potential diagnostic tool for IHC dysfunction, including those related to IHC synaptopathy.

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Abbreviations

ABR:

Auditory brainstem response

AR:

Acoustic reflex

CANS:

Central auditory nervous system

dB:

Decibel

DPOAE:

Distortion product otoacoustic emissions

HL:

Hearing level

IHCs:

Inner hair cells

MEMR:

Middle ear muscle response

MOC:

Medial olivocochlear

OHCs:

Outer hair cells

SD :

Standard deviation

SEM:

Standard error of the mean

SPL:

Sound pressure level

References

  • Anderson H, Barr B, Wedenberg E (1969) Early diagnosis of 8th-nerve tumours by acoustic reflex tests. Acta Otolaryngol Suppl 263:232–237

    CAS  PubMed  Google Scholar 

  • Arslan HH, Edizer DT, Cebeci S, Erdal M (2014) Diagnostic utility of Stenger test: reappraisal of its value. Int Tinnitus J 19:57–62

    Article  PubMed  Google Scholar 

  • Badri R, Siegel JH, Wright BA (2011) Auditory filter shapes and high-frequency hearing in adults who have impaired speech in noise performance despite clinically normal audiograms. J Acoust Soc Am 129:852–863

    Article  PubMed  PubMed Central  Google Scholar 

  • Bauch CD, Olsen WO, Harner SG (1983) Auditory brain-stem response and acoustic reflex test. Arch Otolaryngol 109:522–525

    Article  CAS  PubMed  Google Scholar 

  • Bennett M (1984) Impedance concepts relating to the acoustic reflex. In: The acoustic reflex. basic principles and clinical applications. (Silman S, ed), pp 35–61. Orlando, FL: Academic Press, Inc

  • Bharadwaj HM, Mai AR, Simpson JM, Choi I, Heinz MG, Shinn-Cunningham BG (2019) Non-invasive assays of cochlear synaptopathy - candidates and considerations. Neuroscience

  • Bohne BA, Kenworthy A, Carr CD (1982) Density of myelinated nerve fibers in the chinchilla cochlea. J Acoust Soc Am 72:102–107

    Article  CAS  PubMed  Google Scholar 

  • Borg E (1971) Efferent inhibition of afferent acoustic activity in the unanesthetized rabbit. Exp Neurol 31:301–312

    Article  CAS  PubMed  Google Scholar 

  • Borg E, Counter SA, Rosler G (1984) Theories of middle-ear muscle functions. In: The acoustic reflex: basic principles and clinical applications. Orlando, FL.: Academic Press, Inc

  • Borg E, Engstrom B (1982) Acoustic reflex after experimental lesions to inner and outer hair cells. Hear Res 6:25–34

    Article  CAS  PubMed  Google Scholar 

  • Borg E, Zakrisson JE (1974) Stapedius reflex and monaural masking. Acta Otolaryngol 78:155–161

    Article  CAS  PubMed  Google Scholar 

  • Callan DE, Lasky RE, Fowler CG (1999) Neural networks applied to retrocochlear diagnosis. Journal of Speech, Language, and Hearing Research : JSLHR 42:287–299

    Article  CAS  PubMed  Google Scholar 

  • Charaziak KK, Shera CA (2017) Compensating for ear-canal acoustics when measuring otoacoustic emissions. J Acoust Soc Am 141:515

    Article  PubMed  PubMed Central  Google Scholar 

  • de Swanepoel W, Werner S, Hugo R, Louw B, Owen R, Swanepoel A (2007) High frequency immittance for neonates: a normative study. Acta Otolaryngol 127:49–56

    Article  PubMed  Google Scholar 

  • El-Badry MM, McFadden SL (2009) Evaluation of inner hair cell and nerve fiber loss as sufficient pathologies underlying auditory neuropathy. Hear Res 255:84–90

    Article  PubMed  PubMed Central  Google Scholar 

  • Emanuel DC, Henson OE, Knapp RR (2012) Survey of audiological immittance practices. Am J Audiol 21:60–75

