The Origin Along the Cochlea of Otoacoustic Emissions Evoked by Mid-Frequency Tone Pips.

Auditory nerve compound action potential CEOAE Click-evoked otoacoustic emissions Cochlear amplifier TEOAE Transient-evoked otoacoustic emissions

Journal

Journal of the Association for Research in Otolaryngology : JARO
ISSN: 1438-7573
Titre abrégé: J Assoc Res Otolaryngol
Pays: United States
ID NLM: 100892857

Informations de publication

Date de publication:
27 Jun 2024
Historique:
received: 14 07 2023
accepted: 12 06 2024
medline: 28 6 2024
pubmed: 28 6 2024
entrez: 27 6 2024
Statut: aheadofprint

Résumé

Tone-pip-evoked otoacoustic emissions (PEOAEs) are transient-evoked otoacoustic emissions (OAEs) that are hypothesized to originate from reflection of energy near the best-frequency (BF) cochlear place of the stimulus frequency. However, individual PEOAEs have energy with a wide range of delays. We sought to determine whether some PEOAE energy is consistent with having been generated far from BF. PEOAEs from 35 and 47 dB SPL tone pips were obtained by removing pip-stimulus energy by subtracting the ear-canal sound pressure from scaled-down 59 dB SPL tone pips (which evoke relatively small OAEs). PEOAE delays were measured at each peak in the PEOAE absolute-value waveforms. While measuring PEOAEs and auditory-nerve compound action potentials (CAPs), amplification was blocked sequentially from apex to base by cochlear salicylate perfusion. The perfusion time when a CAP was reduced identified when the perfusion reached the tone-pip BF place. The perfusion times when each PEOAE peak was reduced identified where along the cochlea it received cochlear amplification. PEOAEs and CAPs were measured simultaneously using one pip frequency in each ear (1.4 to 4 kHz across 16 ears). Most PEOAE peaks received amplification primarily between the BF place and 1-2 octaves basal of the BF place. PEOAE peaks with short delays received amplification basal of BF place. PEOAE peaks with longer delays sometimes received amplification apical of BF place, consistent with previous stimulus-frequency-OAE results. PEOAEs provide information about cochlear amplification primarily within ~ 1.5 octave of the tone-pip BF place, not about regions > 3 octaves basal of BF.

Identifiants

pubmed: 38937327
doi: 10.1007/s10162-024-00955-0
pii: 10.1007/s10162-024-00955-0
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : NIDCD NIH HHS
ID : R01 DC014997
Pays : United States

Informations de copyright

© 2024. The Author(s) under exclusive licence to Association for Research in Otolaryngology.

