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Journal of the Association for Research in Otolaryngology

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01-02-2021 | Research Article

Effects of Kainic Acid-Induced Auditory Nerve Damage on Envelope-Following Responses in the Budgerigar (Melopsittacus undulatus)

Authors: John L. Wilson, Kristina S. Abrams, Kenneth S. Henry

Published in: Journal of the Association for Research in Otolaryngology | Issue 1/2021

Abstract

Sensorineural hearing loss is a prevalent problem that adversely impacts quality of life by compromising interpersonal communication. While hair cell damage is readily detectable with the clinical audiogram, this traditional diagnostic tool appears inadequate to detect lost afferent connections between inner hair cells and auditory nerve (AN) fibers, known as cochlear synaptopathy. The envelope-following response (EFR) is a scalp-recorded response to amplitude modulation, a critical acoustic feature of speech. Because EFRs can have greater amplitude than wave I of the auditory brainstem response (ABR; i.e., the AN-generated component) in humans, the EFR may provide a more sensitive way to detect cochlear synaptopathy. We explored the effects of kainate- (kainic acid) induced excitotoxic AN injury on EFRs and ABRs in the budgerigar (Melopsittacus undulatus), a parakeet species used in studies of complex sound discrimination. Kainate reduced ABR wave I by 65–75 % across animals while leaving otoacoustic emissions unaffected or mildly enhanced, consistent with substantial and selective AN synaptic loss. Compared to wave I loss, EFRs showed similar or greater percent reduction following kainate for amplitude-modulation frequencies from 380 to 940 Hz and slightly less reduction from 80 to 120 Hz. In contrast, forebrain-generated middle latency responses showed no consistent change post-kainate, potentially due to elevated “central gain” in the time period following AN damage. EFR reduction in all modulation frequency ranges was highly correlated with wave I reduction, though within-animal effect sizes were greater for higher modulation frequencies. These results suggest that even low-frequency EFRs generated primarily by central auditory nuclei might provide a useful noninvasive tool for detecting synaptic injury clinically.

Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48. https://doi.org/10.18637/jss.v067.i01CrossRef

Bharadwaj HM, Masud S, Mehraei G, Verhulst S, Shinn-Cunningham BG (2015) Individual differences reveal correlates of hidden hearing deficits. J Neurosci 35(5):2161–2172CrossRef

Bharadwaj HM, Verhulst S, Shaheen L, Liberman MC, Shinn-Cunningham BG (2014) Cochlear neuropathy and the coding of supra-threshold sound. Front Syst Neurosci 8:26CrossRef

Bledsoe SC, Bobbin RP, Chihal DM (1981) Kainic acid: an evaluation of its action on cochlear potentials. Hear Res 4:109–120. https://doi.org/10.1016/0378-5955(81)90040-xCrossRefPubMed

Bode HW (1945) Network analysis and feedback amplifier design. Van Nostrand, Toronto

Bourien J, Tang Y, Batrel C, Huet A, Lenoir M, Ladrech S, Desmadryl G, Nouvian R, Puel JL, Wang J (2014) Contribution of auditory nerve fibers to compound action potential of the auditory nerve. J Neurophysiol 112(5):1025–1039CrossRef

Bramhall N, Beach EF, Epp B, Le Prell CG et al (2019) The search for noise-induced cochlear synaptopathy in humans: mission impossible? Hear Res 377:88–103CrossRef

Brittan-Powell EF, Dooling RJ, Gleich O (2002) Auditory brainstem responses in adult budgerigars (Melopsittacus undulatus). J Acoust Soc Am 112:999–1008. https://doi.org/10.1121/1.1494807CrossRefPubMed

Carney LH (2018) Supra-threshold hearing and fluctuation profiles: implications for sensorineural and hidden hearing loss. J Assoc Res Otolaryngol 19:331–352CrossRef

Carney LH, Ketterer AD, Abrams KS, Schwarz DM, Idrobo F (2013) Detection thresholds for amplitude modulations of tones in budgerigar, rabbit, and human. Adv Exp Med Biol 787:391–398. https://doi.org/10.1007/978-1-4614-1590-9_43CrossRefPubMedPubMedCentral

Caspary DM, Ling L, Turner JG, Hughes LF (2008) Inhibitory neurotransmission, plasticity and aging in the mammalian central auditory system. J Exp Biol 211:1781–1791. https://doi.org/10.1242/jeb.013581CrossRefPubMedPubMedCentral

