Skip to main content

Causes and Consequences of Sensory Hair Cell Damage and Recovery in Fishes

  • Chapter
Fish Hearing and Bioacoustics

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 877))

Abstract

Sensory hair cells are the mechanotransductive receptors that detect gravity, sound, and vibration in all vertebrates. Damage to these sensitive receptors often results in deficits in vestibular function and hearing. There are currently two main reasons for studying the process of hair cell loss in fishes. First, fishes, like other non-mammalian vertebrates, have the ability to regenerate hair cells that have been damaged or lost via exposure to ototoxic chemicals or acoustic overstimulation. Thus, they are used as a biomedical model to understand the process of hair cell death and regeneration and find therapeutics that treat or prevent human hearing loss. Secondly, scientists and governmental natural resource managers are concerned about the potential effects of intense anthropogenic sounds on aquatic organisms, including fishes. Dr. Arthur N. Popper and his students, postdocs and research associates have performed pioneering experiments in both of these lines of fish hearing research. This review will discuss the current knowledge regarding the causes and consequences of both lateral line and inner ear hair cell damage in teleost fishes.

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

Access this chapter

Chapter
USD 29.95
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 169.99
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

  • Aman A, Nguyen M, Piotrowski T (2011) Wnt/Beta-catenin dependent cell proliferation underlies segmented lateral line morphogenesis. Dev Biol 249:470–482

    Article  CAS  Google Scholar 

  • Amoser S, Ladich F (2003) Diversity in noise-induced temporary hearing loss in otophysine fishes. J Acoust Soc Am 113:2170–2179

    Article  PubMed  Google Scholar 

  • ASHA (2014) The American Speech-Language-Hearing Association (ASHA) register. http://www.asha.org. Accessed 10 July 2014

  • Baggeroer A, Munk W (1992) The Heard Island feasibility test. Phys Today 45:22–30

    Article  Google Scholar 

  • Bang PI, Sewell WF, Malicki JJ (2000) Behavioral screen for dominant mutations affecting zebrafish auditory system. Assoc Res Otolaryngol Abs 23:177–187

    Google Scholar 

  • Bang PI, Yelick PC, Malicki JJ et al (2002) High-throughput behavioral screening method for detection auditory response defects in zebrafish. J Neurosci Methods 118:177–187

    Article  PubMed  Google Scholar 

  • Barbazuk WB, Korf I, Kadavi C et al (2000) The syntenic relationship of zebrafish and human genomes. Genome Res 10:1351–1358

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Bhandiwad AA, Zeddies DG, Raible DW, Rubel EW, Sisneros JA (2013) Auditory sensitivity of larval zebrafish (Danio rerio) measured using a prepulse inhibition assay. J Exp Biol 216:3504–3513

    Article  PubMed Central  PubMed  Google Scholar 

  • Blaxter JA, Fuiman LA (1989) Function of the free neuromasts of marine teleost larvae. In: Coombs S, Gorner P, Munz H (eds) The mechanosensory lateral line. Springer, New York, pp 481–499

    Chapter  Google Scholar 

  • Boeger WA, Pie MR, Ostrensky A et al (2006) The effect of exposure to seismic prospecting on coral reef fishes. Braz J Oceanogr 54:235–239

    Article  Google Scholar 

  • Brown AD, Mussen TD, Sisneros JA et al (2011) Reevaluating the use of aminoglycoside antibiotics in behavioral studies of the lateral line. Hear Res 272:1–4

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Brown AD, Sisneros JA, Jurasin T et al (2013) Differences in lateral line morphology between hatchery- and wild-origin steelhead. PLoS One 8(3), e59162

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Bruintjes R, Radford AN (2013) Context-dependent impacts of anthropogenic noise on individual and social behavior in a cooperatively breeding fish. Anim Behav 85:1343–1349

    Article  Google Scholar 

  • Buck LM, Winter MJ, Redfern WS et al (2012) Ototoxin-induced cellular damage in neuromasts disrupts lateral line function in larval zebrafish. Hear Res 284:67–81

