|
|
Behavioral methods for the functional assessment of hair cells in zebrafish |
Qin Yang1,2, Peng Sun3, Shi Chen4, Hongzhe Li5,6(), Fangyi Chen1() |
1. Department of Biology, South University of Science and Technology of China, Shenzhen 518000, China 2. Department of Basic Medicine, Wuhan University, Wuhan 430000, China 3. State Key Laboratory of Analog and Mixed-Signal VLSI, University of Macau, Macau, China 4. Key Laboratory of Combinatorial Biosynthesis and Drug Discovery, Ministry of Education, School of Pharmaceutical Sciences, and Medical Research Institute, Wuhan University, Wuhan 430072, China 5. Research Service, VA Loma Linda Healthcare System, Loma Linda, CA 92357, USA 6. Department of Otolaryngology – Head & Neck Surgery, Loma Linda University School of Medicine, Loma Linda, CA 92350, USA |
|
|
Abstract Zebrafish is an emerging animal model for studies on auditory system. This model presents high comparability with humans, good accessibility to the hearing organ, and high throughput capacity. To better utilize this animal model, methodologies need to be used to quantify the hearing function of the zebrafish. Zebrafish displays a series of innate and robust behavior related to its auditory function. Here, we reviewed the advantage of using zebrafish in auditory research and then introduced three behavioral tests, as follows: the startle response, the vestibular-ocular reflex, and rheotaxis. These tests are discussed in terms of their physiological characteristics, up-to-date technical development, and apparatus description. Test limitation and areas to improve are also introduced. Finally, we revealed the feasibility of these applications in zebrafish behavioral assessment and their potential in the high-throughput screening on hearing-related genes and drugs.
|
Keywords
zebrafish (Danio rerio)
behavior
auditory
startle response
vestibular-ocular reflex
rheotaxis
|
Corresponding Author(s):
Hongzhe Li,Fangyi Chen
|
Online First Date: 24 March 2017
Issue Date: 01 June 2017
|
|
1 |
He Y, Cai C, Tang D , Sun S, Li H. Effect of histone deacetylase inhibitors trichostatin A and valproic acid on hair cell regeneration in zebrafish lateral line neuromasts. Front Cell Neurosci 2014; 8: 382
https://doi.org/10.3389/fncel.2014.00382
pmid: 25431550
|
2 |
Shen X, Liu F, Wang Y , Wang H, Ma J, Xia W , Zhang J , Jiang N , Sun S, Wang X, Ma D . Down-regulation of msrb3 and destruction of normal auditory system development through hair cell apoptosis in zebrafish. Int J Dev Biol 2015; 59(4-6): 195–203
https://doi.org/10.1387/ijdb.140200md
pmid: 26505252
|
3 |
Stawicki TM, Esterberg R, Hailey DW , Raible DW , Rubel EW . Using the zebrafish lateral line to uncover novel mechanisms of action and prevention in drug-induced hair cell death. Front Cell Neurosci 2015; 9: 46
https://doi.org/10.3389/fncel.2015.00046
pmid: 25741241
|
4 |
Steiner AB, Kim T, Cabot V , Hudspeth AJ . Dynamic gene expression by putative hair-cell progenitors during regeneration in the zebrafish lateral line. Proc Natl Acad Sci USA 2014; 111(14): E1393–E1401
https://doi.org/10.1073/pnas.1318692111
pmid: 24706895
|
5 |
Zamora LY, Lu Z. Alcohol-induced morphological deficits in the development of octavolateral organs of the zebrafish (Danio rerio). Zebrafish 2013; 10(1): 52–61
https://doi.org/10.1089/zeb.2012.0830
