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Journal of the Association for Research in Otolaryngology

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05.10.2023 | Original Article: General Research

Histological Correlates of Auditory Nerve Injury from Kainic Acid in the Budgerigar (Melopsittacus undulatus)

verfasst von: Yingxuan Wang, Kristina S. Abrams, Margaret Youngman, Kenneth S. Henry

Erschienen in: Journal of the Association for Research in Otolaryngology | Ausgabe 5/2023

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Abstract

Purpose

Loss of auditory nerve afferent synapses with cochlear hair cells, called cochlear synaptopathy, is a common pathology in humans caused by aging and noise overexposure. The perceptual consequences of synaptopathy in isolation from other cochlear pathologies are still unclear. Animal models provide an effective approach to resolve uncertainty regarding the physiological and perceptual consequences of auditory nerve loss, because neural lesions can be induced and readily quantified. The budgerigar, a parakeet species, has recently emerged as an animal model for synaptopathy studies based on its capacity for vocal learning and ability to behaviorally discriminate simple and complex sounds with acuity similar to humans. Kainic acid infusions in the budgerigar produce a profound reduction of compound auditory nerve responses, including wave I of the auditory brainstem response, without impacting physiological hair cell measures. These results suggest selective auditory nerve damage. However, histological correlates of neural injury from kainic acid are still lacking.

Methods

We quantified the histological effects caused by intracochlear infusion of kainic acid (1 mM; 2.5 µL), and evaluated correlations between the histological and physiological assessments of auditory nerve status.

Results

Kainic acid infusion in budgerigars produced pronounced loss of neural auditory nerve soma (60% on average) in the cochlear ganglion, and of peripheral axons, at time points 2 or more months following injury. The hair cell epithelium was unaffected by kainic acid. Neural loss was significantly correlated with reduction of compound auditory nerve responses and auditory brainstem response wave I.

Conclusion

Compound auditory nerve responses and wave I provide a useful index of cochlear synaptopathy in this animal model.

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):711–717. https://doi.org/10.1007/s10162-011-0283-2CrossRefPubMedPubMedCentral

Viana LM, O’Malley JT, Burgess BJ, Jones DD, Oliveira CA, Santos F, Merchant SN, Liberman LD, Liberman MC (2015) Cochlear neuropathy in human presbycusis: confocal analysis of hidden hearing loss in post-mortem tissue. Hear Res 327:78–88. https://doi.org/10.1016/j.heares.2015.04.014CrossRefPubMedPubMedCentral

Wu PZ, Liberman LD, Bennett K, de Gruttola V, O’Malley JT, Liberman MC (2019) Primary neural degeneration in the human cochlea: evidence for hidden hearing loss in the aging ear. Neuroscience 407:8–20. https://doi.org/10.1016/j.neuroscience.2018.07.053CrossRefPubMed

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):e0162726. https://doi.org/10.1371/journal.pone.0162726CrossRefPubMedPubMedCentral

Grant KJ, Mepani AM, Wu PZ, Hancock KE, de Gruttola V, Liberman MC, Maison SF (2020) Electrophysiological markers of cochlear function correlate with hearing-in-noise performance among audiometrically normal subjects. J Neurophysiol 124(2):418–431. https://doi.org/10.1152/jn.00016.2020CrossRefPubMedPubMedCentral

Grose JH, Buss E, Hall JW 3rd (2017) Loud music exposure and cochlear synaptopathy in young adults: isolated auditory brainstem response effects but no perceptual consequences. Trends Hear 21:2331216517737417. https://doi.org/10.1177/2331216517737417CrossRefPubMedPubMedCentral

Prendergast G, Millman RE, Guest H, Munro KJ, Kluk K, Dewey RS, Hall DA, Heinz MG, Plack CJ (2017) Effects of noise exposure on young adults with normal audiograms II: behavioral measures. Hear Res 356:74–86. https://doi.org/10.1016/j.heares.2017.10.007CrossRefPubMedPubMedCentral

Guest H, Munro KJ, Prendergast G, Plack CJ (2019) Reliability and interrelations of seven proxy measures of cochlear synaptopathy. Hear Res 375:34–43. https://doi.org/10.1016/j.heares.2019.01.018CrossRefPubMedPubMedCentral

Henry KS (2022) Animal models of hidden hearing loss: does auditory-nerve-fiber loss cause real-world listening difficulties? Mol Cell Neurosci 118:103692. https://doi.org/10.1016/j.mcn.2021.103692CrossRefPubMed

10.

