Skip to main content
SpringerLink
Log in

In Vivo Analysis of Hair Cell Sensory Organs in Zebrafish: From Morphology to Function

  • Protocol
  • First Online:
Developmental, Physiological, and Functional Neurobiology of the Inner Ear

Part of the book series: Neuromethods ((NM,volume 176))

Abstract

Hair cells are the sensory receptors of the vertebrate auditory and vestibular systems. In aquatic vertebrates, hair cells are present in the inner ear, where they are required for hearing and balance, and in the lateral line, where they detect fluid flow. In mammals, hair cell epithelia are embedded within a bony labyrinth in the skull, which makes access challenging for in vivo studies. In larval zebrafish, however, both inner ear and lateral line hair cells can be easily studied in vivo as they are present in accessible locations and in transparent tissue. In addition, zebrafish hair cells have remarkable genetic conservation with humans, and recent advances in reverse genetics have streamlined the process to generate novel zebrafish mutants. Thus, zebrafish are suitable models for studying the genetics underlying hearing and balance and contributing a mechanistic understanding of human sensorineural hearing loss. This methods chapter serves as a guide to creating and studying novel zebrafish mutants, covering a range of topics from zebrafish breeding and propagation to embryo microinjections for targeted mutagenesis (morpholino, CRISPR-Cas9, and tol2-based transgenesis). Once these mutants are created, we discuss ways to test auditory-vestibular phenotypes. We also outline several powerful in vivo methods to study inner ear and lateral line morphology, assess hair cell function, and examine subcellular structures within hair cells. We showcase several previously characterized zebrafish mutants that can be used as controls and exemplars (emx2, cdh23, pcdh15a, myo7aa, caV1.3a) for these approaches. Finally, we discuss recent in vivo advances being applied to study and manipulate hair cells with optogenetics techniques such as genetically-encoded indicators and actuators for functional studies.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Protocol
USD 49.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 249.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  1. Montgomery JC, Coombs SL (2017) Lateral line neuroethology. In: Reference module in life sciences. Elsevier. https://doi.org/10.1016/B978-0-12-809633-8.03040-5

  2. Haque KD, Pandey AK, Kelley MW, Puligilla C (2015) Culture of embryonic mouse cochlear explants and gene transfer by electroporation. J Vis Exp:e52260. https://doi.org/10.3791/52260

  3. Ogier JM, Burt RA, Drury HR et al (2019) Organotypic culture of neonatal murine inner ear explants. Front Cell Neurosci 13. https://doi.org/10.3389/fncel.2019.00170

  4. Kimmel CB (1989) Genetics and early development of zebrafish. Trends Genet 5:283–288. https://doi.org/10.1016/0168-9525(89)90103-0

    Article  CAS  PubMed  Google Scholar 

  5. Vaz RL, Outeiro TF, Ferreira JJ (2018) Zebrafish as an animal model for drug discovery in Parkinson’s disease and other movement disorders: a systematic review. Front Neurol 9:347. https://doi.org/10.3389/fneur.2018.00347

    Article  PubMed  PubMed Central  Google Scholar 

  6. Kimmel CB, Patterson J, Kimmel RO (1974) The development and behavioral characteristics of the startle response in the zebra fish. Dev Psychobiol 7:47–60. https://doi.org/10.1002/dev.420070109

    Article  CAS  PubMed  Google Scholar 

  7. 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/10.1186/1471-2202-11-110

    Article  PubMed  PubMed Central  Google Scholar 

  8. Suli A, Watson GM, Rubel EW, Raible DW (2012) Rheotaxis in larval zebrafish is mediated by lateral line mechanosensory hair cells. PLoS One 7. https://doi.org/10.1371/journal.pone.0029727

  9. Tanimoto M, Ota Y, Inoue M, Oda Y (2011) Origin of inner ear hair cells: morphological and functional differentiation from ciliary cells into hair cells in zebrafish inner ear. J Neurosci 31:3784–3794. https://doi.org/10.1523/JNEUROSCI.5554-10.2011

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Amsterdam A, Varshney G, Burgess S (2011) Retroviral-mediated insertional mutagenesis in zebrafish. Methods Cell Biol 104:59–82. https://doi.org/10.1016/B978-0-12-374814-0.00004-5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Bill BR, Petzold AM, Clark KJ et al (2009) A primer for morpholino use in zebrafish. Zebrafish 6:69–77. https://doi.org/10.1089/zeb.2008.0555

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Hoshijima K, Jurynec MJ, Klatt Shaw D et al (2019) Highly efficient CRISPR-Cas9-based methods for generating deletion mutations and F0 embryos that lack gene function in zebrafish. Dev Cell 51:645–657.e4. https://doi.org/10.1016/j.devcel.2019.10.004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Irion U, Krauss J, Nüsslein-Volhard C (2014) Precise and efficient genome editing in zebrafish using the CRISPR/Cas9 system. Development 141:4827–4830. https://doi.org/10.1242/dev.115584

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Kwan KM, Fujimoto E, Grabher C et al (2007) The Tol2kit: a multisite gateway-based construction kit for Tol2 transposon transgenesis constructs. Dev Dyn 236:3088–3099. https://doi.org/10.1002/dvdy.21343

    Article  CAS  PubMed  Google Scholar 

  15. Moens CB, Donn TM, Wolf-Saxon ER, Ma TP (2008) Reverse genetics in zebrafish by TILLING. Brief Funct Genomic Proteomic 7:454–459. https://doi.org/10.1093/bfgp/eln046

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Solnica-Krezel L, Schier AF, Driever W (1994) Efficient recovery of enu-induced mutations from the zebrafish germline. Genetics 136:1401–1420

    Article  CAS  Google Scholar 

  17. Varshney GK, Carrington B, Pei W et al (2016) A high-throughput functional genomics workflow based on CRISPR/Cas9-mediated targeted mutagenesis in zebrafish. Nat Protoc 11:2357–2375. https://doi.org/10.1038/nprot.2016.141

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Antonellis PJ, Pollock LM, Chou S-W et al (2014) ACF7 is a hair-bundle antecedent, positioned to integrate cuticular plate actin and somatic tubulin. J Neurosci 34:305–312. https://doi.org/10.1523/JNEUROSCI.1880-13.2014

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Erickson T, Morgan CP, Olt J et al (2017) Integration of Tmc1/2 into the mechanotransduction complex in zebrafish hair cells is regulated by Transmembrane O-methyltransferase (Tomt). eLife 6:e28474. https://doi.org/10.7554/eLife.28474

    Article  PubMed  PubMed Central  Google Scholar 

  20. Graydon CW, Manor U, Kindt KS (2017) In vivo ribbon mobility and turnover of ribeye at zebrafish hair cell synapses. Sci Rep 7:7467. https://doi.org/10.1038/s41598-017-07940-z