pmid: 23461415
|
6 |
Duncan JS, Fritzsch B. Evolution of sound and balance perception: innovations that aggregate single hair cells into the ear and transform a gravistatic sensor into the organ of corti. Anat Rec (Hoboken) 2012; 295(11): 1760–1774
https://doi.org/10.1002/ar.22573
pmid: 23044863
|
7 |
Ou HC, Santos F, Raible DW , Simon JA , Rubel EW . Drug screening for hearing loss: using the zebrafish lateral line to screen for drugs that prevent and cause hearing loss. Drug Discov Today 2010; 15(7-8): 265–271
https://doi.org/10.1016/j.drudis.2010.01.001
pmid: 20096805
|
8 |
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 . The zebrafish reference genome sequence and its relationship to the human genome. Nature 2013; 496(7446): 498–503
https://doi.org/10.1038/nature12111
pmid: 23594743
|
9 |
Nicolson T. The genetics of hearing and balance in zebrafish. Annu Rev Genet 2005; 39(1): 9–22
https://doi.org/10.1146/annurev.genet.39.073003.105049
pmid: 16285850
|
10 |
Kanungo J, Cuevas E, Ali SF , Paule MG . Zebrafish model in drug safety assessment. Curr Pharm Des 2014; 20(34): 5416–5429
https://doi.org/10.2174/1381612820666140205145658
pmid: 24502596
|
11 |
Schibler A, Malicki J. A screen for genetic defects of the zebrafish ear. Mech Dev 2007; 124(7-8): 592–604
https://doi.org/10.1016/j.mod.2007.04.005
pmid: 17574823
|
12 |
Whitfield TT, Riley BB, Chiang MY , Phillips B . Development of the zebrafish inner ear. Dev Dyn 2002; 223(4): 427–458
https://doi.org/10.1002/dvdy.10073
pmid: 11921334
|
13 |
Ton C, Parng C. The use of zebrafish for assessing ototoxic and otoprotective agents. Hear Res 2005; 208(1-2): 79–88
https://doi.org/10.1016/j.heares.2005.05.005
pmid: 16014323
|
14 |
Tanimoto M, Ota Y, Horikawa K , Oda Y. Auditory input to CNS is acquired coincidentally with development of inner ear after formation of functional afferent pathway in zebrafish. J Neurosci 2009; 29(9): 2762–2767
https://doi.org/10.1523/JNEUROSCI.5530-08.2009
pmid: 19261871
|
15 |
Fritzsch B, Beisel KW. Evolution and development of the vertebrate ear. Brain Res Bull 2001; 55(6): 711–721
https://doi.org/10.1016/S0361-9230(01)00558-5
pmid: 11595355
|
16 |
Haden M, Einarsson R, Yazejian B . Patch clamp recordings of hair cells isolated from zebrafish auditory and vestibular end organs. Neuroscience 2013; 248: 79–87
https://doi.org/10.1016/j.neuroscience.2013.05.062
pmid: 23747350
|
17 |
Olt J, Johnson SL, Marcotti W . In vivo and in vitro biophysical properties of hair cells from the lateral line and inner ear of developing and adult zebrafish. J Physiol 2014; 592(10): 2041–2058
https://doi.org/10.1113/jphysiol.2013.265108
pmid: 24566541
|
18 |
Trapani JG, Nicolson T. Physiological recordings from zebrafish lateral-line hair cells and afferent neurons. Methods Cell Biol 2010; 100: 219–231
https://doi.org/10.1016/B978-0-12-384892-5.00008-6
pmid: 21111219
|
19 |
Trapani JG, Nicolson T. Mechanism of spontaneous activity in afferent neurons of the zebrafish lateral-line organ. J Neurosci 2011; 31(5): 1614–1623
https://doi.org/10.1523/JNEUROSCI.3369-10.2011
pmid: 21289170
|
20 |
Uribe PM, Sun H, Wang K , Asuncion JD , Wang Q, Chen CW, Steyger PS , Smith ME , Matsui JI . Aminoglycoside-induced hair cell death of inner ear organs causes functional deficits in adult zebrafish (Danio rerio). PLoS ONE 2013; 8(3): e58755