    Article  CAS  PubMed  Google Scholar 

  • Casper BM, Popper AN, Matthews F et al (2012) Recovery of barotrauma injuries in Chinook salmon, Oncorhynchus tshawytscha from exposure to pile driving sound. PLoS One 7, e39593

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Casper BM, Smith ME, Halvorsen MB et al (2013a) Effects of exposure to pile driving sounds on fish inner ear tissues. Comp Biochem Physiol A 166:352–360

    Article  CAS  Google Scholar 

  • Casper BM, Halvorsen MB, Mathews F et al (2013b) Recovery of barotrauma injuries resulting from exposure to pile driving sounds in two sizes of hybrid striped bass. PLoS One 8, e73844

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Cervi AL, Poling KR, Higgs DM (2012) Behavioral measure of frequency detection and discrimination in the zebrafish, Danio rerio. Zebrafish 9:1–7

    Article  PubMed  Google Scholar 

  • Cheng AG, Cunningham LL, Rubel EW (2003) Hair cell death in the avian basilar papilla: characterization of the in vivo model and caspase activation. J Assoc Res Otolaryngol 4:91–105

    Article  PubMed Central  PubMed  Google Scholar 

  • Cheng AG, Cunningham LL, Rubel EW (2005) Mechanisms of hair cell death and protection. Curr Opin Otolaryngol Head Neck Surg 13:343–348

    Article  PubMed  Google Scholar 

  • Chiu LL, Cunningham LL, Raible DW et al (2008) Using the zebrafish lateral line to screen for ototoxicity. J Assoc Res Otolaryngol 9:178–190

    Article  PubMed Central  PubMed  Google Scholar 

  • Coffey B (2014) Melanin as an oto-protective pigment in two fish species: Poecilia latipinna and Cyprinus carpio. Western Kentucky University, Master’s Thesis

    Google Scholar 

  • Coffin AB, Ramcharitar J (2015) Chemical ototoxicity of the fish inner ear and lateral line. In: Sisneros J (ed) Fish hearing and bioacoustics: an anthology in honor of Arthur N. Popper and Richard R. Fay. Springer, New York (this volume)

    Google Scholar 

  • Coffin AB, Kelley M, Manley GA et al (2004) Evolution of sensory hair cells. In: Manley GA, Popper AN, Fay RR (eds) Evolution of the vertebrate auditory system. Springer, New York, pp 55–94

    Chapter  Google Scholar 

  • Coffin AB, Reinhart KE, Owens KN et al (2009) Extracellular divalent cations modulate aminoglycoside-induced hair cell death in the zebrafish lateral line. Hear Res 253:42–51

    Article  CAS  PubMed  Google Scholar 

  • Coffin AB, Ou H, Owens KN et al (2010) Chemical screening for hair cell loss and protection in the zebrafish lateral line. Zebrafish 7:3–11

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Coffin AB, Rubel EW, Raible DW (2013) Bax, Bcl2, and p53 differentially regulate neomycin- and gentamicin-induced hair cell death in the zebrafish lateral line. J Assoc Res Otolaryngol 14:645–659

    Article  PubMed Central  PubMed  Google Scholar 

  • Coombs S (2001) Smart skins: information processing by lateral line flow sensors. Auton Robot 11:255–261

    Article  Google Scholar 

  • Coombs S, Braun CB, Donovan B (2001) The orienting response of Lake Michigan mottled sculpin is mediated by canal neuromasts. J Exp Biol 204:337–348

    CAS  PubMed  Google Scholar 

  • Corwin JT (1981) Postembryonic production and gaining in inner ear hair cells in sharks. J Comp Neurol 201:541–553

    Article  CAS  PubMed  Google Scholar 

  • Corwin JT (1983) Postembryonic growth of the macula neglecta auditory detector in the ray, Raja clavata: continual increases in hair cell number, neural convergence, and physiological sensitivity. J Comp Neurol 217:345–356

    Article  CAS  PubMed  Google Scholar 

  • Corwin JT, Bullock TH, Schweitzer J (1982) The auditory brainstem response in five vertebrate classes. Electroencephalogr Clin Neurophysiol 54:629–641

    Article  CAS  PubMed  Google Scholar 

  • Cunningham LL, Cheng AG, Rubel EW (2002) Caspase activation in hair cells of the mouse utricle exposed to neomycin. J Neurosci 22:8532–8540