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Smith ET, Pacentine I, Shipman A et al (2020) Disruption of tmc1/2a/2b genes in zebrafish reveals subunit requirements in subtypes of inner ear hair cells. J Neurosci. https://doi.org/10.1523/JNEUROSCI.0163-20.2020

  22. Esterberg R, Hailey DW, Rubel EW, Raible DW (2014) ER–mitochondrial calcium flow underlies vulnerability of mechanosensory hair cells to damage. J Neurosci 34:9703–9719. https://doi.org/10.1523/JNEUROSCI.0281-14.2014

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Monesson-Olson BD, Browning-Kamins J, Aziz-Bose R et al (2014) Optical stimulation of zebrafish hair cells expressing channelrhodopsin-2. PLoS One 9. https://doi.org/10.1371/journal.pone.0096641

  24. Zhang Q, Li S, Wong H-TC et al (2018) Synaptically silent sensory hair cells in zebrafish are recruited after damage. Nat Commun 9:1388. https://doi.org/10.1038/s41467-018-03806-8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Ernest S, Rauch GJ, Haffter P et al (2000) Mariner is defective in myosin VIIA: a zebrafish model for human hereditary deafness. Hum Mol Genet 9:2189–2196

    Article  CAS  Google Scholar 

  26. Gleason MR, Nagiel A, Jamet S et al (2009) The transmembrane inner ear (Tmie) protein is essential for normal hearing and balance in the zebrafish. Proc Natl Acad Sci 106:21347–21352. https://doi.org/10.1073/pnas.0911632106

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Nicolson T, Rüsch A, Friedrich RW et al (1998) Genetic analysis of vertebrate sensory hair cell mechanosensation: the zebrafish circler mutants. Neuron 20:271–283

    Article  CAS  Google Scholar 

  28. Obholzer N, Wolfson S, Trapani JG et al (2008) Vesicular glutamate transporter 3 is required for synaptic transmission in zebrafish hair cells. J Neurosci 28:2110–2118. https://doi.org/10.1523/JNEUROSCI.5230-07.2008

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Seiler C, Finger-Baier KC, Rinner O et al (2005) Duplicated genes with split functions: independent roles of protocadherin15 orthologues in zebrafish hearing and vision. Dev Camb Engl 132:615–623. https://doi.org/10.1242/dev.01591

    Article  CAS  Google Scholar 

  30. Seiler C, Ben-David O, Sidi S et al (2004) Myosin VI is required for structural integrity of the apical surface of sensory hair cells in zebrafish. Dev Biol 272:328–338. https://doi.org/10.1016/j.ydbio.2004.05.004

    Article  CAS  PubMed  Google Scholar 

  31. Sidi S, Busch-Nentwich E, Friedrich R et al (2004) gemini encodes a zebrafish L-type calcium channel that localizes at sensory hair cell ribbon synapses. J Neurosci 24:4213–4223. https://doi.org/10.1523/JNEUROSCI.0223-04.2004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Söllner C, Rauch G-J, Siemens J et al (2004) Mutations in cadherin 23 affect tip links in zebrafish sensory hair cells. Nature 428:955–959. https://doi.org/10.1038/nature02484

    Article  CAS  PubMed  Google Scholar 

  33. Delmaghani S, Aghaie A, Bouyacoub Y et al (2016) Mutations in CDC14A, encoding a protein phosphatase involved in hair cell ciliogenesis, cause autosomal-recessive severe to profound deafness. Am J Hum Genet 98:1266–1270. https://doi.org/10.1016/j.ajhg.2016.04.015

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Riazuddin S, Belyantseva IA, Giese APJ et al (2012) Alterations of the CIB2 calcium- and integrin-binding protein cause Usher syndrome type 1J and nonsyndromic deafness DFNB48. Nat Genet 44:1265–1271. https://doi.org/10.1038/ng.2426

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Jiang T, Kindt K, Wu DK (2017) Transcription factor Emx2 controls stereociliary bundle orientation of sensory hair cells. eLife 6:e23661. https://doi.org/10.7554/eLife.23661

    Article  PubMed  PubMed Central  Google Scholar 

  36. Nicolson T (2005) The genetics of hearing and balance in zebrafish. Annu Rev Genet 39:9–22. https://doi.org/10.1146/annurev.genet.39.073003.105049

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

  38. Kwak S-J, Vemaraju S, Moorman SJ et al (2006) Zebrafish pax5 regulates development of the utricular macula and vestibular function. Dev Dyn 235:3026–3038. https://doi.org/10.1002/dvdy.20961

    Article  CAS  PubMed  Google Scholar 

  39. 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<329::aid-neu2>3.0.co;2-h

    Article  CAS  PubMed  Google Scholar 

  40. 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.00311.2004

    Article  PubMed  Google Scholar 

  41. Fay RR, Popper AN (2000) Evolution of hearing in vertebrates: the inner ears and processing. Hear Res 149:1–10. https://doi.org/10.1016/S0378-5955(00)00168-4

    Article  CAS  PubMed  Google Scholar 

  42. Ladich F, Schulz-Mirbach T (2016) Diversity in fish auditory systems: one of the riddles of sensory biology. Front Ecol Evol 4. https://doi.org/10.3389/fevo.2016.00028

  43. Faucher K, Parmentier E, Becco C et al (2010) Fish lateral system is required for accurate control of shoaling behaviour. Anim Behav 79:679–687. https://doi.org/10.1016/j.anbehav.2009.12.020

    Article  Google Scholar 

  44. McHenry MJ, Feitl KE, Strother JA, Van Trump WJ (2009) Larval zebrafish rapidly sense the water flow of a predator’s strike. Biol Lett 5:477–479. https://doi.org/10.1098/rsbl.2009.0048

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Mekdara PJ, Schwalbe MAB, Coughlin LL, Tytell ED (2018) The effects of lateral line ablation and regeneration in schooling giant danios. J Exp Biol 221. https://doi.org/10.1242/jeb.175166

  46. Olszewski J, Haehnel M, Taguchi M, Liao JC (2012) Zebrafish larvae exhibit rheotaxis and can escape a continuous suction source using their lateral line. PLoS One 7:e36661. https://doi.org/10.1371/journal.pone.0036661

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Kindt KS, Finch G, Nicolson T (2012) Kinocilia mediate mechanosensitivity in developing zebrafish hair cells. Dev Cell 23:329–341. https://doi.org/10.1016/j.devcel.2012.05.022

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Mackenzie SM, Raible DW (2012) Proliferative regeneration of zebrafish lateral line hair cells after different ototoxic insults. PLoS One 7:e47257. https://doi.org/10.1371/journal.pone.0047257