https://doi.org/10.1371/journal.pone.0058755
pmid: 23533589
|
21 |
Egner SA, Mann DA. Auditory sensitivity of sergeant major damselfish Abudefduf saxatilis from post-settlement juvenile to adult. Mar Ecol Prog Ser 2005; 285: 213–222
https://doi.org/10.3354/meps285213
|
22 |
Higgs DM, Rollo AK, Souza MJ , Popper AN . Development of form and function in peripheral auditory structures of the zebrafish (Danio rerio). J Acoust Soc Am 2003; 113(2): 1145–1154
https://doi.org/10.1121/1.1536185
pmid: 12597208
|
23 |
Lechner W, Heiss E, Schwaha T , Glösmann M , Ladich F . Ontogenetic development of weberian ossicles and hearing abilities in the African bullhead catfish. PLoS ONE 2011; 6(4): e18511
https://doi.org/10.1371/journal.pone.0018511
pmid: 21533262
|
24 |
Lechner W, Wysocki LE, Ladich F . Ontogenetic development of auditory sensitivity and sound production in the squeaker catfish Synodontis schoutedeni. BMC Biol 2010; 8(1): 10
https://doi.org/10.1186/1741-7007-8-10
pmid: 20113466
|
25 |
Vasconcelos RO, Ladich F. Development of vocalization, auditory sensitivity and acoustic communication in the Lusitanian toadfish Halobatrachus didactylus. J Exp Biol 2008; 211(Pt 4): 502–509
https://doi.org/10.1242/jeb.008474
pmid: 18245626
|
26 |
Bang PI, Sewell WF, Malicki JJ . Morphology and cell type heterogeneities of the inner ear epithelia in adult and juvenile zebrafish (Danio rerio). J Comp Neurol 2001; 438(2): 173–190
https://doi.org/10.1002/cne.1308
pmid: 11536187
|
27 |
Wang J, Song Q, Yu D , Yang G, Xia L, Su K , Shi H, Wang J, Yin S . Ontogenetic development of the auditory sensory organ in zebrafish (Danio rerio): changes in hearing sensitivity and related morphology. Sci Rep 2015; 5: 15943
https://doi.org/10.1038/srep15943
pmid: 26526229
|
28 |
Browning LM, Huang T, Xu XH . Real-time in vivo imaging of size-dependent transport and toxicity of gold nanoparticles in zebrafish embryos using single nanoparticle plasmonic spectroscopy. Interface Focus 2013; 3(3): 20120098
https://doi.org/10.1098/rsfs.2012.0098
pmid: 24427540
|
29 |
Pinto-Teixeira F, Muzzopappa M, Swoger J , Mineo A , Sharpe J , López-Schier H . Intravital imaging of hair-cell development and regeneration in the zebrafish. Front Neuroanat 2013; 7: 33
https://doi.org/10.3389/fnana.2013.00033
pmid: 24130521
|
30 |
Tanimoto M, Ota Y, Inoue M , Oda Y. Origin of inner ear hair cells: morphological and functional differentiation from ciliary cells into hair cells in zebrafish inner ear. J Neurosci 2011; 31(10): 3784–3794
https://doi.org/10.1523/JNEUROSCI.5554-10.2011
pmid: 21389233
|
31 |
Wolman M, Granato M. Behavioral genetics in larval zebrafish: learning from the young. Dev Neurobiol 2012; 72(3): 366–372
https://doi.org/10.1002/dneu.20872
pmid: 22328273
|
32 |
Raible DW, Kruse GJ. Organization of the lateral line system in embryonic zebrafish. J Comp Neurol 2000; 421(2): 189–198
https://doi.org/10.1002/(SICI)1096-9861(20000529)421:2<189::AID-CNE5>3.0.CO;2-K
pmid: 10813781
|
33 |
Niihori M, Platto T, Igarashi S , Hurbon A , Dunn AM , Tran P, Tran H, Mudery JA , Slepian MJ , Jacob A . Zebrafish swimming behavior as a biomarker for ototoxicity-induced hair cell damage: a high-throughput drug development platform targeting hearing loss. Transl Res 2015; 166(5): 440–450
https://doi.org/10.1016/j.trsl.2015.05.002
pmid: 26027789