    Article  PubMed  Google Scholar 

  • Gelfand SA, Schwander T, Silman S (1990) Acoustic reflex thresholds in normal and cochlear-impaired ears: effects of no-response rates on 90th percentiles in a large sample. J Speech Hear Disord 55:198–205

    Article  CAS  PubMed  Google Scholar 

  • Gerhardt KJ, Walton JP (1986) Binaural acoustic reflex activity following monaural noise exposure in decerebrate chinchillas. Audiology : Official Organ of the International Society of Audiology 25:309–320

    Article  CAS  Google Scholar 

  • Guest H, Munro KJ, Plack CJ (2019) Acoustic middle-ear-muscle-reflex thresholds in humans with normal audiograms: no relations to tinnitus, speech perception in noise, or noise exposure. Neuroscience 407:75–82

    Article  CAS  PubMed  Google Scholar 

  • Guest H, Munro KJ, Prendergast G, Millman RE, Plack CJ (2018) Impaired speech perception in noise with a normal audiogram: no evidence for cochlear synaptopathy and no relation to lifetime noise exposure. Hear Res 364:142–151

    Article  PubMed  PubMed Central  Google Scholar 

  • Holte L, Margolis RH, Cavanaugh RM Jr (1991) Developmental changes in multifrequency tympanograms. Audiology : Official Organ of the International Society of Audiology 30:1–24

    Article  CAS  Google Scholar 

  • Hunter LL, Margolis RH (1992) Multifrequency tympanometry: current clinical application. Am J Audiol 1:33–43

    Article  CAS  PubMed  Google Scholar 

  • Hunter LLS, N. (2014) Acoustic immittance measures: basic and advanced practice. Plural Publishing, San Diego, CA

    Google Scholar 

  • Jerger J, Anthony L, Jerger S, Mauldin L (1974) Studies in impedance audiometry. 3. Middle Ear Disorders Archives of Otolaryngology 99:165–171

    Article  CAS  PubMed  Google Scholar 

  • Jerger J, Jerger S, Mauldin L (1972) Studies in impedance audiometry. I. Normal and sensorineural ears. Arch Otolaryngol 96:513–523

    Article  CAS  PubMed  Google Scholar 

  • Jerger S, Jerger J, Hall J (1979) A new acoustic reflex pattern. Arch Otolaryngol 105:24–28

    Article  CAS  PubMed  Google Scholar 

  • Keefe DH, Fitzpatrick D, Liu YW, Sanford CA, Gorga MP (2010) Wideband acoustic-reflex test in a test battery to predict middle-ear dysfunction. Hear Res 263:52–65

    Article  PubMed  Google Scholar 

  • Kiang NY, Rho JM, Northrop CC, Liberman MC, Ryugo DK (1982) Hair-cell innervation by spiral ganglion cells in adult cats. Science 217:175–177

    Article  CAS  PubMed  Google Scholar 

  • Kobler JB, Guinan JJ Jr, Vacher SR, Norris BE (1992) Acoustic reflex frequency selectivity in single stapedius motoneurons of the cat. J Neurophysiol 68:807–817

    Article  CAS  PubMed  Google Scholar 

  • Lobarinas E, Salvi R, Ding D (2013) Insensitivity of the audiogram to carboplatin induced inner hair cell loss in chinchillas. Hear Res 302:113–120

    Article  CAS  PubMed  Google Scholar 

  • Lobarinas E, Salvi R, Ding D (2016) Selective inner hair cell dysfunction in chinchillas impairs hearing-in-noise in the absence of outer hair cell loss. J Assoc Res Otolaryngol 17:89–101

    Article  PubMed  Google Scholar 

  • Lobarinas E, Salvi R, Ding D (2020) Gap detection deficits in chinchillas with selective carboplatin-induced inner hair cell loss. J Assoc Res Otolaryngol

  • Middelweerd MJ, Festen JM, Plomp R (1990) Difficulties with speech intelligibility in noise in spite of a normal pure-tone audiogram. Audiology : Official Organ of the International Society of Audiology 29:1–7