Chambers AR, Resnik J, Yuan Y, Whitton JP, Edge AS, Liberman MC, Polley DB (2016) Central gain restores auditory processing following near-complete cochlear denervation. Neuron. 89(4):867–879CrossRef

Cohen J (1988) Statistical power analysis for the behavioral sciences. Laurence Erlbaum Associates, USA

Conti G, Modica V, Castrataro A, Fileni A, Colosimo C Jr (1988) Latency of the auditory brainstem response (ABR) and head size: evidence of the relationship by means of radiographic data. Scand Audiol Suppl 30:219–223PubMed

Costalupes JA, Young ED, Gibson DJ (1984) Effects of continuous noise backgrounds on rate response of auditory-nerve fibers in cat. J Neurophysiol 51(6):1326–1344CrossRef

Dimitrijevic A, Alsamri J, John MS, Purcell D, George S, Zeng F (2016) Human envelope following responses to amplitude modulation: effects of aging and modulation depth. Ear Hear 37(5):e322–e335CrossRef

Dolphin WF, Mountain DC (1992) The envelope following response: scalp potentials elicited in the Mongolian gerbil using sinusoidally AM acoustic signals. Hear Res 58(1):70–78CrossRef

Dooling RJ, Lohr B, Dent ML (2000) Hearing in birds and reptiles. In: Dooling RJ, Fay RR, Popper AN (eds) Comparative hearing: birds and reptiles. Springer, New York, pp 308–359CrossRef

Dooling RJ, Searcy MH (1981) Amplitude modulation thresholds for the parakeet (Melopsittacus undulatus). J Comp Physiol 43:383–388. https://doi.org/10.1007/BF00611177CrossRef

Harris KC, Vaden KI, McClaskey CM, Dias JW, Dubno JR (2018) Complementary metrics of human auditory nerve function derived from compound action potentials. J Neurophysiol 119(3):1019–1028. https://doi.org/10.1152/jn.00638.2017CrossRefPubMed

Henry KS, Abrams KS (2018) Persistent auditory nerve damage following kainic acid excitotoxicity in the budgerigar (Melopsittacus undulates). J Assoc Res Otolaryngol 19(4):435–449CrossRef

Henry KS, Amburgey KN, Abrams KS, Carney LH (2020) Identifying cues for tone-in-noise detection using decision variable correlation in the budgerigar (Melopsittacus undulatus). J Acoust Soc Am 147:984–997CrossRef

Henry KS, Amburgey KN, Abrams KS, Idrobo F, Carney LH (2017) Formant-frequency discrimination of synthesized vowels in budgerigars (Melopsittacus undulatus) and humans. J Acoust Soc Am 142:2073–2083. https://doi.org/10.1121/1.5006912CrossRefPubMedPubMedCentral

Henry KS, Lucas JR (2008) Coevolution of auditory sensitivity and temporal resolution with acoustic signal space in three songbirds. Anim Behav 76:1659–1671CrossRef

Henry KS, Neilans EG, Abrams KS, Idrobo F, Carney LH (2016) Neural correlates of behavioral amplitude modulation sensitivity in the budgerigar midbrain. J Neurophysiol 115(4):1905–1916CrossRef

Hickox AE, Larsen E, Heinz MG, Shinobu L, Whitton JP (2017) Translational issues in cochlear synaptopathy. Hear Res 349:164–171. https://doi.org/10.1016/j.heares.2016.12.010CrossRefPubMedPubMedCentral

Hickox AE, Liberman MC (2014) Is noise-induced cochlear neuropathy key to the generation of hyperacusis or tinnitus? J Neurophysiol 111:552–564. https://doi.org/10.1152/jn.00184.2013CrossRefPubMed

Juiz JM, Rueda J, Merchán JA, Sala ML (1989) The effects of kainic acid on the cochlear ganglion of the rat. Hear Res 40:65–74. https://doi.org/10.1016/0378-5955(89)90100-7CrossRefPubMed

Keshishzadeh S, Garrett M, Vasilkov V, Verhulst S (2020) The derived-band envelope following response and its sensitivity to sensorineural hearing deficits. Hear Res 392:107979. https://doi.org/10.1016/j.heares.2020.107979CrossRefPubMed