|
34 |
McNeil PL, Boyle D, Henry TB , Handy RD , Sloman KA . Effects of metal nanoparticles on the lateral line system and behavior in early life stages of zebrafish (Danio rerio). Aquat Toxicol 2014; 152: 318–323
https://doi.org/10.1016/j.aquatox.2014.04.022
pmid: 24813264
|
35 |
Olszewski J, Haehnel M, Taguchi M , Liao JC . Zebrafish larvae exhibit rheotaxis and can escape a continuous suction source using their lateral line. PLoS ONE 2012; 7(5): e36661
https://doi.org/10.1371/journal.pone.0036661
pmid: 22570735
|
36 |
Olive R, Wolf S, Dubreuil A , Bormuth V , Debrégeas G , Candelier R . Rheotaxis of larval zebrafish: behavioral study of a multi-sensory process. Front Syst Neurosci 2016; 10: 14
https://doi.org/10.3389/fnsys.2016.00014
pmid: 26941620
|
37 |
Suli A, Watson GM, Rubel EW , Raible DW . Rheotaxis in larval zebrafish is mediated by lateral line mechanosensory hair cells. PLoS ONE 2012; 7(2): e29727
https://doi.org/10.1371/journal.pone.0029727
pmid: 22359538
|
38 |
Kimmel CB, Patterson J, Kimmel RO . The development and behavioral characteristics of the startle response in the zebrafish. Dev Psychobiol 1974; 7(1): 47–60
https://doi.org/10.1002/dev.420070109
pmid: 4812270
|
39 |
McElligott MB, O’malley DM. Prey tracking by larval zebrafish: axial kinematics and visual control. Brain Behav Evol 2005; 66(3): 177–196
https://doi.org/10.1159/000087158
pmid: 16088102
|
40 |
Burgess HA, Granato M. Modulation of locomotor activity in larval zebrafish during light adaptation. J Exp Biol 2007; 210(14): 2526–2539
https://doi.org/10.1242/jeb.003939
pmid: 17601957
|
41 |
Zeddies DG, Fay RR. Development of the acoustically evoked behavioral response in zebrafish to pure tones. J Exp Biol 2005; 208(7): 1363–1372
https://doi.org/10.1242/jeb.01534
pmid: 15781896
|
42 |
Nicolson T, Rüsch A, Friedrich RW , Granato M , Ruppersberg JP , Nüsslein-Volhard C . Genetic analysis of vertebrate sensory hair cell mechanosensation: the zebrafish circler mutants. Neuron 1998; 20(2): 271–283
https://doi.org/10.1016/S0896-6273(00)80455-9
pmid: 9491988
|
43 |
Chatterjee P, Padmanarayana M, Abdullah N , Holman CL , LaDu J, Tanguay RL, Johnson CP . Otoferlin deficiency in zebrafish results in defects in balance and hearing: rescue of the balance and hearing phenotype with full-length and truncated forms of mouse otoferlin. Mol Cell Biol 2015; 35(6): 1043–1054
https://doi.org/10.1128/MCB.01439-14
pmid: 25582200
|
44 |
Cervi AL, Poling KR, Higgs DM . Behavioral measure of frequency detection and discrimination in the zebrafish, Danio rerio. Zebrafish 2012; 9(1): 1–7
https://doi.org/10.1089/zeb.2011.0720
pmid: 22356697
|
45 |
Liu F, Xia W, Hu J , Wang Y, Yang F, Sun S , Zhang J , Jiang N , Wang H, Tian W, Wang X , Ma D. Solute carrier family 26 member a2 (slc26a2) regulates Otic development and hair cell survival in zebrafish. PLoS ONE 2015; 10(9): e0136832
https://doi.org/10.1371/journal.pone.0136832
pmid: 26375458
|
46 |
Higgs DM, Souza MJ, Wilkins HR , Presson JC , Popper AN . Age- and size-related changes in the inner ear and hearing ability of the adult zebrafish (Danio rerio). J Assoc Res Otolaryngol 2002; 3(2): 174–184
https://doi.org/10.1007/s101620020035
pmid: 12162367
|
47 |
Bang PI, Yelick PC, Malicki JJ , Sewell WF . High-throughput behavioral screening method for detecting auditory response defects in zebrafish. J Neurosci Methods 2002; 118(2): 177–187
