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Journal of the Association for Research in Otolaryngology

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15-02-2024 | Original Article

Measuring Optokinetic Reflex and Vestibulo-Ocular Reflex in Unilateral Vestibular Organ Damage Model of Zebrafish

Authors: Kang Hyeon Lim, Hong Ki Kim, Saemi Park, Eunjung Han, Insik Song, Hee Soo Yoon, Jaeyoung Kim, Yunkyoung Lee, Yong Hun Jang, Yoon Chan Rah, Sang Hyun Lee, June Choi

Published in: Journal of the Association for Research in Otolaryngology | Issue 2/2024

Abstract

One-sided vestibular disorders are common in clinical practice; however, their models have not been fully established. We investigated the effect of unilateral or bilateral deficits in the vestibular organs on the vestibulo-ocular reflex (VOR) and optokinetic reflex (OKR) of zebrafish using in-house equipment. For physical dislodgement of the otoliths in the utricles of zebrafish larvae, one or both utricles were separated from the surrounding tissue using glass capillaries. The video data from VOR and OKR tests with the larvae was collected and processed using digital signal processing techniques such as fast Fourier transform and low-pass filters. The results showed that unilateral and bilateral damage to the vestibular system significantly reduced VOR and OKR. In contrast, no significant difference was observed between unilateral and bilateral damage. This study confirmed that VOR and OKR were significantly reduced in zebrafish with unilateral and bilateral vestibular damage. Follow-up studies on unilateral vestibular disorders can be conducted using this tool.

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Strupp M, Dlugaiczyk J, Ertl-Wagner BB, Rujescu D, Westhofen M, Dieterich M (2020) Vestibular disorders Dtsch Arztebl Int 117:300–310. https://doi.org/10.3238/arztebl.2020.0300CrossRefPubMed

Aleman M (2022) Vestibular disease. Vet Clin North Am Equine Pract 38:397–407. https://doi.org/10.1016/j.cveq.2022.05.008CrossRefPubMed

Gottlob I (2000) Nystagmus. Curr Opin Ophthalmol 11:330–335. https://doi.org/10.1097/00055735-200010000-00007CrossRefPubMed

Dieterich M, Brandt T (1995) Vestibulo-ocular reflex. Curr Opin Neurol 8:83–88. https://doi.org/10.1097/00019052-199502000-00014CrossRefPubMed

Barr CC, Schultheis LW, Robinson DA (1976) Voluntary, non-visual control of the human vestibulo-ocular reflex. Acta Otolaryngol 81:365–375. https://doi.org/10.3109/00016487609107490CrossRefPubMed

Halmagyi GM, Chen L, MacDougall HG, Weber KP, McGarvie LA, Curthoys IS (2017) The video head impulse test. Front Neurol 8:258. https://doi.org/10.3389/fneur.2017.00258CrossRefPubMedPubMedCentral

Soussi-Yanicostas N (2022) Zebrafish as a model for neurological disorders. Int J Mol Sci 23. https://doi.org/10.3390/ijms23084321

Nicolson T (2017) The genetics of hair-cell function in zebrafish. J Neurogenet 31:102–112. https://doi.org/10.1080/01677063.2017.1342246CrossRefPubMedPubMedCentral

Ehrlich DE, Schoppik D (2017) Control of movement initiation underlies the development of balance. Curr Biol 27:334–344. https://doi.org/10.1016/j.cub.2016.12.003CrossRefPubMedPubMedCentral

10.

Han E, Ho OhK, Park S, Chan Rah Y, Park HC, Koun S, Choi J (2020) Analysis of behavioral changes in zebrafish (Danio rerio) larvae caused by aminoglycoside-induced damage to the lateral line and muscles. Neurotoxicology 78:134–142. https://doi.org/10.1016/j.neuro.2020.03.005CrossRefPubMed

11.

Han E, Lee DH, Park S, Rah YC, Park HC, Choi JW, Choi J (2022) Noise-induced hearing loss in zebrafish model: characterization of tonotopy and sex-based differences. Hear Res 418:108485. https://doi.org/10.1016/j.heares.2022.108485CrossRefPubMed

12.