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

11.

Kujawa SG, Liberman MC (2009) Adding insult to injury: cochlear nerve degeneration after “temporary” noise-induced hearing loss. J Neurosci 29(45):14077–14085. https://doi.org/10.1523/JNEUROSCI.2845-09.2009CrossRefPubMedPubMedCentral

12.

Lin HW, Furman AC, Kujawa SG, Liberman MC (2011) Primary neural degeneration in the Guinea pig cochlea after reversible noise-induced threshold shift. J Assoc Res Otolaryngol 12(5):605–616. https://doi.org/10.1007/s10162-011-0277-0CrossRefPubMedPubMedCentral

13.

Yuan Y, Shi F, Yin Y, Tong M, Lang H, Polley DB, Liberman MC, Edge AS (2014) Ouabain-induced cochlear nerve degeneration: synaptic loss and plasticity in a mouse model of auditory neuropathy. J Assoc Res Otolaryngol 15(1):31–43. https://doi.org/10.1007/s10162-013-0419-7CrossRefPubMed

14.

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):867–879. https://doi.org/10.1016/j.neuron.2015.12.041CrossRefPubMedPubMedCentral

15.

Henry KS, Abrams KS (2018) Persistent auditory nerve damage following kainic acid excitotoxicity in the budgerigar (Melopsittacus undulatus). J Assoc Res Otolaryngol 19(4):435–449. https://doi.org/10.1007/s10162-018-0671-yCrossRefPubMedPubMedCentral

16.

McLennan H (1983) Receptors for the excitatory amino acids in the mammalian central nervous system. Prog Neurobiol 20(3–4):251–271. https://doi.org/10.1016/0301-0082(83)90004-7CrossRefPubMed

17.

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(2):145–151. https://doi.org/10.1016/0378-5955(85)90006-1CrossRefPubMed

18.

Juiz JM, Rueda J, Merchan JA, Sala ML (1989) The effects of kainic acid on the cochlear ganglion of the rat. Hear Res 40(1–2):65–74. https://doi.org/10.1016/0378-5955(89)90100-7CrossRefPubMed

19.

Shero M, Salvi RJ, Chen L, Hashino E (1998) Excitotoxic effect of kainic acid on chicken cochlear afferent neurons. Neurosci Lett 257(2):81–84. https://doi.org/10.1016/s0304-3940(98)00821-0CrossRefPubMed

20.

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(2):172–181. https://doi.org/10.1002/1096-9861(20010205)430:2%3c172::aid-cne1023%3e3.0.co;2-wCrossRefPubMed

21.

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(1–2):161–167. https://doi.org/10.1016/0378-5955(96)00047-0CrossRefPubMed

22.

Ding D, Qi W, Jiang H, Salvi R (2021) Excitotoxic damage to auditory nerve afferents and spiral ganglion neurons is correlated with developmental upregulation of AMPA and KA receptors. Hear Res 411:108358. https://doi.org/10.1016/j.heares.2021.108358CrossRefPubMed

23.

Walia A, Lee C, Hartsock J, Goodman SS, Dolle R, Salt AN, Lichtenhan JT, Rutherford MA (2021) Reducing auditory nerve excitability by acute antagonism of Ca(2+)-permeable AMPA receptors. Front Synaptic Neurosci 13:680621. https://doi.org/10.3389/fnsyn.2021.680621CrossRefPubMedPubMedCentral

24.

Okanoya K, Dooling RJ (1987) Hearing in passerine and psittacine birds: a comparative study of absolute and masked auditory thresholds. J Comp Psychol 101(1):7–15. https://doi.org/10.1037/0735-7036.101.1.7CrossRefPubMed

25.

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(2):984. https://doi.org/10.1121/10.0000621CrossRefPubMedPubMedCentral

26.

Dent ML, Dooling RJ, Pierce AS (2000) Frequency discrimination in budgerigars (Melopsittacus undulatus): effects of tone duration and tonal context. J Acoust Soc Am 107(5 Pt 1):2657–2664. https://doi.org/10.1121/1.428651CrossRefPubMed

27.