https://doi.org/10.1016/S0165-0270(02)00118-8
pmid: 12204308
|
48 |
Go W, Bessarab D, Korzh V . atp2b1a regulates Ca(2+) export during differentiation and regeneration of mechanosensory hair cells in zebrafish. Cell Calcium 2010; 48(5): 302–313
https://doi.org/10.1016/j.ceca.2010.09.012
pmid: 21084119
|
49 |
Burgess HA, Granato M. Sensorimotor gating in larval zebrafish. J Neurosci 2007; 27(18): 4984–4994
https://doi.org/10.1523/JNEUROSCI.0615-07.2007
pmid: 17475807
|
50 |
Bhandiwad AA, Zeddies DG, Raible DW , Rubel EW , Sisneros JA . Auditory sensitivity of larval zebrafish (Danio rerio) measured using a behavioral prepulse inhibition assay. J Exp Biol 2013; 216(18): 3504–3513
https://doi.org/10.1242/jeb.087635
pmid: 23966590
|
51 |
Hedrick TL. Software techniques for two- and three-dimensional kinematic measurements of biological and biomimetic systems. Bioinspir Biomim 2008; 3(3): 034001
https://doi.org/10.1088/1748-3182/3/3/034001
pmid: 18591738
|
52 |
Neumeister H, Szabo TM, Preuss T . Behavioral and physiological characterization of sensorimotor gating in the goldfish startle response. J Neurophysiol 2008; 99(3): 1493–1502
https://doi.org/10.1152/jn.00959.2007
pmid: 18199818
|
53 |
Curtin PC, Preuss T. Glycine and GABAA receptors mediate tonic and phasic inhibitory processes that contribute to prepulse inhibition in the goldfish startle network. Front Neural Circuits 2015; 9: 12
https://doi.org/10.3389/fncir.2015.00012
pmid: 25852486
|
54 |
Ku Y, Ahn JW, Kwon C , Suh MW, Lee JH, Oh SH , Kim HC. Gap prepulse inhibition of the auditory late response in healthy subjects. Psychophysiology 2015; 52(11): 1511–1519
https://doi.org/10.1111/psyp.12507
pmid: 26272085
|
55 |
Maple AM, Smith KJ, Perna MK , Brown RW . Neonatal quinpirole treatment produces prepulse inhibition deficits in adult male and female rats. Pharmacol Biochem Behav 2015; 137: 93–100
https://doi.org/10.1016/j.pbb.2015.08.011
pmid: 26296939
|
56 |
Moyer CE, Erickson SL, Fish KN , Thiels E , Penzes P , Sweet RA . Developmental trajectories of auditory cortex synaptic structures and gap-prepulse inhibition of acoustic startle between early adolescence and young adulthood in mice. Cereb Cortex 2016; 26(5): 2115–2126
pmid: 25759333
|
57 |
Saletti PG, Maior RS, Hori E , Almeida RM , Nishijo H , Tomaz C . Whole-body prepulse inhibition protocol to test sensorymotor gating mechanisms in monkeys. PLoS ONE 2014; 9(8): e105551
https://doi.org/10.1371/journal.pone.0105551
pmid: 25144368
|
58 |
Dehmel S, Eisinger D, Shore SE . Gap prepulse inhibition and auditory brainstem-evoked potentials as objective measures for tinnitus in guinea pigs. Front Syst Neurosci 2012; 6: 42
https://doi.org/10.3389/fnsys.2012.00042
pmid: 22666193
|
59 |
Walter M, Tziridis K, Ahlf S , Schulze H . Context dependent auditory thresholds determined by brainstem audiometry and prepulse inhibition in Mongolian gerbils. Open Journal of Acoustics 2012; 2(01): 34–49
https://doi.org/10.4236/oja.2012.21004
|
60 |
Ernest S, Rosa FM. A genomic region encompassing a newly identified exon provides enhancing activity sufficient for normal myo7aa expression in zebrafish sensory hair cells. Dev Neurobiol 2015; 75(9): 961–983
https://doi.org/10.1002/dneu.22263
pmid: 25556989
|
61 |