Konishi M (1964) Effects of deafening on song development in two species of juncos. Condor 66:85–102CrossRef

Kujawa SG, Liberman MC (2009) Adding insult to injury: cochlear nerve degeneration after “temporary” noise-induced hearing loss. J Neurosci 29:14077–14085. https://doi.org/10.1523/JNEUROSCI.2845-09.2009CrossRefPubMedPubMedCentral

Kujawa SG, Liberman MC (2015) Synaptopathy in the noise-exposed and aging cochlea: primary neural degeneration in acquired sensorineural hearing loss. Hear Res 330:191–199CrossRef

Kuwada S, Anderson JS, Batra R, Fitzpatrick DC, Teissier N, D’Angelo WR (2002) Sources of the scalp-recorded amplitude-modulation following response. J Am Acad Audiol 13(4):188–204CrossRef

Liberman MC, Epstein MJ, Cleveland SS, Wang H, Maison SF (2016) Toward a differential diagnosis of hidden hearing loss in humans. PLoS One 11(9):1–15CrossRef

Liberman LD, Liberman MC (2015) Dynamics of cochlear synaptopathy after acoustic overexposure. J Assoc Res Otolaryngol 16:205–219. https://doi.org/10.1007/s10162-015-0510-3CrossRefPubMedPubMedCentral

Lin FR, Niparko JK, Ferrucci L (2011) Hearing loss prevalence in the United States. Arch Intern Med 171(20):1851–1852CrossRef

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

Long GR, Talmadge CL, Lee J (2008) Measuring distortion product otoacoustic emissions using continuously sweeping primaries. J Acoust Soc Am 124:1613–1626CrossRef

Makary CA, Shin J, Kujawa SG, Liberman MC, Merchant SN (2011) Age-related primary cochlear neuronal degeneration in human temporal bones. J Assoc Res Otolaryngol 12(6):711–717CrossRef

Mepani AM, Verhulst S, Liberman MC, Maison S. (2020) Detection of cochlear synaptopathy using EFRs: influence of stimulus envelope. Poster presentation at the American Auditory Society Scientific and Technology Meeting in Scottsdale, AZ

Mills J, Schmiedt R, Schulte B, Dubno J (2006) Age-related hearing loss: a loss of voltage, not hair cells. Semin Hear 27:228–236CrossRef

Otte J, Schuknecht HF, Kerr AG (1978) Ganglion cell populations in normal and pathological human cochleae: implications for cochlear implantation. Laryngoscope. 88:1231–1246. https://doi.org/10.1288/00005537-197808000-00004CrossRefPubMed

Parthasarathy A, Kujawa SG (2018) Synaptopathy in the aging cochlea: characterizing early-neural deficits in auditory temporal envelope processing. J Neurosci 38(32):7108–7119CrossRef

Prendergast G, Guest H, Munro KJ, Kluk K, Leger A, Hall DA, Heinz MG, Plack CJ (2017) Effects of noise exposure on young adults with normal audiograms I: electrophysiology. Hear Res 344:68–71CrossRef

Pujol R, Lenoir M, Robertson D, Eybalin M, Johnstone BM (1985) Kainic acid selectively alters auditory dendrites connected with cochlear inner hair cells. Hear Res 18:145–151CrossRef

Salvi RJ, Sun W, Ding DL, Chen GD, Lobarinas E, Wang J, Radziwon K, Auerbach BD (2017) Inner hair cell loss disrupts hearing and cochlear function leading to sensory deprivation and enhanced central auditory gain. Front Neurosci 10:1–14. https://doi.org/10.3389/fnins.2016.00621CrossRef

Schaette R, McAlpine D (2011) Tinnitus with a normal audiogram: physiological evidence for hidden hearing loss and computational model. J Neurosci 31(38):13452–13457CrossRef

Schermuly L, Klinke R (1985) Change of characteristic frequency of pigeon primary auditory afferents with temperature. J Comp Phys A 156:209–211. https://doi.org/10.1007/BF00610863CrossRef

Schmiedt, RA. (2010). The physiology of cochlear presbycusis. In: Gordon-Salant S et al. (eds.) The aging auditory system, Springer handbook of auditory research 34, Springer Science + Business Media, pp 9-38