Rihel J, Prober DA, Arvanites A, Lam K, Zimmerman S, Jang S, Haggarty SJ, Kokel D, Rubin LL, Peterson RT, Schier AF (2010) Zebrafish behavioral profiling links drugs to biological targets and rest/wake regulation. Science 327:348–351. https://doi.org/10.1126/science.1183090CrossRefPubMedPubMedCentral

13.

Furutani-Seiki M, Jiang YJ, Brand M, Heisenberg CP, Houart C, Beuchle D, van Eeden FJ, Granato M, Haffter P, Hammerschmidt M, Kane DA, Kelsh RN, Mullins MC, Odenthal J, Nüsslein-Volhard C (1996) Neural degeneration mutants in the zebrafish, Danio rerio. Development 123:229–239. https://doi.org/10.1242/dev.123.1.229CrossRefPubMed

14.

Hong SJ, Im GJ, Chang J, Chae SW, Lee SH, Kwon SY, Jung HH, Chung AY, Park HC, Choi J (2013) Protective effects of edaravone against cisplatin-induced hair cell damage in zebrafish. Int J Pediatr Otorhinolaryngol 77:1025–1031. https://doi.org/10.1016/j.ijporl.2013.04.003CrossRefPubMed

15.

Choi J, Im GJ, Chang J, Chae SW, Lee SH, Kwon SY, Chung AY, Park HC, Jung HH (2013) Protective effects of apocynin on cisplatin-induced ototoxicity in an auditory cell line and in zebrafish. J Appl Toxicol 33:125–133. https://doi.org/10.1002/jat.1729CrossRefPubMed

16.

Han E, Choi YJ, Park S, Rah YC, Park H-C, Lee SH, Choi J (2024) A comprehensive characterizations of zebrafish rheotactic behaviors and its application to otoprotective drug screening. Expert Systems with Applications 237:121496. https://doi.org/10.1016/j.eswa.2023.121496

17.

Howe K, Clark MD, Torroja CF, Torrance J, Berthelot C, Muffato M, Collins JE, Humphray S, McLaren K, Matthews L, McLaren S, Sealy I, Caccamo M, Churcher C, Scott C, Barrett JC, Koch R, Rauch GJ, White S, Chow W, Kilian B, Quintais LT, Guerra-Assunção JA, Zhou Y, Gu Y, Yen J, Vogel JH, Eyre T, Redmond S, Banerjee R, Chi J, Fu B, Langley E, Maguire SF, Laird GK, Lloyd D, Kenyon E, Donaldson S, Sehra H, Almeida-King J, Loveland J, Trevanion S, Jones M, Quail M, Willey D, Hunt A, Burton J, Sims S, McLay K, Plumb B, Davis J, Clee C, Oliver K, Clark R, Riddle C, Elliot D, Threadgold G, Harden G, Ware D, Begum S, Mortimore B, Kerry G, Heath P, Phillimore B, Tracey A, Corby N, Dunn M, Johnson C, Wood J, Clark S, Pelan S, Griffiths G, Smith M, Glithero R, Howden P, Barker N, Lloyd C, Stevens C, Harley J, Holt K, Panagiotidis G, Lovell J, Beasley H, Henderson C, Gordon D, Auger K, Wright D, Collins J, Raisen C, Dyer L, Leung K, Robertson L, Ambridge K, Leongamornlert D, McGuire S, Gilderthorp R, Griffiths C, Manthravadi D, Nichol S, Barker G, Whitehead S, Kay M, Brown J, Murnane C, Gray E, Humphries M, Sycamore N, Barker D, Saunders D, Wallis J, Babbage A, Hammond S, Mashreghi-Mohammadi M, Barr L, Martin S, Wray P, Ellington A, Matthews N, Ellwood M, Woodmansey R, Clark G, Cooper J, Tromans A, Grafham D, Skuce C, Pandian R, Andrews R, Harrison E, Kimberley A, Garnett J, Fosker N, Hall R, Garner P, Kelly D, Bird C, Palmer S, Gehring I, Berger A, Dooley CM, Ersan-Ürün Z, Eser C, Geiger H, Geisler M, Karotki L, Kirn A, Konantz J, Konantz M, Oberländer M, Rudolph-Geiger S, Teucke M, Lanz C, Raddatz G, Osoegawa K, Zhu B, Rapp A, Widaa S, Langford C, Yang F, Schuster SC, Carter NP, Harrow J, Ning Z, Herrero J, Searle SM, Enright A, Geisler R, Plasterk RH, Lee C, Westerfield M, de Jong PJ, Zon LI, Postlethwait JH, Nüsslein-Volhard C, Hubbard TJ, Roest Crollius H, Rogers J, Stemple DL (2013) The zebrafish reference genome sequence and its relationship to the human genome. Nature 496:498–503. https://doi.org/10.1038/nature12111CrossRefPubMedPubMedCentral