Références

Abdala C, Ortmann AJ, Shera CA (2018) Reflection- and distortion-source otoacoustic emissions: evidence for increased irregularity in the human cochlea during aging. Journal of the Association for Reseach in Otolaryngology 5:493–510
doi: 10.1007/s10162-018-0680-x
Stiepan S, Shera CA, Abdala C (2023) Characterizing a joint reflection-distortion OAE profile in humans with endolymphatic hydrops. Ear Hear 44(6):1437–1450
pubmed: 37450653 doi: 10.1097/AUD.0000000000001387
Guinan JJ Jr et al (2021) Altered mapping of sound frequency to cochlear place in ears with endolymphatic hydrops provide insight into the pitch anomaly of diplacusis. Sci Rep 11(1):10380
pubmed: 34001971 pmcid: 8128888 doi: 10.1038/s41598-021-89902-0
Lee C et al (2020) Early detection of endolymphatic hydrops using the auditory nerve overlapped waveform (ANOW). Neuroscience 425:251–266
pubmed: 31809731 doi: 10.1016/j.neuroscience.2019.11.004
Lefler SM et al (2021) Measurements from ears with endolymphatic hydrops and 2-Hydroxypropyl-beta-cyclodextrin provide evidence that loudness recruitment can have a cochlear origin. Front Surg 8:687490
pubmed: 34676239 pmcid: 8523923 doi: 10.3389/fsurg.2021.687490
Valenzuela CV et al (2020) Is cochlear synapse loss an origin of low-frequency hearing loss associated with endolymphatic hydrops? Hear Res 398:108099
pubmed: 33125982 pmcid: 9058942 doi: 10.1016/j.heares.2020.108099
Abdala C, Kalluri R (2017) Towards a joint reflection-distortion otoacoustic emission profile: results in normal and impaired ears. J Acoust Soc Am 142(2):812
pubmed: 28863614 pmcid: 5552396 doi: 10.1121/1.4996859
Mertes IB, Marquess A (2023) A survey of U.S. audiologists’ usage of and attitudes toward otoacoustic emissions. Am J Audiol 32(2):417–431
pubmed: 37099746 doi: 10.1044/2023_AJA-22-00096
Goodman SS, Fitzpatrick DF, Ellison JC, Jesteadt W, Keefe DH (2009) High-frequency click-evoked otoacoustic emissions and behavioral thresholds in humans. J Acoust Soc Am 125(2):1014–1032
pubmed: 19206876 pmcid: 2659524 doi: 10.1121/1.3056566
Lewis JD, Goodman SS (2014) The effect of stimulus bandwidth on the nonlinear-derived tone-burst-evoked otoacoustic emission. J Assoc Res Otolaryngol 15(6):915–31
pubmed: 25245497 pmcid: 4389961 doi: 10.1007/s10162-014-0484-6
Francis NA, Guinan JJ Jr (2010) Acoustic stimulation of human medial olivocochlear efferents reduces stimulus-frequency and click-evoked otoacoustic emission delays: Implications for cochlear filter bandwidths. Hear Res 267(1–2):36–45
pubmed: 20430088 pmcid: 2918271 doi: 10.1016/j.heares.2010.04.009
Charaziak KK, Siegel JH (2015) Tuning of SFOAEs evoked by low-frequency tones is not compatible with localized emission generation. Jaro-Journal of the Association for Research in Otolaryngology 16(3):317–329
pmcid: 4417092 doi: 10.1007/s10162-015-0513-0
Charaziak KK, Siegel JH (2014) Estimating cochlear frequency selectivity with stimulus-frequency otoacoustic emissions in chinchillas. Jaro-Journal of the Association for Research in Otolaryngology 15(6):883–896
pmcid: 4389964 doi: 10.1007/s10162-014-0487-3
Christensen AT, Abdala C, Shera CA (2020) A cochlea with three parts? Evidence from otoacoustic emission phase in humans. J Acoust Soc Am 148(3):1585
pubmed: 33003861 pmcid: 7789857 doi: 10.1121/10.0001920
Recio-Spinoso A, Oghalai JS (2017) Mechanical tuning and amplification within the apex of the guinea pig cochlea. J Physiol 595(13):4549–4561
pubmed: 28382742 pmcid: 5491880 doi: 10.1113/JP273881
Shera CA, Guinan JJ Jr, Oxenham AJ (2010) Otoacoustic estimation of cochlear tuning: validation in the chinchilla. J Assoc Res Otolaryngol 11(3):343–365
pubmed: 20440634 pmcid: 2914235 doi: 10.1007/s10162-010-0217-4
Temchin AN, Rich NC, Ruggero MA (2008) Threshold tuning curves of chinchilla auditory-nerve fibers. I. Dependence on characteristic frequency and relation to the magnitudes of cochlear vibrations. J Neurophysiol 100(5):2889–2898
pubmed: 18701751 pmcid: 2585409 doi: 10.1152/jn.90637.2008
Goodman SS et al (2020) The spatial origins of cochlear amplification assessed by stimulus-frequency otoacoustic emissions. Biophys J 118(5):1183–1195
pubmed: 31968228 pmcid: 7063421 doi: 10.1016/j.bpj.2019.12.031
Kalluri R, Shera CA (2007) Near equivalence of human click-evoked and stimulus-frequency otoacoustic emissions. J Acoust Soc Am 121(4):2097–2110
pubmed: 17471725 doi: 10.1121/1.2435981