Schoonhoven R, Boden CJ, Verbunt JPA, De Munck JC (2003) A whole head MEG study of the amplitude-modulation-following response: phase coherence, group delay and dipole source analysis. Clin Neurophysiol 114(11):2096–2106CrossRef

Schrode KM, Muniak MA, Kim YH, Lauer AM (2018) Central compensation in auditory brainstem after damaging noise exposure. eNeuro. 5(4):ENEURO.0250–ENEU18.2018. https://doi.org/10.1523/ENEURO.0250-18.2018CrossRef

Schuknecht HF, Woellner RC (1953) Hearing losses following partial sectioning of the cochlear nerve. Laryngoscope. 63:441–465PubMed

Shaheen LA, Valero MD, Liberman MC (2015) Towards a diagnosis of cochlear neuropathy with envelope following responses. J Assoc Res Otolaryngol 16(6):727–745CrossRef

Shero M, Salvi RJ, Chen L, Hashino E (1998) Excitotoxic effect of kainic acid on chicken cochlear afferent neurons. Neurosci Lett 257:81–84. https://doi.org/10.1016/S0304-3940(98)00821-0CrossRefPubMed

Sun H, Salvi RJ, Ding DL, Hashino E, Shero M, Zheng XY (2000) Excitotoxic effect of kainic acid on chicken otoacoustic emissions and cochlear potentials. J Acoust Soc Am 107:2136–2142. https://doi.org/10.1121/1.428495CrossRefPubMed

Sun H, Hashino E, Ding DL, Salvi RJ (2001) Reversible and irreversible damage to cochlear afferent neurons by kainic acid excitotoxicity. J Comp Neurol 430:172–181CrossRef

Valero MD, Burton JA, Hauser SN, Hackett TA, Ramachandran R, Liberman MC (2017) Noise-induced cochlear synaptopathy in rhesus monkeys (Macaca mulatta). Hear Res 353:213–223CrossRef

Verhulst S, Altoe A, Vasilkov V (2018) Computational modeling of the human auditory periphery: auditory-nerve responses, evoked potentials and hearing loss. Hear Res 360:55–75CrossRef

Wong SJ, Abrams KS, Amburgey KN, Wang Y, Henry KS (2019) Effects of selective auditory-nerve damage on the behavioral audiogram and temporal integration in the budgerigar. Hear Res 374:24–34CrossRef

Yeend I, Beach EF, Sharma M, Dillon H (2017) The effects of noise exposure and musical training on suprathreshold auditory processing and speech perception in noise. Hear Res 353:224–236CrossRef

Yuan Y, Shi F, Yin Y, Tong M, Lang H, Polley DB, Liberman MC, Edge ASB (2014) Ouabain-induced cochlear nerve degeneration: synaptic loss and plasticity in a mouse model of auditory neuropathy. J Assoc Res Otolaryngol 15:31–43. https://doi.org/10.1007/s10162-013-0419-7CrossRefPubMed

Zaaroor M, Starr A (1991) Auditory brain-stem evoked potentials in cat after kainic acid induced neuronal loss. I. Superior olivary complex. Electroencephaolgr Clin Neurophysiol 80:422–435. https://doi.org/10.1016/0168-5597(91)90091-bCrossRef

Zheng XY, Wang J, Salvi RJ, Henderson D (1996) Effects of kainic acid on the cochlear potentials and distortion product otoacoustic emissions in chinchilla. Hear Res 95:161–167. https://doi.org/10.1016/0378-5955(96)00047-0CrossRefPubMed

Zhong Z, Henry KS, Heinz MG (2014) Sensorineural hearing loss amplifies neural coding of envelope information in the central auditory system of chinchillas. Hear Res 309:55–62CrossRef

Title: Effects of Kainic Acid-Induced Auditory Nerve Damage on Envelope-Following Responses in the Budgerigar (Melopsittacus undulatus)
Authors: John L. Wilson
Kristina S. Abrams
Kenneth S. Henry
Publication date: 01-02-2021
Publisher: Springer US
Published in: Journal of the Association for Research in Otolaryngology / Issue 1/2021
Print ISSN: 1525-3961
Electronic ISSN: 1438-7573
DOI: https://doi.org/10.1007/s10162-020-00776-x

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Effects of Kainic Acid-Induced Auditory Nerve Damage on Envelope-Following Responses in the Budgerigar (Melopsittacus undulatus)

Abstract

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Abstract

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