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Pickett SB, Thomas ED, Sebe JY et al (2018) Cumulative mitochondrial activity correlates with ototoxin susceptibility in zebrafish mechanosensory hair cells. eLife 7. https://doi.org/10.7554/eLife.38062

  50. Sheets L, He XJ, Olt J et al (2017) Enlargement of ribbons in zebrafish hair cells increases calcium currents but disrupts afferent spontaneous activity and timing of stimulus onset. J Neurosci 37:6299–6313. https://doi.org/10.1523/JNEUROSCI.2878-16.2017

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Trapani JG, Nicolson T (2011) Mechanism of spontaneous activity in afferent neurons of the zebrafish lateral-line organ. J Neurosci 31:1614–1623. https://doi.org/10.1523/JNEUROSCI.3369-10.2011

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Tilney LG, Tilney MS, DeRosier DJ (1992) Actin filaments, stereocilia, and hair cells: how cells count and measure. Annu Rev Cell Biol 8:257–274. https://doi.org/10.1146/annurev.cb.08.110192.001353

    Article  CAS  PubMed  Google Scholar 

  53. Hudspeth AJ, Corey DP (1977) Sensitivity, polarity, and conductance change in the response of vertebrate hair cells to controlled mechanical stimuli. Proc Natl Acad Sci U S A 74:2407–2411. https://doi.org/10.1073/pnas.74.6.2407

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Fettiplace R, Kim KX (2014) The physiology of mechanoelectrical transduction channels in hearing. Physiol Rev 94:951–986. https://doi.org/10.1152/physrev.00038.2013

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Puel J-L, Ladrech S, Chabert R et al (1991) Electrophysiological evidence for the presence of NMDA receptors in the guinea pig cochlea. Hear Res 51:255–264. https://doi.org/10.1016/0378-5955(91)90042-8

    Article  CAS  PubMed  Google Scholar 

  56. Ruel J, Emery S, Nouvian R et al (2008) Impairment of SLC17A8 encoding vesicular glutamate transporter-3, VGLUT3, underlies nonsyndromic deafness DFNA25 and inner hair cell dysfunction in null mice. Am J Hum Genet 83:278–292. https://doi.org/10.1016/j.ajhg.2008.07.008

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Safieddine S, Wenthold RJ (1997) The glutamate receptor subunit δ1 is highly expressed in hair cells of the auditory and vestibular systems. J Neurosci 17:7523–7531. https://doi.org/10.1523/JNEUROSCI.17-19-07523.1997

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Nicolson T (2015) Ribbon synapses in zebrafish hair cells. Hear Res 322. https://doi.org/10.1016/j.heares.2015.04.003

  59. Sterling P, Matthews G (2005) Structure and function of ribbon synapses. Trends Neurosci 28:20–29. https://doi.org/10.1016/j.tins.2004.11.009

    Article  CAS  PubMed  Google Scholar 

  60. Eatock RA, Lysakowski A (2006) Mammalian vestibular hair cells. In: Vertebrate hair cells. Springer, New York, NY, pp 348–442

    Chapter  Google Scholar 

  61. Burns JC, Kelly MC, Hoa M et al (2015) Single-cell RNA-Seq resolves cellular complexity in sensory organs from the neonatal inner ear. Nat Commun 6:8557. https://doi.org/10.1038/ncomms9557

    Article  CAS  PubMed  Google Scholar 

  62. Chen D-Y, Liu X-F, Lin X-J et al (2017) A dominant variant in DMXL2 is linked to nonsyndromic hearing loss. Genet Med 19:553–558. https://doi.org/10.1038/gim.2016.142

    Article  CAS  PubMed  Google Scholar 

  63. Ealy M, Ellwanger DC, Kosaric N et al (2016) Single-cell analysis delineates a trajectory toward the human early otic lineage. Proc Natl Acad Sci U S A 113:8508–8513. https://doi.org/10.1073/pnas.1605537113

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Gao X, Dai P (2014) Impact of next-generation sequencing on molecular diagnosis of inherited non-syndromic hearing loss. J Otol 9:122–125. https://doi.org/10.1016/j.joto.2014.11.003

    Article  Google Scholar 

  65. Kolla L, Kelly MC, Mann ZF et al (2020) Characterization of the development of the mouse cochlear epithelium at the single cell level. Nat Commun 11:2389. https://doi.org/10.1038/s41467-020-16113-y

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Morgan A, Vuckovic D, Krishnamoorthy N et al (2019) Next-generation sequencing identified SPATC1L as a possible candidate gene for both early-onset and age-related hearing loss. Eur J Hum Genet 27:70–79. https://doi.org/10.1038/s41431-018-0229-9

    Article  CAS  PubMed  Google Scholar 

  67. Ryu N, Lee S, Park H-J et al (2017) Identification of a novel splicing mutation within SLC17A8 in a Korean family with hearing loss by whole-exome sequencing. Gene 627:233–238. https://doi.org/10.1016/j.gene.2017.06.040

    Article  CAS  PubMed  Google Scholar 

  68. Scheffer DI, Shen J, Corey DP, Chen Z-Y (2015) Gene expression by mouse inner ear hair cells during development. J Neurosci 35:6366–6380. https://doi.org/10.1523/JNEUROSCI.5126-14.2015

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Vona B, Müller T, Nanda I et al (2014) Targeted next-generation sequencing of deafness genes in hearing-impaired individuals uncovers informative mutations. Genet Med 16:945–953. https://doi.org/10.1038/gim.2014.65

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Westerfield M (1995) The zebrafish book: a guide for the laboratory use of zebrafish (Danio rerio), 3rd edn. M. Westerfield

    Google Scholar 

  71. Maeda R, Kindt KS, Mo W et al (2014) Tip-link protein protocadherin 15 interacts with transmembrane channel-like proteins TMC1 and TMC2. Proc Natl Acad Sci U S A 111:12907–12912. https://doi.org/10.1073/pnas.1402152111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Postlethwait JH, Woods IG, Ngo-Hazelett P et al (2000) Zebrafish comparative genomics and the origins of vertebrate chromosomes. Genome Res 10:1890–1902. https://doi.org/10.1101/gr.164800

    Article  CAS  PubMed  Google Scholar 

  73. Lush ME, Diaz DC, Koenecke N et al (2019) scRNA-Seq reveals distinct stem cell populations that drive hair cell regeneration after loss of Fgf and Notch signaling. eLife 8:e44431. https://doi.org/10.7554/eLife.44431

    Article  PubMed  PubMed Central  Google Scholar 

  74. Créton R, Speksnijder JE, Jaffe LF (1998) Patterns of free calcium in zebrafish embryos. J Cell Sci 111(Pt 12):1613–1622

    Article  Google Scholar 

  75. Rosen JN, Sweeney MF, Mably JD (2009) Microinjection of Zebrafish embryos to analyze gene function. J Vis Exp. https://doi.org/10.3791/1115