Lappe-Osthege M, Talamo S, Helmchen C , Sprenger A . Overestimation of saccadic peak velocity recorded by electro-oculography compared to video-oculography and scleral search coil. Clin Neurophysiol 2010; 121(10): 1786–1787
https://doi.org/10.1016/j.clinph.2010.03.051
pmid: 20451445
|
62 |
Kimmel DL, Mammo D, Newsome WT . Tracking the eye non-invasively: simultaneous comparison of the scleral search coil and optical tracking techniques in the macaque monkey. Front Behav Neurosci 2012; 6: 49
https://doi.org/10.3389/fnbeh.2012.00049
pmid: 22912608
|
63 |
Moorman SJ, Burress C, Cordova R , Slater J . Stimulus dependence of the development of the zebrafish (Danio rerio) vestibular system. J Neurobiol 1999; 38(2): 247–258
https://doi.org/10.1002/(SICI)1097-4695(19990205)38:2<247::AID-NEU7>3.0.CO;2-3
pmid: 10022570
|
64 |
Easter SS Jr, Nicola GN. The development of eye movements in the zebrafish (Danio rerio). Dev Psychobiol 1997; 31(4): 267–276
https://doi.org/10.1002/(SICI)1098-2302(199712)31:4<267::AID-DEV4>3.0.CO;2-P
pmid: 9413674
|
65 |
Beck JC, Gilland E, Tank DW , Baker R . Quantifying the ontogeny of optokinetic and vestibuloocular behaviors in zebrafish, medaka, and goldfish. J Neurophysiol 2004; 92(6): 3546–3561
https://doi.org/10.1152/jn.00311.2004
pmid: 15269231
|
66 |
Mo W, Chen F, Nechiporuk A , Nicolson T . Quantification of vestibular-induced eye movements in zebrafish larvae. BMC Neurosci 2010; 11(1): 110
https://doi.org/10.1186/1471-2202-11-110
pmid: 20815905
|
67 |
Clemens Grisham R , Kindt K , Finger-Baier K , Schmid B , Nicolson T . Mutations in ap1b1 cause mistargeting of the Na(+)/K(+)-ATPase pump in sensory hair cells. PLoS ONE 2013; 8(4): e60866
https://doi.org/10.1371/journal.pone.0060866
pmid: 23593334
|
68 |
Lambert FM, Beck JC, Baker R , Straka H . Semicircular canal size determines the developmental onset of angular vestibuloocular reflexes in larval Xenopus. J Neurosci 2008; 28(32): 8086–8095
https://doi.org/10.1523/JNEUROSCI.1288-08.2008
pmid: 18685033
|
69 |
Sheets L, Trapani JG, Mo W , Obholzer N , Nicolson T . Ribeye is required for presynaptic Ca(V)1.3a channel localization and afferent innervation of sensory hair cells. Development 2011; 138(7): 1309–1319
https://doi.org/10.1242/dev.059451
pmid: 21350006
|
70 |
Bianco IH, Ma LH, Schoppik D , Robson DN , Orger MB , Beck JC , Li JM, Schier AF, Engert F , Baker R . The tangential nucleus controls a gravito-inertial vestibulo-ocular reflex. Curr Biol 2012; 22(14): 1285–1295
https://doi.org/10.1016/j.cub.2012.05.026
pmid: 22704987
|
71 |
Migliaccio AA, Schubert MC, Jiradejvong P , Lasker DM , Clendaniel RA , Minor LB . The three-dimensional vestibulo-ocular reflex evoked by high-acceleration rotations in the squirrel monkey. Exp Brain Res 2004; 159(4): 433–446
https://doi.org/10.1007/s00221-004-1974-2
pmid: 15349709
|
72 |
Moorman SJ, Cordova R, Davies SA . A critical period for functional vestibular development in zebrafish. Dev Dyn 2002; 223(2): 285–291
https://doi.org/10.1002/dvdy.10052
pmid: 11836792
|
73 |
Delcourt J, Becco C, Vandewalle N , Poncin P . A video multitracking system for quantification of individual behavior in a large fish shoal: advantages and limits. Behav Res Methods 2009; 41(1): 228–235
https://doi.org/10.3758/BRM.41.1.228
pmid: 19182144
|
74 |