    CAS  PubMed  Google Scholar 

  • Edds-Walton PL, Finneran JJ (2006) Evaluation of evidence for altered behavior and auditory deficits in fishes due to human-generated noise sources. Technical Report 1939, SPAWAR, Department of the Navy, San Diego, CA

    Google Scholar 

  • Enger PS (1981) Frequency discrimination in teleosts – central or peripheral? In: Tavolga WN, Popper AN, Fay RR (eds) Hearing and sound communication in fishes. Springer, New York

    Google Scholar 

  • 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  PubMed  Google Scholar 

  • Esterberg R, Coffin AB, Ou H et al (2013) Fish in a dish: drug discovery for hearing habilitation. Drug Discov Today Dis Models 10(1). doi:10.1016/j.ddmod.2012.02.001

    Google Scholar 

  • Faucher K, Aas-Hansen Ø, DamsgÃ¥rd B et al (2009) Damage and functional recovery of the Atlantic cod (Gadus morhua) inner ear hair cells following local injection of gentamicin. Int J Audiol 48:456–464

    Article  PubMed  Google Scholar 

  • Fay RR, Megela Simmons A (1999) The sense of hearing in fish and amphibians. In: Fay RR, Popper AN (eds) Comparative hearing: fish and amphibians. Springer, New York, pp 269–318

    Chapter  Google Scholar 

  • Fay RR, Popper AN (1999) Hearing in fishes and amphibians: an introduction. In: Fay RR, Popper AN (eds) Comparative hearing: fish and amphibians. Springer, New York, pp 1–14

    Chapter  Google Scholar 

  • Gerhard GS (2003) Comparative aspects of zebrafish (Danio rerio) as a model for aging research. Exp Gerontol 38:1333–1341

    Article  CAS  PubMed  Google Scholar 

  • Ghysen A, Dambly-Chaudière C (2004) Development of the zebrafish lateral line. Curr Opin Neurobiol 14:67–73

    Article  CAS  PubMed  Google Scholar 

  • Giari L, Dezfuli BS, Astolfi L et al (2012) Ultrastructural effects of cisplatin on the inner ear and lateral line system of zebrafish (Danio rerio) larvae. J Appl Toxicol 32:293–299

    Article  CAS  PubMed  Google Scholar 

  • Haehnel M, Taguchi M, Liao JC (2012) Heterogeneity and dynamics of lateral line afferent innervation. J Comp Neurol 520:1376–1386

    Article  PubMed Central  PubMed  Google Scholar 

  • Halvorsen MB, Casper BM, Woodley CM et al (2011) Predicting and mitigating hydroacoustic impacts on fish from pile installations. NCHRP Research Results Digest 363, Project 25–28, National Cooperative Highway Research Program, Transportation Research Board, National Academy of Sciences, Washington, DC

    Google Scholar 

  • Halvorsen MB, Casper BM, Woodley CM et al (2012a) Threshold for onset of injury in Chinook salmon from exposure to impulsive pile driving sounds. PLoS One 7, e38968

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Halvorsen MB, Casper BM, Matthews F et al (2012b) Effects of exposure to pile driving sounds on the lake sturgeon, Nile tilapia, and hogchoker. Proc R Soc B 279:4705–4714

    Article  PubMed Central  PubMed  Google Scholar 

  • Halvorsen MB, Zeddies DG, Ellison WT, Chicoine DR, Popper AN (2012c) Effects of mid-frequency active sonar on hearing in fish. J Acoust Soc Am 131:599–607

    Article  PubMed  Google Scholar 

  • Halvorsen MB, Zeddies DG, Chicoine DR, Popper AN (2013) Effects of low-frequency naval sonar exposure on three species of fish. J Acoust Soc Am 134:EL205–EL210

    Article  PubMed  Google Scholar 

  • Han Y, Mu Y, Li X et al (2011) Grhl2 deficiency impairs otic development and hearing ability in a zebrafish model of the progressive dominant hearing loss DFNA28. Hum Mol Genet 20:3213–3226

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed Central  PubMed  Google Scholar 