  76. Xu Q (1999) Microinjection into Zebrafish embryos. In: Guille M (ed) Molecular methods in developmental biology: Xenopus and Zebrafish. Humana Press, Totowa, NJ, pp 125–132

    Chapter  Google Scholar 

  77. Kok FO, Shin M, Ni C-W et al (2015) Reverse genetic screening reveals poor correlation between morpholino-induced and mutant phenotypes in zebrafish. Dev Cell 32:97–108. https://doi.org/10.1016/j.devcel.2014.11.018

    Article  CAS  PubMed  Google Scholar 

  78. Stainier DYR, Raz E, Lawson ND et al (2017) Guidelines for morpholino use in zebrafish. PLoS Genet 13. https://doi.org/10.1371/journal.pgen.1007000

  79. Hwang WY, Fu Y, Reyon D et al (2013) Heritable and precise zebrafish genome editing using a CRISPR-Cas system. PLoS One 8:e68708. https://doi.org/10.1371/journal.pone.0068708

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Kim BH, Zhang G (2020) Generating stable knockout zebrafish lines by deleting large chromosomal fragments using multiple gRNAs. G3 10:1029–1037. https://doi.org/10.1534/g3.119.401035

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Varshney GK, Pei W, LaFave MC et al (2015) High-throughput gene targeting and phenotyping in zebrafish using CRISPR/Cas9. Genome Res 25:1030–1042. https://doi.org/10.1101/gr.186379.114

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Shah AN, Davey CF, Whitebirch AC et al (2015) Rapid reverse genetic screening using CRISPR in zebrafish. Nat Methods 12:535–540. https://doi.org/10.1038/nmeth.3360

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Buglo E, Sarmiento E, Martuscelli NB et al (2020) Genetic compensation in a stable slc25a46 mutant zebrafish: a case for using F0 CRISPR mutagenesis to study phenotypes caused by inherited disease. PLoS One 15:e0230566. https://doi.org/10.1371/journal.pone.0230566

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. El-Brolosy MA, Kontarakis Z, Rossi A et al (2019) Genetic compensation triggered by mutant mRNA degradation. Nature 568:193–197. https://doi.org/10.1038/s41586-019-1064-z

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Rossi A, Kontarakis Z, Gerri C et al (2015) Genetic compensation induced by deleterious mutations but not gene knockdowns. Nature 524:230–233. https://doi.org/10.1038/nature14580

    Article  CAS  PubMed  Google Scholar 

  86. Wilkie AO (1994) The molecular basis of genetic dominance. J Med Genet 31:89–98. https://doi.org/10.1136/jmg.31.2.89

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Hyatt TM, Ekker SC (1998) Chapter 8 vectors and techniques for ectopic gene expression in zebrafish. In: Detrich HW, Westerfield M, Zon LI (eds) Methods in cell biology. Academic, pp 117–126

    Google Scholar 

  88. Distel M, Hocking JC, Volkmann K, Köster RW (2010) The centrosome neither persistently leads migration nor determines the site of axonogenesis in migrating neurons in vivo. J Cell Biol 191:875–890. https://doi.org/10.1083/jcb.201004154

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Ernest S, Rosa FM (2015) A genomic region encompassing a newly identified exon provides enhancing activity sufficient for normal myo7aa expression in zebrafish sensory hair cells. Dev Neurobiol 75:961–983. https://doi.org/10.1002/dneu.22263

    Article  CAS  PubMed  Google Scholar 

  90. McDermott BM, Asai Y, Baucom JM et al (2010) Transgenic labeling of hair cells in the zebrafish acousticolateralis system. Gene Expr Patterns 10:113–118. https://doi.org/10.1016/j.gep.2010.01.001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Odermatt B, Nikolaev A, Lagnado L (2012) Encoding of luminance and contrast by linear and nonlinear synapses in the retina. Neuron 73:758–773. https://doi.org/10.1016/j.neuron.2011.12.023

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Xiao T, Roeser T, Staub W, Baier H (2005) A GFP-based genetic screen reveals mutations that disrupt the architecture of the zebrafish retinotectal projection. Development 132:2955–2967. https://doi.org/10.1242/dev.01861

    Article  CAS  PubMed  Google Scholar 

  93. Esain V, Postlethwait JH, Charnay P, Ghislain J (2010) FGF-receptor signalling controls neural cell diversity in the zebrafish hindbrain by regulating olig2 and sox9. Development 137:33–42. https://doi.org/10.1242/dev.038026

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Mandal A, Pinter K, Mosqueda N et al (2021) Retrograde mitochondrial transport is essential for organelle distribution and health in zebrafish neurons. J Neurosci 41(7):1371–1392

    Article  CAS  Google Scholar 

  95. Faucherre A, Pujol-Martí J, Kawakami K, López-Schier H (2009) Afferent neurons of the zebrafish lateral line are strict selectors of hair-cell orientation. PLoS One 4:e4477. https://doi.org/10.1371/journal.pone.0004477

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Mo W, Nicolson T (2011) Both pre- and postsynaptic activity of Nsf prevents degeneration of hair-cell synapses. PLoS One 6:e27146. https://doi.org/10.1371/journal.pone.0027146

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Baxendale S, Whitfield TT (2016) Chapter 6—methods to study the development, anatomy, and function of the zebrafish inner ear across the life course. In: Detrich HW, Westerfield M, Zon LI (eds) Methods in cell biology. Academic, pp 165–209

    Google Scholar 

  98. Swinburne IA, Mosaliganti KR, Upadhyayula S et al (2018) Lamellar projections in the endolymphatic sac act as a relief valve to regulate inner ear pressure. eLife 7:e37131. https://doi.org/10.7554/eLife.37131

    Article  PubMed  PubMed Central  Google Scholar 

  99. Zecca A, Dyballa S, Voltes A et al (2015) The order and place of neuronal differentiation establish the topography of sensory projections and the entry points within the hindbrain. J Neurosci 35:7475–7486. https://doi.org/10.1523/JNEUROSCI.3743-14.2015

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  100. Gale JE, Marcotti W, Kennedy HJ et al (2001) FM1-43 dye behaves as a permeant blocker of the hair-cell mechanotransducer channel. J Neurosci 21:7013–7025

    Article  CAS  Google Scholar 

  101. Meyers JR, MacDonald RB, Duggan A et al (2003) Lighting up the senses: FM1-43 loading of sensory cells through nonselective ion channels. J Neurosci 23:4054–4065

    Article  CAS  Google Scholar 

  102. Seiler C, Nicolson T (1999) Defective calmodulin-dependent rapid apical endocytosis in zebrafish sensory hair cell mutants. J Neurobiol 41:424–434. https://doi.org/10.1002/(SICI)1097-4695(19991115)41:3<424::AID-NEU10>3.0.CO;2-G