Shera CA, Guinan JJ Jr (1999) Evoked otoacoustic emissions arise by two fundamentally different mechanisms: a taxonomy for mammalian OAEs. J Acoust Soc Am 105(2 Pt 1):782–798
pubmed: 9972564 doi: 10.1121/1.426948
Brass D, Kemp DT (1993) Suppression of stimulus frequency otoacoustic emissions. J Acoust Soc Am 93(2):920–939
pubmed: 8445127 doi: 10.1121/1.405453
Siegel JH et al (2005) Delays of stimulus-frequency otoacoustic emissions and cochlear vibrations contradict the theory of coherent reflection filtering. J Acoust Soc Am 118(4):2434–2443
pubmed: 16266165 doi: 10.1121/1.2005867
Keefe DH et al (2008) Two-tone suppression of stimulus frequency otoacoustic emissions. J Acoust Soc Am 123(3):1479–1494
pubmed: 18345837 doi: 10.1121/1.2828209
Lichtenhan JT (2012) Effects of low-frequency biasing on otoacoustic and neural measures suggest that stimulus-frequency otoacoustic emissions originate near the peak region of the traveling wave. J Assoc Res Otolaryngol 13(1):17–28
pubmed: 22002610 doi: 10.1007/s10162-011-0296-x
Guinan JJ (1990) Changes in stimulus frequency otoacoustic emissions produced by two-tone suppression and efferent stimulation in cats. In: Dallos P et al (eds) Mechanics and biophysics of hearing. Springer, New York, pp 170–177
doi: 10.1007/978-1-4757-4341-8_21
Salt AN et al (2013) Large endolymphatic potentials from low-frequency and infrasonic tones in the guinea pig. J Acoust Soc Am 133(3):1561–1571
pubmed: 23464026 doi: 10.1121/1.4789005
Lee C et al (2019) Cochlear compound action potentials from high-level tone bursts originate from wide cochlear regions that are offset toward the most sensitive cochlear region. J Neurophysiol 121(3):1018–1033
pubmed: 30673362 pmcid: 6520629 doi: 10.1152/jn.00677.2018
Lichtenhan JT et al (2016) Drug delivery into the cochlear apex: improved control to sequentially affect finely spaced regions along the entire length of the cochlear spiral. J Neurosci Methods 273:201–209
pubmed: 27506463 pmcid: 5075496 doi: 10.1016/j.jneumeth.2016.08.005
Lichtenhan JT et al (2014) The auditory nerve overlapped waveform (ANOW) originates in the cochlear apex. J Assoc Res Otolaryngol 15(3):395–411
pubmed: 24515339 pmcid: 4010591 doi: 10.1007/s10162-014-0447-y
Lichtenhan JT et al (2017) Direct administration of 2-hydroxypropyl-beta-cyclodextrin into guinea pig cochleae: effects on physiological and histological measurements. PLoS ONE 12(4):e0175236
pubmed: 28384320 pmcid: 5383289 doi: 10.1371/journal.pone.0175236
Tsuji J, Liberman MC (1997) Intracellular labeling of auditory nerve fibers in guinea pig: central and peripheral projections. J Comp Neurol 381(2):188–202
pubmed: 9130668 doi: 10.1002/(SICI)1096-9861(19970505)381:2<188::AID-CNE6>3.0.CO;2-#
Kakehata S, Santos-Sacchi J (1996) Effects of salicylate and lanthanides on outer hair cell motility and associated gating charge. J Neurosci 16(16):4881–4889
pubmed: 8756420 pmcid: 6579298 doi: 10.1523/JNEUROSCI.16-16-04881.1996
Evans EF, Borerwe TA (1982) Ototoxic effects of salicylates on the responses of single cochlear nerve fibres and on cochlear potentials. Br J Audiol 16(2):101–108
pubmed: 7093561 doi: 10.3109/03005368209081454
Wu T et al (2010) Effect of salicylate on KCNQ4 of the guinea pig outer hair cell. J Neurophysiol 103(4):1969–1977
pubmed: 20147414 pmcid: 2853271 doi: 10.1152/jn.01057.2009
Wallace MN et al (2021) Salicylate decreases the spontaneous firing rate of guinea pig auditory nerve fibres. Neurosci Lett 747:135705
pubmed: 33548408 pmcid: 7957321 doi: 10.1016/j.neulet.2021.135705
Guinan JJ (2022) Cochlear amplification in the short-wave region by outer hair cells changing organ-of-Corti area to amplify the fluid traveling wave. Hear Res 426:108641
doi: 10.1016/j.heares.2022.108641
Fisher JA et al (2012) The spatial pattern of cochlear amplification. Neuron 76(5):989–997
pubmed: 23217746 pmcid: 3721062 doi: 10.1016/j.neuron.2012.09.031
Fallah E, Strimbu CE, Olson ES (2021) Nonlinearity of intracochlear motion and local cochlear microphonic: comparison between guinea pig and gerbil. Hear Res 405:108234
pubmed: 33930834 pmcid: 8113154 doi: 10.1016/j.heares.2021.108234
Fallah E, Strimbu CE, Olson ES (2019) Nonlinearity and amplification in cochlear responses to single and multi-tone stimuli. Hear Res 377:271–281
pubmed: 31015062 pmcid: 6511461 doi: 10.1016/j.heares.2019.04.001
Dewey JB, Applegate BE, Oghalai JS (2019) Amplification and suppression of traveling waves along the mouse Organ of Corti: evidence for spatial variation in the longitudinal coupling of outer hair cell-generated forces. J Neurosci 39(10):1805–1816