    Article  CAS  Google Scholar 

  • Moller AR (1974a) Responses of units in the cochlear nucleus to sinusoidally amplitude-modulated tones. Exp Neurol 45:105–117

    Article  CAS  PubMed  Google Scholar 

  • Moller AR (1974b) The acoustic middle ear muscle reflex. Springer, Verlag, Berlin

    Book  Google Scholar 

  • Moller AR (1984) Neurophysiological basis of the acoustic middle-ear reflex. In: The acoustic reflex: basic principles and clinical applications. (Silman S, ed). Orlando, FL: Academic Press, Inc

  • Mukerji S, Windsor AM, Lee DJ (2010) Auditory brainstem circuits that mediate the middle ear muscle reflex. Trends Amplif 14:170–191

    Article  PubMed  PubMed Central  Google Scholar 

  • Muller M, Hoidis S, Smolders JW (2010) A physiological frequency-position map of the chinchilla cochlea. Hear Res 268:184–193

    Article  PubMed  Google Scholar 

  • Olsen WO, Noffsinger D, Kurdziel S (1975) Acoustic reflex and reflex decay. Occurrence in patients with cochlear and eighth nerve lesions. Arch Otolaryngol 101:622–625

    Article  CAS  PubMed  Google Scholar 

  • Pawlowski K, Koulich E, Wright CG, Roland P (2013) Ototopic applications of povidone iodine/dexamethasone in the rat. Otology & neurotology : official publication of the American Otological Society, American Neurotology Society [and] European Academy of Otology and Neurotology 34:167–174

  • Plack CJ, Barker D, Prendergast G (2014) Perceptual consequences of “hidden” hearing loss. Trends in Hearing 18

  • Prasher D, Cohen M (1993) Effectiveness of acoustic reflex threshold criteria in the diagnosis of retrocochlear pathology. Scand Audiol 22:11–18

    Article  CAS  PubMed  Google Scholar 

  • Qiu C, Salvi R, Ding D, Burkard R (2000) Inner hair cell loss leads to enhanced response amplitudes in auditory cortex of unanesthetized chinchillas: evidence for increased system gain. Hear Res 139:153–171

    Article  CAS  PubMed  Google Scholar 

  • Rosowski JJ, Ravicz ME, Songer JE (2006) Structures that contribute to middle-ear admittance in chinchilla. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 192:1287–1311

    Article  PubMed  PubMed Central  Google Scholar 

  • Salvi R, Sun W, Ding D, Chen GD, Lobarinas E, Wang J, Radziwon K, Auerbach BD (2016) Inner hair cell loss disrupts hearing and cochlear function leading to sensory deprivation and enhanced central auditory gain. Front Neurosci 10:621

    PubMed  Google Scholar 

  • Salvi RJ, Ding D, Wang J, Jiang HY (2000b) A review of the effects of selective inner hair cell lesions on distortion product otoacoustic emissions, cochlear function and auditory evoked potentials. Noise Health 2:9–26

    PubMed  Google Scholar 

  • Salvi RJ, Wang J, Ding D (2000a) Auditory plasticity and hyperactivity following cochlear damage. Hear Res 147:261–274

    Article  CAS  PubMed  Google Scholar 

  • Shaffer LA, Withnell RH, Dhar S, Lilly DJ, Goodman SS, Harmon KM (2003) Sources and mechanisms of DPOAE generation: implications for the prediction of auditory sensitivity. Ear Hear 24:367–379

    Article  PubMed  Google Scholar 

  • Silman S, Gelfand SA (1981) The relationship between magnitude of hearing loss and acoustic reflex threshold levels. J Speech Hear Disord 46:312–316

    Article  CAS  PubMed  Google Scholar 

  • Takeno S, Harrison RV, Mount RJ, Wake M, Harada Y (1994) Induction of selective inner hair cell damage by carboplatin. Scanning Microsc 8:97–106