    Article  CAS  PubMed  Google Scholar 

  103. Erickson T, Pacentine IV, Venuto A et al (2020) The lhfpl5 Ohnologs lhfpl5a and lhfpl5b are required for mechanotransduction in distinct populations of sensory hair cells in zebrafish. Front Mol Neurosci 12. https://doi.org/10.3389/fnmol.2019.00320

  104. Pacentine IV, Nicolson T (2019) Subunits of the mechano-electrical transduction channel, Tmc1/2b, require Tmie to localize in zebrafish sensory hair cells. PLoS Genet 15:e1007635. https://doi.org/10.1371/journal.pgen.1007635

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  105. Hartwell RD, England SJ, Monk NAM et al (2019) Anteroposterior patterning of the zebrafish ear through Fgf- and Hh-dependent regulation of hmx3a expression. PLoS Genet 15:e1008051. https://doi.org/10.1371/journal.pgen.1008051

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  106. Monroe JD, Manning DP, Uribe PM et al (2016) Hearing sensitivity differs between zebrafish lines used in auditory research. Hear Res 341:220–231. https://doi.org/10.1016/j.heares.2016.09.004

    Article  PubMed  PubMed Central  Google Scholar 

  107. Thomas ED, Raible DW (2019) Distinct progenitor populations mediate regeneration in the zebrafish lateral line. eLife 8:e43736. https://doi.org/10.7554/eLife.43736

    Article  PubMed  PubMed Central  Google Scholar 

  108. Toro C, Trapani JG, Pacentine I et al (2015) Dopamine modulates the activity of sensory hair cells. J Neurosci 35:16494–16503. https://doi.org/10.1523/JNEUROSCI.1691-15.2015

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  109. Wada H, Ghysen A, Satou C et al (2010) Dermal morphogenesis controls lateral line patterning during postembryonic development of teleost fish. Dev Biol 340:583–594. https://doi.org/10.1016/j.ydbio.2010.02.017

    Article  CAS  PubMed  Google Scholar 

  110. Behra M, Gallardo VE, Bradsher J et al (2012) Transcriptional signature of accessory cells in the lateral line, using the Tnk1bp1:EGFP transgenic zebrafish line. BMC Dev Biol 12:6. https://doi.org/10.1186/1471-213X-12-6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  111. Higashijima S, Hotta Y, Okamoto H (2000) Visualization of cranial motor neurons in live transgenic zebrafish expressing green fluorescent protein under the control of the islet-1 promoter/enhancer. J Neurosci 20:206–218

    Article  CAS  Google Scholar 

  112. Nechiporuk A, Linbo T, Poss KD, Raible DW (2007) Specification of epibranchial placodes in zebrafish. Development 134:611–623. https://doi.org/10.1242/dev.02749

    Article  CAS  PubMed  Google Scholar 

  113. Haas P, Gilmour D (2006) Chemokine signaling mediates self-organizing tissue migration in the zebrafish lateral line. Dev Cell 10:673–680. https://doi.org/10.1016/j.devcel.2006.02.019

    Article  CAS  PubMed  Google Scholar 

  114. Geng F-S, Abbas L, Baxendale S et al (2013) Semicircular canal morphogenesis in the zebrafish inner ear requires the function of gpr126 (lauscher), an adhesion class G protein-coupled receptor gene. Development 140:4362–4374. https://doi.org/10.1242/dev.098061

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  115. Whitfield TT, Granato M, van Eeden FJ et al (1996) Mutations affecting development of the zebrafish inner ear and lateral line. Dev Camb Engl 123:241–254

    CAS  Google Scholar 

  116. Riley BB, Chiang M, Farmer L, Heck R (1999) The deltaA gene of zebrafish mediates lateral inhibition of hair cells in the inner ear and is regulated by pax2.1. Dev Camb Engl 126:5669–5678

    CAS  Google Scholar 

  117. Kozlowski DJ, Whitfield TT, Hukriede NA et al (2005) The zebrafish dog-eared mutation disrupts eya1, a gene required for cell survival and differentiation in the inner ear and lateral line. Dev Biol 277:27–41. https://doi.org/10.1016/j.ydbio.2004.08.033

    Article  CAS  PubMed  Google Scholar 

  118. Andermann P, Ungos J, Raible DW (2002) Neurogenin1 defines zebrafish cranial sensory ganglia precursors. Dev Biol 251:45–58. https://doi.org/10.1006/dbio.2002.0820

    Article  CAS  PubMed  Google Scholar 

  119. Hwang P, Chou S-W, Chen Z, McDermott BM (2015) The stereociliary paracrystal is a dynamic cytoskeletal scaffold in vivo. Cell Rep 13:1287–1294. https://doi.org/10.1016/j.celrep.2015.10.003

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  120. Pelassa I, Zhao C, Pasche M et al (2014) Synaptic vesicles are “primed” for fast clathrin-mediated endocytosis at the ribbon synapse. Front Mol Neurosci 7:91. https://doi.org/10.3389/fnmol.2014.00091

    Article  PubMed  PubMed Central  Google Scholar 

  121. Ohta S, Ji YR, Martin D, Wu DK (2020) Emx2 regulates hair cell rearrangement but not positional identity within neuromasts. eLife. https://elifesciences.org/articles/60432. Accessed 22 Jan 2021

  122. Blanco-Sánchez B, Clément A, Fierro J et al (2018) Grxcr1 promotes hair bundle development by destabilizing the physical interaction between harmonin and sans usher syndrome proteins. Cell Rep 25:1281–1291.e4. https://doi.org/10.1016/j.celrep.2018.10.005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  123. World Health Organization ( 2021) World report on hearing. https://apps.who.int/iris/handle/10665/339913. License: CCBY-NC-SA 3.0 IGO

  124. Gopal SR, Chen DH-C, Chou S-W et al (2015) Zebrafish models for the mechanosensory hair cell dysfunction in usher syndrome 3 reveal that clarin-1 is an essential hair bundle protein. J Neurosci 35:10188–10201. https://doi.org/10.1523/JNEUROSCI.1096-15.2015

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  125. Nagiel A, Andor-Ardó D, Hudspeth AJ (2008) Specificity of afferent synapses onto plane-polarized hair cells in the posterior lateral line of the zebrafish. J Neurosci 28:8442–8453. https://doi.org/10.1523/JNEUROSCI.2425-08.2008

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  126. Dow E, Jacobo A, Hossain S et al (2018) Connectomics of the zebrafish’s lateral-line neuromast reveals wiring and miswiring in a simple microcircuit. eLife 7:e33988. https://doi.org/10.7554/eLife.33988