pubmed: 30651330 pmcid: 6407303 doi: 10.1523/JNEUROSCI.2608-18.2019
Ruel J et al (1999) AMPA-preferring glutamate receptors in cochlear physiology of adult guinea-pig. J Physiol 518(Pt 3):667–80
pubmed: 10420005 pmcid: 2269473 doi: 10.1111/j.1469-7793.1999.0667p.x
Pujol R, Puel JL (1999) Excitotoxicity, synaptic repair, and functional recovery in the mammalian cochlea: a review of recent findings. Ann N Y Acad Sci 884:249–254
pubmed: 10842598 doi: 10.1111/j.1749-6632.1999.tb08646.x
Ruel J et al (2000) The selective AMPA receptor antagonist GYKI 53784 blocks action potential generation and excitotoxicity in the guinea pig cochlea. Neuropharmacology 39(11):1959–1973
pubmed: 10963740 doi: 10.1016/S0028-3908(00)00069-1
Lichtenhan JT, Cooper NP, Guinan JJ Jr (2013) A new auditory threshold estimation technique for low frequencies: proof of concept. Ear Hear 34(1):42–51
pubmed: 22874644 pmcid: 3495092 doi: 10.1097/AUD.0b013e31825f9bd3
Lewis JD, Goodman SS (2014) The effect of stimulus bandwidth on the nonlinear-derived tone-burst-evoked otoacoustic emission. J Assoc Res Otolaryngol 15(6):915–931
pubmed: 25245497 pmcid: 4389961 doi: 10.1007/s10162-014-0484-6
Mertes IB, Goodman SS (2013) Short-latency transient-evoked otoacoustic emissions as predictors of hearing status and thresholds. J Acoust Soc Am 134(3):2127–2135
pubmed: 23967943 doi: 10.1121/1.4817831
Goodman SS et al (2018) Identifying the origin(s) of transient, tone-pip evoked otoacoustic emissions. Otoacoustic emissions: evoking the future. San Marino, California
Goodman SS, Mertes IB, Scheperle RA (2011) Delays and growth rates of multiple TEOAE components. In: Shera CA, Olson ES (eds) What fire is in mine ears: progress in auditory biomechanics. American Institute of Physics, New York, pp 279–285
Carvalho S et al (2003) Effect of click intensity on click-evoked otoacoustic emission waveforms: implications for the origin of emissions. Hear Res 175(1–2):215–225
pubmed: 12527140 doi: 10.1016/S0378-5955(02)00745-1
Moleti A, Botti T, Sisto R (2012) Transient-evoked otoacoustic emission generators in a nonlinear cochlea. J Acoust Soc Am 131(4):2891–2903
pubmed: 22501067 doi: 10.1121/1.3688474
Talmadge CL et al (2000) Modeling the combined effects of basilar membrane nonlinearity and roughness on stimulus frequency otoacoustic emission fine structure. J Acoust Soc Am 108(6):2911–2932
pubmed: 11144584 doi: 10.1121/1.1321012
Goodman SS, Boothalingam S, Lichtenhan JT (2021) Medial olivocochlear reflex effects on amplitude growth functions of long- and short-latency components of click-evoked otoacoustic emissions in humans. J Neurophysiol 125(5):1938–1953
pubmed: 33625926 pmcid: 8356769 doi: 10.1152/jn.00410.2020
Shera CA et al (2004) The dual effect of “suppressor” tones on stimulus-frequency otoacoustic emissions. Association for Research in Otolaryngology MidWinter Meeting Abstracts 27:538
Vencovsky V, Vetesnik A, Gummer AW (2020) Nonlinear reflection as a cause of the short-latency component in stimulus-frequency otoacoustic emissions simulated by the methods of compression and suppression. J Acoust Soc Am 147(6):3992–4008
pubmed: 32611132 doi: 10.1121/10.0001394
Keefe DH et al (2011) Detecting high-frequency hearing loss with click-evoked otoacoustic emissions. J Acoust Soc Am 129(1):245–261
pubmed: 21303007 pmcid: 3055286 doi: 10.1121/1.3514527
Yates GK, Withnell RH (1999) The role of intermodulation distortion in transient-evoked otoacoustic emissions. Hear Res 136(1–2):49–64
pubmed: 10511624 doi: 10.1016/S0378-5955(99)00108-2
Withnell RH, Yates GK, Kirk DL (2000) Changes to low-frequency components of the TEOAE following acoustic trauma to the base of the cochlea. Hear Res 139(1–2):1–12
pubmed: 10601708 doi: 10.1016/S0378-5955(99)00132-X

Auteurs

Shawn S Goodman (SS)

Department of Communication Sciences and Disorders, University of Iowa, Iowa City, Iowa, USA.

Shannon M Lefler (SM)

Department of Otolaryngology, Washington University School of Medicine in St. Louis, Saint Louis, MO, USA.

Choongheon Lee (C)

Department of Otolaryngology, University of Rochester, Rochester, NY, USA.

John J Guinan (JJ)

Massachusetts Eye and Ear, Eaton-Peabody Laboratories, Boston, MA, USA.
Department of Otolaryngology, Harvard Medical School, Boston, MA, USA.

Jeffery T Lichtenhan (JT)

Department of Otolaryngology, University of South Florida Morsani College of Medicine, Tampa, FL, USA. jlichtenhan@gmail.com.

Classifications MeSH