Fontaine E, Lentink D, Kranenbarg S , Müller UK , van Leeuwen JL , Barr AH , Burdick JW . Automated visual tracking for studying the ontogeny of zebrafish swimming. J Exp Biol 2008; 211(8): 1305–1316
https://doi.org/10.1242/jeb.010272
pmid: 18375855
|
75 |
Pardo-Martin C, Chang TY, Koo BK , Gilleland CL , Wasserman SC , Yanik MF . High-throughput in vivo vertebrate screening. Nat Methods 2010; 7(8): 634–636
https://doi.org/10.1038/nmeth.1481
pmid: 20639868
|
76 |
Pulak R. Tools for automating the imaging of zebrafish larvae. Methods 2016; 96: 118–126
https://doi.org/10.1016/j.ymeth.2015.11.021
pmid: 26631716
|
77 |
Liu F, Yang F, Wen D , Xia W, Hao L, Hu J , Zong J, Shen X, Ma J , Jiang N , Sun S, Zhang J, Wang H , Wang X, Ma Z, Ma D . Grhl1 deficiency affects inner ear development in zebrafish. Int J Dev Biol 2015; 59(10-12): 417–423
https://doi.org/10.1387/ijdb.140230FL
pmid: 25896282
|
78 |
Goldfarb A, Avraham KB. Genetics of deafness: recent advances and clinical implications. J Basic Clin Physiol Pharmacol 2002; 13(2): 75–88
https://doi.org/10.1515/JBCPP.2002.13.2.75
pmid: 16411422
|
79 |
Sang Q, Zhang J, Feng R , Wang X, Li Q, Zhao X , Xing Q, Chen W, Du J , Sun S, Chai R, Liu D , Jin L, He L, Li H , Wang L. Ildr1b is essential for semicircular canal development, migration of the posterior lateral line primordium and hearing ability in zebrafish: implications for a role in the recessive hearing impairment DFNB42. Hum Mol Genet 2014; 23(23): 6201–6211
https://doi.org/10.1093/hmg/ddu340
pmid: 24990150
|
80 |
Harris JA, Cheng AG, Cunningham LL , MacDonald G , Raible DW , Rubel EW . Neomycin-induced hair cell death and rapid regeneration in the lateral line of zebrafish (Danio rerio). J Assoc Res Otolaryngol 2003; 4(2): 219–234
https://doi.org/10.1007/s10162-002-3022-x
pmid: 12943374
|
81 |
Akagi J, Khoshmanesh K, Evans B , Hall CJ , Crosier KE , Cooper JM , Crosier PS , Wlodkowic D . Miniaturized embryo array for automated trapping, immobilization and microperfusion of zebrafish embryos. PLoS ONE 2012; 7(5): e36630
https://doi.org/10.1371/journal.pone.0036630
pmid: 22606275
|
82 |
Lammer E, Kamp HG, Hisgen V , Koch M, Reinhard D, Salinas ER , Wendler K , Zok S, Braunbeck T. Development of a flow-through system for the fish embryo toxicity test (FET) with the zebrafish (Danio rerio). Toxicol In Vitro 2009; 23(7): 1436–1442
https://doi.org/10.1016/j.tiv.2009.05.014
pmid: 19486937
|
83 |
Ou H, Simon JA, Rubel EW , Raible DW . Screening for chemicals that affect hair cell death and survival in the zebrafish lateral line. Hear Res 2012; 288(1-2): 58–66
https://doi.org/10.1016/j.heares.2012.01.009
pmid: 22310494
|
84 |
Owens KN, Santos F, Roberts B , Linbo T , Coffin AB , Knisely AJ , Simon JA , Rubel EW , Raible DW . Identification of genetic and chemical modulators of zebrafish mechanosensory hair cell death. PLoS Genet 2008; 4(2): e1000020
https://doi.org/10.1371/journal.pgen.1000020
pmid: 18454195
|
85 |
Li P, White RM, Zon LI . Transplantation in zebrafish. Methods Cell Biol 2011; 105: 403–417
https://doi.org/10.1016/B978-0-12-381320-6.00017-5
pmid: 21951540
|
86 |
Brandt T. Modeling brain function: the vestibulo-ocular reflex. Curr Opin Neurol 2001; 14(1): 1–4
https://doi.org/10.1097/00019052-200102000-00001
pmid: 11176210
|
|
Viewed |
|
|
|
Full text
|
|
|
|
|
Abstract
|
|
|
|
|
Cited |
|
|
|
|
|
Shared |
|
|
|
|
|
Discussed |
|
|
|
|