    Article  PubMed  PubMed Central  Google Scholar 

  127. Jacobo A, Dasgupta A, Erzberger A et al (2019) Notch-mediated determination of hair-bundle polarity in mechanosensory hair cells of the zebrafish lateral line. Curr Biol 29:3579–3587.e7. https://doi.org/10.1016/j.cub.2019.08.060

    Article  CAS  PubMed  Google Scholar 

  128. Lozano-Ortega M, Valera G, Xiao Y et al (2018) Hair cell identity establishes labeled lines of directional mechanosensation. PLoS Biol 16:e2004404. https://doi.org/10.1371/journal.pbio.2004404

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  129. Navajas Acedo J, Voas MG, Alexander R et al (2019) PCP and Wnt pathway components act in parallel during zebrafish mechanosensory hair cell orientation. Nat Commun 10:3993. https://doi.org/10.1038/s41467-019-12005-y

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  130. Grisham RC, Kindt K, Finger-Baier K et al (2013) Mutations in ap1b1 cause mistargeting of the Na+/K+-ATPase pump in sensory hair cells. PLoS One 8:e60866. https://doi.org/10.1371/journal.pone.0060866

    Article  CAS  Google Scholar 

  131. Chou S-W, Chen Z, Zhu S et al (2017) A molecular basis for water motion detection by the mechanosensory lateral line of zebrafish. Nat Commun 8:1–16. https://doi.org/10.1038/s41467-017-01604-2

    Article  CAS  Google Scholar 

  132. Chatterjee P, Padmanarayana M, Abdullah N et al (2015) 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 35:1043–1054. https://doi.org/10.1128/MCB.01439-14

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  133. Einhorn Z, Trapani JG, Liu Q, Nicolson T (2012) Rabconnectin3α promotes stable activity of the H+ pump on synaptic vesicles in hair cells. J Neurosci 32:11144–11156. https://doi.org/10.1523/JNEUROSCI.1705-12.2012

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  134. Lin S, Vollrath MA, Mangosing S et al (2016) The zebrafish pinball wizard gene encodes WRB, a tail-anchored-protein receptor essential for inner-ear hair cells and retinal photoreceptors. J Physiol 594:895–914. https://doi.org/10.1113/JP271437

    Article  CAS  PubMed  Google Scholar 

  135. Lukasz D, Kindt KS (2018) In vivo calcium imaging of lateral-line hair cells in larval zebrafish. J Vis Exp. https://doi.org/10.3791/58794

  136. Trapani JG, Nicolson T (2010) Chapter 8—physiological recordings from zebrafish lateral-line hair cells and afferent neurons. In: William H, Detrich MW, Zon LI (eds) Methods in cell biology. Academic, pp 219–231

    Google Scholar 

  137. Olt J, Johnson SL, Marcotti W (2014) In vivo and in vitro biophysical properties of hair cells from the lateral line and inner ear of developing and adult zebrafish. J Physiol 592:2041–2058. https://doi.org/10.1113/jphysiol.2013.265108

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  138. Ricci AJ, Bai J-P, Song L et al (2013) Patch-clamp recordings from lateral line neuromast hair cells of the living zebrafish. J Neurosci 33:3131–3134. https://doi.org/10.1523/JNEUROSCI.4265-12.2013

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  139. Haehnel M, Taguchi M, Liao JC (2012) Heterogeneity and dynamics of lateral line afferent innervation during development in zebrafish (Danio rerio). J Comp Neurol 520:1376–1386. https://doi.org/10.1002/cne.22798

    Article  PubMed  PubMed Central  Google Scholar 

  140. Ohn T-L, Rutherford MA, Jing Z et al (2016) Hair cells use active zones with different voltage dependence of Ca2+ influx to decompose sounds into complementary neural codes. Proc Natl Acad Sci U S A 113(32):E4716–E4725. https://doi.org/10.1073/pnas.1605737113

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  141. Song S, Lee JA, Kiselev I et al (2018) Mathematical modeling and analyses of interspike-intervals of spontaneous activity in afferent neurons of the zebrafish lateral line. Sci Rep 8:14851. https://doi.org/10.1038/s41598-018-33064-z

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  142. Trapani JG, Obholzer N, Mo W et al (2009) Synaptojanin1 is required for temporal fidelity of synaptic transmission in hair cells. PLoS Genet 5:e1000480. https://doi.org/10.1371/journal.pgen.1000480

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  143. Furman AC, Kujawa SG, Liberman MC (2013) Noise-induced cochlear neuropathy is selective for fibers with low spontaneous rates. J Neurophysiol 110:577–586. https://doi.org/10.1152/jn.00164.2013

    Article  PubMed  PubMed Central  Google Scholar 

  144. Olt J, Ordoobadi AJ, Marcotti W, Trapani JG (2016) Physiological recordings from the zebrafish lateral line. Methods Cell Biol 133:253–279. https://doi.org/10.1016/bs.mcb.2016.02.004

    Article  CAS  PubMed  Google Scholar 

  145. Troconis EL, Ordoobadi AJ, Sommers TF et al (2017) Intensity-dependent timing and precision of startle response latency in larval zebrafish. J Physiol 595:265–282. https://doi.org/10.1113/JP272466

    Article  CAS  PubMed  Google Scholar 

  146. Zhang QX, He XJ, Wong HC, Kindt KS (2016) Functional calcium imaging in zebrafish lateral-line hair cells. Methods Cell Biol 133:229–252. https://doi.org/10.1016/bs.mcb.2015.12.002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  147. Smedemark-Margulies N, Trapani JG (2013) Tools, methods, and applications for optophysiology in neuroscience. Front Mol Neurosci 6. https://doi.org/10.3389/fnmol.2013.00018

  148. Esterberg R, Linbo T, Pickett SB et al (2016) Mitochondrial calcium uptake underlies ROS generation during aminoglycoside-induced hair cell death. J Clin Invest 126:3556–3566. https://doi.org/10.1172/JCI84939

    Article  PubMed  PubMed Central  Google Scholar 

  149. Wong HC, Zhang Q, Beirl AJ et al (2019) Synaptic mitochondria regulate hair-cell synapse size and function. eLife 8:e48914. https://doi.org/10.7554/eLife.48914

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  150. Pichler P, Lagnado L (2019) The transfer characteristics of hair cells encoding mechanical stimuli in the lateral line of zebrafish. J Neurosci 39:112–124. https://doi.org/10.1523/JNEUROSCI.1472-18.2018

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  151. Sheets L, Kindt KS, Nicolson T (2012) Presynaptic CaV1.3 channels regulate synaptic ribbon size and are required for synaptic maintenance in sensory hair cells. J Neurosci 32:17273–17286. https://doi.org/10.1523/JNEUROSCI.3005-12.2012

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  152. Bhandiwad AA, Zeddies DG, Raible DW et al (2013) Auditory sensitivity of larval zebrafish (Danio rerio) measured using a behavioral prepulse inhibition assay. J Exp Biol 216:3504–3513. https://doi.org/10.1242/jeb.087635