18.

Sun P, Zhang Y, Zhao F, Wu JP, Pun SH, Peng C, Du M, Vai MI, Liu D, Chen F (2018) An assay for systematically quantifying the vestibulo-ocular reflex to assess vestibular function in zebrafish larvae. Front Cell Neurosci 12:257. https://doi.org/10.3389/fncel.2018.00257CrossRefPubMedPubMedCentral

19.

Graham SL, Klistorner A (2017) Afferent visual pathways in multiple sclerosis: a review. Clin Exp Ophthalmol 45:62–72. https://doi.org/10.1111/ceo.12751CrossRefPubMed

20.

Burn DJ, Lees AJ (2002) Progressive supranuclear palsy: where are we now? Lancet Neurol 1:359–369. https://doi.org/10.1016/s1474-4422(02)00161-8CrossRefPubMed

21.

Vargas-Alvarez A, Ninchritz-Becerra E, Goiburu M, Betances F, Rey-Martinez J, Altuna X (2021) Clinical prevalence of enhanced vestibulo-ocular reflex responses on video head impulse test. Otol Neurotol 42:e1160–e1169. https://doi.org/10.1097/mao.0000000000003171CrossRefPubMed

22.

Scheetz SD, Shao E, Zhou Y, Cario CL, Bai Q, Burton EA (2018) An open-source method to analyze optokinetic reflex responses in larval zebrafish. J Neurosci Methods 293:329–337. https://doi.org/10.1016/j.jneumeth.2017.10.012CrossRefPubMed

23.

Mo W, Chen F, Nechiporuk A, Nicolson T (2010) Quantification of vestibular-induced eye movements in zebrafish larvae. BMC Neurosci 11:110. https://doi.org/10.1186/1471-2202-11-110CrossRefPubMedPubMedCentral

24.

Mueller KP, Schnaedelbach OD, Russig HD, Neuhauss SC (2011) VisioTracker, an innovative automated approach to oculomotor analysis. J Vis Exp. https://doi.org/10.3791/3556CrossRefPubMedPubMedCentral

25.

Bianco IH, Ma LH, Schoppik D, Robson DN, Orger MB, Beck JC, Li JM, Schier AF, Engert F, Baker R (2012) The tangential nucleus controls a gravito-inertial vestibulo-ocular reflex. Curr Biol 22:1285–1295. https://doi.org/10.1016/j.cub.2012.05.026CrossRefPubMedPubMedCentral

26.

Roelofs CO (1954) Optokinetic nystagmus. Doc Ophthalmol 7–8:579–650. https://doi.org/10.1007/bf00238148CrossRefPubMed

27.

Izawa Y, Suzuki H (2020) Suppressive control of optokinetic and vestibular nystagmus by the primate frontal eye field. J Neurophysiol 124:691–702. https://doi.org/10.1152/jn.00015.2020CrossRefPubMed

28.

Mueller KP, Neuhauss SC (2010) Quantitative measurements of the optokinetic response in adult fish. J Neurosci Methods 186:29–34. https://doi.org/10.1016/j.jneumeth.2009.10.020CrossRefPubMed

29.