  • Hastings MC, Popper AN (2005) Effects of sound on fish. California Department of Transportation Contract 43A0139 Task Order, 1

    Google Scholar 

  • Hastings MC, Popper AN, Finneran JJ et al (1996) Effect of low frequency underwater sound on hair cells of the inner ear and lateral line of the teleost fish Astronotus ocellatus. J Acoust Soc Am 99:1759–1766

    Article  CAS  PubMed  Google Scholar 

  • Hawkins AD (1993) Underwater sound and fish behavior. In: Pitcher TJ (ed) Behaviour of teleost fishes. Chapman and Hall, London, pp 129–169

    Chapter  Google Scholar 

  • Hawkins AD, Rasmussen KJ (1978) The calls of gadoid fish. J Mar Biol Assoc UK 58:891–911

    Article  Google Scholar 

  • Hernández PP, Moreno V, Olivari FA et al (2006) Sub-lethal concentrations of waterborne copper are toxic to lateral line neuromasts in zebrafish (Danio rerio). Hear Res 213:1–10

    Article  PubMed  CAS  Google Scholar 

  • Hernández PP, Olivari FA, Sarrazin AF et al (2007) Regeneration in zebrafish lateral line neuromasts: expression of the neural progenitor cell marker sox2 and proliferation-dependent and-independent mechanisms of hair cell renewal. Dev Neurobiol 67:637–654

    Article  PubMed  CAS  Google Scholar 

  • Higgs DM, Radford CA (2013) The contribution of the lateral line to ‘hearing’ in fish. J Exp Biol 216:1484–1490

    Article  CAS  PubMed  Google Scholar 

  • Higgs DM, Rollo AK, Souza MJ et al (2003) Development of form and function in peripheral auditory structures of the zebrafish (Danio rerio). J Acoust Soc Am 113:1145–1154

    Article  PubMed  Google Scholar 

  • Hirose Y, Simon JA, Ou HC (2011) Hair cell toxicity in anti-cancer drugs: evaluating an anti-cancer drug library for independent and synergistic toxic effects on hair cells using the zebrafish lateral line. J Assoc Res Otolaryngol 12:719–728

    Article  PubMed Central  PubMed  Google Scholar 

  • Hulander M, Kiernan AT, Blomqvuist SR et al (2003) Lack of pendrin expression leads to deafness and expansion of the endolymphatic compartment in the inner ears of Foxi1 null mutant mice. Development 130:2013–2025

    Article  CAS  PubMed  Google Scholar 

  • Indzhykulian AA, Stepanyan R, Nelina A et al (2013) Molecular remodeling of tip links underlies mechanosensory regeneration in auditory hair cells. PLoS Biol 11(6), e1001583

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Janssen J (2000) Toxicity of Co2+: implications for lateral line studies. J Comp Physiol A 186:957–960

    Article  CAS  PubMed  Google Scholar 

  • Jiang H, Sha S-H, Forge A et al (2006) Caspase-independent pathways of hair cell death induced by kanamycin in vivo. Cell Death Differ 13:20–30

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kenyon TN, Ladich F, Yan HY (1998) A comparative study of hearing ability in fishes: the auditory brainstem approach. J Comp Physiol A 182:307–318

    Article  CAS  PubMed  Google Scholar 

  • Kim CH, Kang SU, Pyun J et al (2008) Epicatechin protects auditory cells against cisplatin-induced death. Apoptosis 13:1184–1194

    Article  CAS  PubMed  Google Scholar 

  • Ladich F (2000) Acoustic communication and the evolution of hearing in fishes. Philos Trans R Soc Lond 335:1285–1288

    Article  Google Scholar 

  • Ladich F, Bass A (1998) Sonic/vocal motor pathways in catfishes: comparisons with other teleosts. Brain Behav Evol 15:315–330

    Article  Google Scholar 

  • Ladich F, Bass A (2008) Vocal-acoustic communication: from behavior to neurons. In: Popper A, Fay R, Webb J (eds) Fish bioacoustics. Springer, New York, pp 253–278