    Article  PubMed  PubMed Central  Google Scholar 

  153. Bang PI, Yelick PC, Malicki JJ, Sewell WF (2002) High-throughput behavioral screening method for detecting auditory response defects in zebrafish. J Neurosci Methods 118:177–187. https://doi.org/10.1016/s0165-0270(02)00118-8

    Article  PubMed  Google Scholar 

  154. Zottoli SJ, Faber DS (2000) Review: The mauthner cell: what has it taught us? Neuroscientist 6(1):26–38. https://doi.org/10.1177/107385840000600111

  155. Zeddies DG, Fay RR (2005) Development of the acoustically evoked behavioral response in zebrafish to pure tones. J Exp Biol 208:1363–1372. https://doi.org/10.1242/jeb.01534

    Article  PubMed  Google Scholar 

  156. Burgess HA, Granato M (2007) Sensorimotor gating in larval zebrafish. J Neurosci 27:4984–4994. https://doi.org/10.1523/JNEUROSCI.0615-07.2007

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  157. Friedrich T, Lambert AM, Masino MA, Downes GB (2012) Mutation of zebrafish dihydrolipoamide branched-chain transacylase E2 results in motor dysfunction and models maple syrup urine disease. Dis Model Mech 5:248–258. https://doi.org/10.1242/dmm.008383

    Article  CAS  PubMed  Google Scholar 

  158. Bagnall MW, Schoppik D (2018) Development of vestibular behaviors in zebrafish. Curr Opin Neurobiol 53:83–89. https://doi.org/10.1016/j.conb.2018.06.004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  159. Oteiza P, Odstrcil I, Lauder G et al (2017) A novel mechanism for mechanosensory-based rheotaxis in larval zebrafish. Nature 547:445–448. https://doi.org/10.1038/nature23014

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  160. Vanwalleghem G, Schuster K, Taylor MA et al (2020) Brain-wide mapping of water flow perception in zebrafish. J Neurosci 40:4130–4144. https://doi.org/10.1523/JNEUROSCI.0049-20.2020

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  161. Arnold GP, Weihs D (1978) The hydrodynamics of rheotaxis in the plaice (Pleuronectes Platessa L.). J Exp Biol 75:147–169

    Article  Google Scholar 

  162. Marsden KC, Jain RA, Wolman MA et al (2018) A Cyfip2-dependent excitatory interneuron pathway establishes the innate startle threshold. Cell Rep 23:878–887. https://doi.org/10.1016/j.celrep.2018.03.095

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  163. Lin JY (2011) A user’s guide to channelrhodopsin variants: features, limitations and future developments. Exp Physiol 96:19–25. https://doi.org/10.1113/expphysiol.2009.051961

    Article  PubMed  Google Scholar 

  164. Ozdemir YI, Hansen CA, Ramy MA et al (2021) Recording channelrhodopsin-evoked field potentials and startle responses from larval zebrafish. Methods Mol Biol 2191:201–220. https://doi.org/10.1007/978-1-0716-0830-2_13

    Article  CAS  PubMed  Google Scholar 

  165. Eaton RC, Farley RD (1975) Mauthner neuron field potential in newly hatched larvae of the zebra fish. J Neurophysiol 38:502–512. https://doi.org/10.1152/jn.1975.38.3.502

    Article  CAS  PubMed  Google Scholar 

  166. Prugh JI, Kimmel CB, Metcalfe WK (1982) Noninvasive recording of the Mauthner neurone action potential in larval zebrafish. J Exp Biol 101:83–92

    Article  CAS  Google Scholar 

  167. Zottoli SJ (1977) Correlation of the startle reflex and Mauthner cell auditory responses in unrestrained goldfish. J Exp Biol 66:243–254

    Article  CAS  Google Scholar 

  168. Liu KS, Fetcho JR (1999) Laser ablations reveal functional relationships of segmental hindbrain neurons in zebrafish. Neuron 23:325–335. https://doi.org/10.1016/S0896-6273(00)80783-7

    Article  CAS  PubMed  Google Scholar 

  169. Fetcho JR (1991) Spinal network of the mauthner cell (part 1 of 2). Brain Behav Evol 37:298–306. https://doi.org/10.1159/000114367

    Article  CAS  PubMed  Google Scholar 

  170. Issa FA, O’Brien G, Kettunen P et al (2011) Neural circuit activity in freely behaving zebrafish (Danio rerio). J Exp Biol 214:1028–1038. https://doi.org/10.1242/jeb.048876

    Article  PubMed  PubMed Central  Google Scholar 

  171. Monesson-Olson BD, Troconis EL, Trapani JG (2014) Recording field potentials from zebrafish larvae during escape responses. J Undergrad Neurosci Educ 13:A52–A58

    PubMed  PubMed Central  Google Scholar 

  172. Sun F, Zhou J, Dai B et al (2020) Next-generation GRAB sensors for monitoring dopaminergic activity in vivo. Nat Methods 17:1156–1166. https://doi.org/10.1038/s41592-020-00981-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  173. Jing M, Li Y, Zeng J et al (2020) An optimized acetylcholine sensor for monitoring in vivo cholinergic activity. Nat Methods 17:1139–1146. https://doi.org/10.1038/s41592-020-0953-2

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  174. Lunsford ET, Skandalis DA, Liao JC (2019) Efferent modulation of spontaneous lateral line activity during and after zebrafish motor commands. J Neurophysiol 122:2438–2448. https://doi.org/10.1152/jn.00594.2019

    Article  PubMed  PubMed Central  Google Scholar 

  175. Panzera LC, Hoppa MB (2019) Genetically encoded voltage indicators are illuminating subcellular physiology of the axon. Front Cell Neurosci 13. https://doi.org/10.3389/fncel.2019.00052

  176. Beck C, Zhang D, Gong Y (2019) Enhanced genetically encoded voltage indicators advance their applications in neuroscience. Curr Opin Biomed Eng 12:111–117. https://doi.org/10.1016/j.cobme.2019.10.010

    Article  PubMed  PubMed Central  Google Scholar 

  177. Power RM, Huisken J (2017) A guide to light-sheet fluorescence microscopy for multiscale imaging. Nat Methods 14:360–373. https://doi.org/10.1038/nmeth.4224

    Article  CAS  PubMed  Google Scholar 

  178. Abu-Siniyeh A, Al-Zyoud W (2020) Highlights on selected microscopy techniques to study zebrafish developmental biology. Lab Anim Res 36:12. https://doi.org/10.1186/s42826-020-00044-2

    Article  PubMed  PubMed Central  Google Scholar 

  179. Santi PA, Johnson SB, Hillenbrand M et al (2009) Thin-sheet laser imaging microscopy for optical sectioning of thick tissues. BioTechniques 46:287–294. https://doi.org/10.2144/000113087