Dooling RJ, Searcy MH (1981) Amplitude-nodulation thresholds for the parakeet (Melopsittacus-undulatus). J Comp Physiol 143(3):383–388. https://doi.org/10.1007/Bf00611177CrossRef

28.

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

29.

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):1905–1916. https://doi.org/10.1152/jn.01003.2015CrossRefPubMedPubMedCentral

30.

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(4):2073. https://doi.org/10.1121/1.5006912CrossRefPubMedPubMedCentral

31.

Henry KS, Abrams KS, Forst J, Mender MJ, Neilans EG, Idrobo F, Carney LH (2017) Midbrain synchrony to envelope structure supports behavioral sensitivity to single-formant vowel-like sounds in noise. J Assoc Res Otolaryngol 18(1):165–181. https://doi.org/10.1007/s10162-016-0594-4CrossRefPubMed

32.

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 374:24–34. https://doi.org/10.1016/j.heares.2019.01.019CrossRefPubMedPubMedCentral

33.

Wilson JL, Abrams KS, Henry KS (2021) Effects of kainic acid-induced auditory nerve damage on envelope-following responses in the budgerigar (Melopsittacus undulatus). J Assoc Res Otolaryngol 22(1):33–49. https://doi.org/10.1007/s10162-020-00776-xCrossRefPubMed

34.

Henry KS, Abrams KS (2021) Normal tone-in-noise sensitivity in trained budgerigars despite substantial auditory-nerve injury: no evidence of hidden hearing loss. J Neurosci 41(1):118–129. https://doi.org/10.1523/JNEUROSCI.2104-20.2020CrossRefPubMedPubMedCentral

35.

Gleich O, Fischer FP, Köppl C, Manley GA (2004) Hearing organ evolution and specialization: archosaurs. In: Fay RR, Popper AN (eds) Evolution of the Vertebrate Auditory System. Springer, New York, pp 224–255CrossRef

36.

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

37.

Manley GA, Clack JA (2004) An outline of the evolution of vertebrate hearing organs. In: Fay RR, Popper AN (eds) Evolution of the Vertebrate Auditory System. Springer, New York, pp 1–26CrossRef

38.

Koppl C (2011) Birds–same thing, but different? Convergent evolution in the avian and mammalian auditory systems provides informative comparative models. Hear Res 273(1–2):65–71. https://doi.org/10.1016/j.heares.2010.03.095CrossRefPubMed

39.

Salvi RJ, Saunders SS, Powers NL, Boettcher FA (1992) Discharge patterns of cochlear ganglion neurons in the chicken. J Comp Physiol A 170(2):227–241. https://doi.org/10.1007/BF00196905CrossRefPubMed

40.

Manley GA, Gleich O, Leppelsack HJ, Oeckinghaus H (1985) Activity patterns of cochlear ganglion neurones in the starling. J Comp Physiol A 157(2):161–181. https://doi.org/10.1007/BF01350025CrossRefPubMed

41.

Gleich O (1989) Auditory primary afferents in the starling: correlation of function and morphology. Hear Res 37(3):255–267. https://doi.org/10.1016/0378-5955(89)90026-9CrossRefPubMed

42.

Manley GA, Schwabedissen G, Gleich O (1993) Morphology of the basilar papilla of the budgerigar. Melopsittacus undulatus J Morphol 218(2):153–165. https://doi.org/10.1002/jmor.1052180205CrossRefPubMed

43.

Ryals BM, Westbrook EW (1988) Ganglion cell and hair cell loss in Coturnix quail associated with aging. Hear Res 36(1):1–8. https://doi.org/10.1016/0378-5955(88)90133-5CrossRefPubMed

44.

Manley GA, Brix J, Kaiser A (1987) Developmental stability of the tonotopic organization of the chick’s basilar papilla. Science 237(4815):655–656. https://doi.org/10.1126/science.3603046CrossRefPubMed

45.

Chen L, Salvi R, Shero M (1994) Cochlear frequency-place map in adult chickens: intracellular biocytin labeling. Hear Res 81(1–2):130–136. https://doi.org/10.1016/0378-5955(94)90160-0CrossRefPubMed

46.