Beck JC, Gilland E, Tank DW, Baker R (2004) Quantifying the ontogeny of optokinetic and vestibuloocular behaviors in zebrafish, medaka, and goldfish. J Neurophysiol 92:3546–3561. https://doi.org/10.1152/jn.00311.2004CrossRefPubMed

30.

Brockerhoff SE, Hurley JB, Janssen-Bienhold U, Neuhauss SC, Driever W, Dowling JE (1995) A behavioral screen for isolating zebrafish mutants with visual system defects. Proc Natl Acad Sci U S A 92:10545–10549. https://doi.org/10.1073/pnas.92.23.10545CrossRefPubMedPubMedCentral

31.

Easter SS Jr, Nicola GN (1997) The development of eye movements in the zebrafish (Danio rerio). Dev Psychobiol 31:267–276. https://doi.org/10.1002/(sici)1098-2302(199712)31:4%3c267::aid-dev4%3e3.0.co;2-pCrossRefPubMed

32.

Rinner O, Rick JM, Neuhauss SC (2005) Contrast sensitivity, spatial and temporal tuning of the larval zebrafish optokinetic response. Invest Ophthalmol Vis Sci 46:137–142. https://doi.org/10.1167/iovs.04-0682CrossRefPubMed

33.

Shao E, Scheetz SD, Xie W, Burton EA (2018) Modulation of the zebrafish optokinetic reflex by pharmacologic agents targeting GABA(A) receptors. Neurosci Lett 671:33–37. https://doi.org/10.1016/j.neulet.2018.01.055CrossRefPubMedPubMedCentral

34.

Jeong SH, Kim HJ, Kim JS (2013) Vestibular neuritis. Semin Neurol 33:185–194. https://doi.org/10.1055/s-0033-1354598CrossRefPubMed

35.

Wright T (2015) Menière’s disease. BMJ Clin Evid 2015

36.

Riley BB, Moorman SJ (2000) Development of utricular otoliths, but not saccular otoliths, is necessary for vestibular function and survival in zebrafish. J Neurobiol 43:329–337. https://doi.org/10.1002/1097-4695(20000615)43:4%3c329::aid-neu2%3e3.0.co;2-hCrossRefPubMed

37.

Roeser T, Baier H (2003) Visuomotor behaviors in larval zebrafish after GFP-guided laser ablation of the optic tectum. J Neurosci 23:3726–3734. https://doi.org/10.1523/jneurosci.23-09-03726.2003CrossRefPubMedPubMedCentral

38.

Virtanen P, Gommers R, Oliphant TE, Haberland M, Reddy T, Cournapeau D, Burovski E, Peterson P, Weckesser W, Bright J, van der Walt SJ, Brett M, Wilson J, Millman KJ, Mayorov N, Nelson ARJ, Jones E, Kern R, Larson E, Carey CJ, Polat İ, Feng Y, Moore EW, VanderPlas J, Laxalde D, Perktold J, Cimrman R, Henriksen I, Quintero EA, Harris CR, Archibald AM, Ribeiro AH, Pedregosa F, van Mulbregt P, Vijaykumar A, Bardelli AP, Rothberg A, Hilboll A, Kloeckner A, Scopatz A, Lee A, Rokem A, Woods CN, Fulton C, Masson C, Häggström C, Fitzgerald C, Nicholson DA, Hagen DR, Pasechnik DV, Olivetti E, Martin E, Wieser E, Silva F, Lenders F, Wilhelm F, Young G, Price GA, Ingold G-L, Allen GE, Lee GR, Audren H, Probst I, Dietrich JP, Silterra J, Webber JT, Slavič J, Nothman J, Buchner J, Kulick J, Schönberger JL, de Miranda Cardoso JV, Reimer J, Harrington J, Rodríguez JLC, Nunez-Iglesias J, Kuczynski J, Tritz K, Thoma M, Newville M, Kümmerer M, Bolingbroke M, Tartre M, Pak M, Smith NJ, Nowaczyk N, Shebanov N, Pavlyk O, Brodtkorb PA, Lee P, McGibbon RT, Feldbauer R, Lewis S, Tygier S, Sievert S, Vigna S, Peterson S, More S, Pudlik T, Oshima T, Pingel TJ, Robitaille TP, Spura T, Jones TR, Cera T, Leslie T, Zito T, Krauss T, Upadhyay U, Halchenko YO, Vázquez-Baeza Y, SciPy C (2020) SciPy 1.0: fundamental algorithms for scientific computing in Python. Nat Methods 17:261–272. https://doi.org/10.1038/s41592-019-0686-2CrossRefPubMedPubMedCentral