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  180. Marques JC, Li M, Schaak D et al (2020) Internal state dynamics shape brainwide activity and foraging behaviour. Nature 577:239–243. https://doi.org/10.1038/s41586-019-1858-z

    Article  CAS  PubMed  Google Scholar 

  181. Bahl A, Engert F (2020) Neural circuits for evidence accumulation and decision making in larval zebrafish. Nat Neurosci 23:94–102. https://doi.org/10.1038/s41593-019-0534-9

    Article  CAS  PubMed  Google Scholar 

  182. Vanwalleghem GC, Ahrens MB, Scott EK (2018) Integrative whole-brain neuroscience in larval zebrafish. Curr Opin Neurobiol 50:136–145. https://doi.org/10.1016/j.conb.2018.02.004

    Article  CAS  PubMed  Google Scholar 

  183. Migault G, van der Plas TL, Trentesaux H et al (2018) Whole-brain calcium imaging during physiological vestibular stimulation in larval zebrafish. Curr Biol 28:3723–3735.e6. https://doi.org/10.1016/j.cub.2018.10.017

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  184. Favre-Bulle IA, Vanwalleghem G, Taylor MA et al (2018) Cellular-resolution imaging of vestibular processing across the larval zebrafish brain. Curr Biol 28:3711–3722.e3. https://doi.org/10.1016/j.cub.2018.09.060

    Article  CAS  PubMed  Google Scholar 

  185. Kindt KS, Sheets L (2018) Transmission disrupted: modeling auditory synaptopathy in zebrafish. Front Cell Dev Biol 6. https://doi.org/10.3389/fcell.2018.00114

  186. Owens KN, Cunningham DE, MacDonald G et al (2007) Ultrastructural analysis of aminoglycoside-induced hair cell death in the zebrafish lateral line reveals an early mitochondrial response. J Comp Neurol 502:522–543. https://doi.org/10.1002/cne.21345

    Article  CAS  PubMed  Google Scholar 

  187. Santos F, MacDonald G, Rubel EW, Raible DW (2006) Lateral line hair cell maturation is a determinant of aminoglycoside susceptibility in zebrafish (Danio rerio). Hear Res 213:25–33. https://doi.org/10.1016/j.heares.2005.12.009

    Article  CAS  PubMed  Google Scholar 

  188. Peterson HP, Troconis EL, Ordoobadi AJ et al (2018) Teaching dose-response relationships through aminoglycoside block of mechanotransduction channels in lateral line hair cells of larval zebrafish. J Undergrad Neurosci Educ 17:A40–A49

    PubMed  PubMed Central  Google Scholar 

  189. Kirshenbaum AP, Chabot E, Gibney N (2019) Startle, pre-pulse sensitization, and habituation in zebrafish. J Neurosci Methods 313:54–59. https://doi.org/10.1016/j.jneumeth.2018.12.017

    Article  PubMed  Google Scholar 

  190. Bhandiwad AA, Raible DW, Rubel EW, Sisneros JA (2018) Noise-induced hypersensitization of the acoustic startle response in larval zebrafish. J Assoc Res Otolaryngol 19:741–752. https://doi.org/10.1007/s10162-018-00685-0

    Article  PubMed  PubMed Central  Google Scholar 

  191. Best JD, Berghmans S, Hunt JJFG et al (2008) Non-associative learning in larval zebrafish. Neuropsychopharmacology 33:1206–1215. https://doi.org/10.1038/sj.npp.1301489

    Article  CAS  PubMed  Google Scholar 

  192. Pantoja C, Hoagland A, Carroll E et al (2017) Measuring behavioral individuality in the acoustic startle behavior in zebrafish. Bio-Protoc 7. https://doi.org/10.21769/BioProtoc.2200

  193. Faria M, Prats E, Novoa-Luna KA et al (2019) Development of a vibrational startle response assay for screening environmental pollutants and drugs impairing predator avoidance. Sci Total Environ 650:87–96. https://doi.org/10.1016/j.scitotenv.2018.08.421

    Article  CAS  PubMed  Google Scholar 

  194. Harris JA, Cheng AG, Cunningham LL et al (2003) Neomycin-induced hair cell death and rapid regeneration in the lateral line of zebrafish (Danio rerio). J Assoc Res Otolaryngol 4:219–234. https://doi.org/10.1007/s10162-002-3022-x

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

We acknowledge the following researchers for contributing images: Natalie Mosqueda (Fig. 6e–g), Katherine Pinter (Fig. 3a–c), and Candy Wong (Fig. 4c, d) and also Alisha Beirl for injecting the neurog1a morpholino (Fig. 6h, i). We thank Alma Jukic for her comments on the manuscript.

Funding

This work was supported by a National Institute on Deafness and Other Communication Disorders (NIDCD) Intramural Research Program Grant 1ZIADC000085-01 (K.S.K) and by a NIDCD NIH R15DC014843 award (J.G.T).

Author information

Authors and Affiliations

  1. Section on Sensory Cell Development and Function, National Institutes on Deafness and Other Communication Disorders, National Institutes of Health, Bethesda, MD, USA

    Saman Hussain, Roberto Aponte-Rivera & Katie S. Kindt

  2. Department of Biology and Neuroscience Program, Amherst College, Amherst, MA, USA

    Rana M. Barghout & Josef G. Trapani

Authors
  1. Saman Hussain
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Roberto Aponte-Rivera
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Rana M. Barghout
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Josef G. Trapani
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Katie S. Kindt
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Katie S. Kindt .

Editor information

Editors and Affiliations

  1. Department of Neuroscience, Baylor College of Medicine, Houston, TX, USA

    Andrew K. Groves

Rights and permissions

Reprints and permissions

Copyright information

© 2022 The Author(s), under exclusive license to Springer Science+Business Media, LLC, part of Springer Nature

About this protocol

Check for updates. Verify currency and authenticity via CrossMark

Cite this protocol

Hussain, S., Aponte-Rivera, R., Barghout, R.M., Trapani, J.G., Kindt, K.S. (2022). In Vivo Analysis of Hair Cell Sensory Organs in Zebrafish: From Morphology to Function. In: Groves, A.K. (eds) Developmental, Physiological, and Functional Neurobiology of the Inner Ear. Neuromethods, vol 176. Humana, New York, NY. https://doi.org/10.1007/978-1-0716-2022-9_9

Download citation

  • DOI: https://doi.org/10.1007/978-1-0716-2022-9_9

  • Published:

  • Publisher Name: Humana, New York, NY

  • Print ISBN: 978-1-0716-2021-2

  • Online ISBN: 978-1-0716-2022-9

  • eBook Packages: Springer Protocols

Publish with us

Policies and ethics

Search

Navigation