Köppl C (1997) Frequency tuning and spontaneous activity in the auditory nerve and cochlear nucleus magnocellularis of the barn owl Tyto alba. J Neurophysiol 77(1):364–377. https://doi.org/10.1152/jn.1997.77.1.364CrossRefPubMed

47.

Weiss S (1990) Pharmacological properties of the N-methyl-D-aspartate receptor system coupled to the evoked release of gamma-[3H] aminobutyric acid from striatal neurons in primary culture. J Pharmacol Exp Ther 252(1):380–386PubMed

48.

Azarias G, Kruusmagi M, Connor S, Akkuratov EE, Liu XL, Lyons D, Brismar H, Broberger C, Aperia A (2013) A specific and essential role for Na, K-ATPase alpha3 in neurons co-expressing alpha1 and alpha3. J Biol Chem 288(4):2734–2743. https://doi.org/10.1074/jbc.M112.425785CrossRefPubMed

49.

Schmiedt RA, Okamura HO, Lang H, Schulte BA (2002) Ouabain application to the round window of the gerbil cochlea: a model of auditory neuropathy and apoptosis. J Assoc Res Otolaryngol 3(3):223–233. https://doi.org/10.1007/s1016200220017CrossRefPubMed

50.

Robertson D (1983) Functional significance of dendritic swelling after loud sounds in the guinea pig cochlea. Hear Res 9(3):263–278. https://doi.org/10.1016/0378-5955(83)90031-xCrossRefPubMed

51.

Keithley EM, Feldman ML (1979) Spiral ganglion cell counts in an age-graded series of rat cochleas. J Comp Neurol 188(3):429–442. https://doi.org/10.1002/cne.901880306CrossRefPubMed

52.

Wang Q, Green SH (2011) Functional role of neurotrophin-3 in synapse regeneration by spiral ganglion neurons on inner hair cells after excitotoxic trauma in vitro. J Neurosci 31(21):7938–7949. https://doi.org/10.1523/JNEUROSCI.1434-10.2011CrossRefPubMedPubMedCentral

53.

Versnel H, Prijs VF, Schoonhoven R (1990) Single-fibre responses to clicks in relationship to the compound action potential in the guinea pig. Hear Res 46(1–2):147–160. https://doi.org/10.1016/0378-5955(90)90145-fCrossRefPubMed

54.

Buchwald JS, Huang C (1975) Far-field acoustic response: origins in the cat. Science 189(4200):382–384. https://doi.org/10.1126/science.1145206CrossRefPubMed

55.

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):1025–1039. https://doi.org/10.1152/jn.00738.2013CrossRefPubMed

56.

Lee C, Guinan JJ Jr, Rutherford MA, Kaf WA, Kennedy KM, Buchman CA, Salt AN, Lichtenhan JT (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. https://doi.org/10.1152/jn.00677.2018CrossRefPubMedPubMedCentral

57.

Brittan-Powell EF, Dooling RJ, Gleich O (2002) Auditory brainstem responses in adult budgerigars (Melopsittacus undulatus). J Acoust Soc Am 112(3 Pt 1):999–1008. https://doi.org/10.1121/1.1494807CrossRefPubMed

58.

Caus Capdevila M, Sienknecht U, Köppl C (2021) Developmental maturation of presynaptic ribbon numbers in chicken basilar-papilla hair cells and its perturbation by long-term overexpression of Wnt9a. Dev Neurobiol 81(6):817–832. https://doi.org/10.1002/dneu.22845CrossRefPubMed

59.

Martinez-Dunst C, Michaels R, Fuchs P (1997) Release sites and calcium channels in hair cells of the chick’s cochlea. J Neurosci 17(23):9133–9144. https://doi.org/10.1523/JNEUROSCI.17-23-09133.1997CrossRefPubMedPubMedCentral

Titel: Histological Correlates of Auditory Nerve Injury from Kainic Acid in the Budgerigar (Melopsittacus undulatus)
verfasst von: Yingxuan Wang
Kristina S. Abrams
Margaret Youngman
Kenneth S. Henry
Publikationsdatum: 05.10.2023
Verlag: Springer US
Erschienen in: Journal of the Association for Research in Otolaryngology / Ausgabe 5/2023
Print ISSN: 1525-3961
Elektronische ISSN: 1438-7573
DOI: https://doi.org/10.1007/s10162-023-00910-5

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