39.

Wuyts FL, Furman J, Vanspauwen R, Van de Heyning P (2007) Vestibular function testing. Curr Opin Neurol 20:19–24. https://doi.org/10.1097/WCO.0b013e3280140808CrossRefPubMed

40.

Chen CC, Bockisch CJ, Bertolini G, Olasagasti I, Neuhauss SC, Weber KP, Straumann D, Ying-Yu Huang M (2014) Velocity storage mechanism in zebrafish larvae. J Physiol 592:203–214. https://doi.org/10.1113/jphysiol.2013.258640CrossRefPubMed

41.

Domarecka E, Skarzynska M, Szczepek AJ, Hatzopoulos S (2020) Use of zebrafish larvae lateral line to study protection against cisplatin-induced ototoxicity: a scoping review. Int J Immunopathol Pharmacol 34:2058738420959554. https://doi.org/10.1177/2058738420959554CrossRefPubMedPubMedCentral

42.

Yao Q, DeSmidt AA, Tekin M, Liu X, Lu Z (2016) Hearing assessment in zebrafish during the first week postfertilization. Zebrafish 13:79–86. https://doi.org/10.1089/zeb.2015.1166CrossRefPubMedPubMedCentral

43.

Lambert FM, Beck JC, Baker R, Straka H (2008) Semicircular canal size determines the developmental onset of angular vestibuloocular reflexes in larval Xenopus. J Neurosci 28:8086–8095. https://doi.org/10.1523/jneurosci.1288-08.2008CrossRefPubMedPubMedCentral

44.

Liu Z, Hildebrand DGC, Morgan JL, Jia Y, Slimmon N, Bagnall MW (2022) Organization of the gravity-sensing system in zebrafish. Nat Commun 13:5060. https://doi.org/10.1038/s41467-022-32824-wCrossRefPubMedPubMedCentral

45.

Baeza-Loya S, Raible DW (2023) Vestibular physiology and function in zebrafish. Front Cell Dev Biol 11:1172933. https://doi.org/10.3389/fcell.2023.1172933CrossRefPubMedPubMedCentral

46.

Songer JE, Eatock RA (2013) Tuning and timing in mammalian type I hair cells and calyceal synapses. J Neurosci 33:3706–3724. https://doi.org/10.1523/jneurosci.4067-12.2013CrossRefPubMedPubMedCentral

Title: Measuring Optokinetic Reflex and Vestibulo-Ocular Reflex in Unilateral Vestibular Organ Damage Model of Zebrafish
Authors: Kang Hyeon Lim
Hong Ki Kim
Saemi Park
Eunjung Han
Insik Song
Hee Soo Yoon
Jaeyoung Kim
Yunkyoung Lee
Yong Hun Jang
Yoon Chan Rah
Sang Hyun Lee
June Choi
Publication date: 15-02-2024
Publisher: Springer US
Published in: Journal of the Association for Research in Otolaryngology / Issue 2/2024
Print ISSN: 1525-3961
Electronic ISSN: 1438-7573
DOI: https://doi.org/10.1007/s10162-024-00936-3

At a glance: The STEP trials

Springer Medicine

Measuring Optokinetic Reflex and Vestibulo-Ocular Reflex in Unilateral Vestibular Organ Damage Model of Zebrafish

Abstract

At a glance: The STEP trials

Springer Medicine

Abstract

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