    CAS  PubMed  Google Scholar 

  • Trautwein P, Hofstetter P, Wang J, Salvi R, Nostrant A (1996) Selective inner hair cell loss does not alter distortion product otoacoustic emissions. Hear Res 96:71–82

    Article  CAS  PubMed  Google Scholar 

  • Trevino M, Lobarinas E, Maulden AC, Heinz MG (2019) The chinchilla animal model for hearing science and noise-induced hearing loss. J Acoust Soc Am 146:3710

    Article  PubMed  PubMed Central  Google Scholar 

  • Uhles ML, Clark WW, Anch M (2000) Effects of alcohol on the acoustic reflex threshold in the chinchilla. Acta Otolaryngol 120:523–528

    Article  CAS  PubMed  Google Scholar 

  • Valero MD, Hancock KE, Liberman MC (2016) The middle ear muscle reflex in the diagnosis of cochlear neuropathy. Hear Res 332:29–38

    Article  PubMed  Google Scholar 

  • Valero MD, Hancock KE, Maison SF, Liberman MC (2018) Effects of cochlear synaptopathy on middle-ear muscle reflexes in unanesthetized mice. Hear Res 363:109–118

    Article  PubMed  PubMed Central  Google Scholar 

  • Vrettakos PA, Dear SP, Saunders JC (1988) Middle ear structure in the chinchilla: a quantitative study. Am J Otolaryngol 9:58–67

    Article  CAS  PubMed  Google Scholar 

  • Wake M, Anderson J, Takeno S, Mount RJ, Harrison RV (1996) Otoacoustic emission amplification after inner hair cell damage. Acta Otolaryngol 116:374–381

    Article  CAS  PubMed  Google Scholar 

  • Wake M, Takeno S, Ibrahim D, Harrison R (1994) Selective inner hair cell ototoxicity induced by carboplatin. Laryngoscope 104:488–493

    Article  CAS  PubMed  Google Scholar 

  • Wang X, Gan RZ (2016) 3D finite element model of the chinchilla ear for characterizing middle ear functions. Biomech Model Mechanobiol 15:1263–1277

    Article  PubMed  PubMed Central  Google Scholar 

  • Wersinger E, Fuchs PA (2011) Modulation of hair cell efferents. Hear Res 279:1–12

    Article  PubMed  Google Scholar 

  • Wojtczak M, Beim JA, Oxenham AJ (2017) Weak middle-ear-muscle reflex in humans with noise-induced tinnitus and normal hearing may reflect cochlear synaptopathy. eNeuro 4

  • Woodford CM, Henderson D, Hamernik RP, Feldman AS (1976) Acoustic reflex threshold of the chinchilla as a function of stimulus duration and frequency. J Acoust Soc Am 59:1204–1207

    Article  CAS  PubMed  Google Scholar 

  • Zhang KD, Coate TM (2017) Recent advances in the development and function of type II spiral ganglion neurons in the mammalian inner ear. Semin Cell Dev Biol 65:80–87

    Article  PubMed  Google Scholar 

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Funding

Research reported in this manuscript was supported by the NIDCD of the National Institutes of Health under award number R01DC014088.

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Authors and Affiliations

  1. School of Behavioral and Brain Sciences, The University of Texas at Dallas, Richardson, TX, USA

    Monica Trevino, Celia Escabi, Hannah Swanner, Karen Pawlowski & Edward Lobarinas

  2. Callier Center for Communication Disorders, The University of Texas at Dallas, 1966 Inwood Road, Dallas, TX, 75235, USA

    Edward Lobarinas

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  1. Monica Trevino
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  2. Celia Escabi
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  3. Hannah Swanner
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  4. Karen Pawlowski
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  5. Edward Lobarinas
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All authors contributed to data collection and writing of the manuscript.

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Correspondence to Edward Lobarinas.

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Trevino, M., Escabi, C., Swanner, H. et al. No Reduction in the 226-Hz Probe Tone Acoustic Reflex Amplitude Following Severe Inner Hair Cell Loss in Chinchillas. JARO 23, 593–602 (2022). https://doi.org/10.1007/s10162-022-00861-3

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