    Google Scholar 

  • Ladich F, Fine ML (2003) Sound production, spine locking, and related adaptations. In: Ladich F, Collin SP, Moller P et al (eds) Catfishes, vol 1, Science Publishers. Inc, Entfield, pp 249–290

    Google Scholar 

  • Ladich F, Fine ML (2006) Sound-generating mechanisms in fishes: a unique diversity in vertebrates. In: Ladich F, Collin SP, Moller P et al (eds) Communication in fishes, vol 1, Science Publishers. Inc, Entfield, pp 3–43

    Google Scholar 

  • Ladich F, Wysocki LE (2003) How does tripus extirpation affect auditory sensitivity in goldfish? Hear Res 182:119–129

    Article  PubMed  Google Scholar 

  • Lagardère JP, Millot S, Parmentier E (2005) Aspects of sound communication in the pearlfish Carapus boraborensis and Carapus homei (Carapidae). J Exp Zool A Comp Exp Biol 303:1066–1074

    Article  PubMed  Google Scholar 

  • Lechner W, Heiss E, Schwaha T et al (2011) Ontogenetic development of Weberian ossicles and hearing abilities in the African bullhead catfish. PLoS One 6(4), e18511

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lin Q, Li W, Chen Y, Sun S, Li H (2013) Disrupting Rb-Raf-1 interaction inhibits hair cell regeneration in zebrafish lateral line neuromasts. Neuroreport 24:190–195

    Article  CAS  PubMed  Google Scholar 

  • Liu X-Z, Walsh J, Mburu P et al (1997) Mutations in the myosin VIIA gene cause non-syndromic recessive deafness. Nat Genet 16:188–190

    Article  CAS  PubMed  Google Scholar 

  • Lombarte A, Yan HY, Popper AN et al (1993) Damage and regeneration of hair cell ciliary bundles in a fish ear following treatment with gentamicin. Hear Res 64:1661–1674

    Article  Google Scholar 

  • Löwenheim H, Furness DN, Kil J et al (1999) Gene disruption of p27Kip1 allows cell proliferation in the postnatal and adult organ of Corti. Proc Natl Acad Sci U S A 96:4084–4088

    Article  PubMed Central  PubMed  Google Scholar 

  • Lush ME, Piotrowski T (2014) Sensory hair cell regeneration in the zebrafish lateral line. Dev Dyn 243:1187–1202

    Article  PubMed Central  PubMed  Google Scholar 

  • Ma EY, Rubel EW, Raible DW (2008) Notch signaling regulates the extent of hair cell regeneration in the zebrafish lateral line. J Neurosci 28:2261–2273

    Article  CAS  PubMed  Google Scholar 

  • Mackenzie SM, Raible DW (2012) Proliferative regeneration of zebrafish lateral line hair cells after different ototoxic insults. PLoS One 7, e47257

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Malicki J, Schier AF, Solnica-Krezel L et al (1996) Mutations affecting development of the zebrafish ear. Development 123:275–283

    CAS  PubMed  Google Scholar 

  • Mansour SL, Twigg SRF, Freeland RM et al (2009) Hearing loss in a mouse model of Muenke syndrome. Hum Mol Genet 18:43–50

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • McCauley RD, Fewtrell J, Popper AN (2003) High intensity anthropogenic sound damages fish ears. J Acoust Soc Am 113:1–5

    Article  Google Scholar 

  • McHenry MJ, van Netten SM (2007) The flexural stiffness of superficial neuromasts in the zebrafish (Danio rerio) lateral line. J Exp Biol 210:4244–4253

    Article  PubMed  Google Scholar 

  • McIver EL, Marchaterre MA, Rice AN, Bass AH (2014) Novel underwater soundscape: acoustic repertoire of plainfin midshipman fish. J Exp Biol 217:2377–2389

    Article  PubMed  Google Scholar 

  • Millimaki BB, Sweet EM, Riley BB (2010) Sox2 is required for maintenance and regeneration, but not initial development, of hair cells in the zebrafish inner ear. Dev Biol 338:262–269

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Montgomery JC, Baker CF, Carton AG (1997) The lateral line can mediate rheotaxis in fish. Nature 38:960–963

    Article  Google Scholar 

  • Murakami SL, Cunningham LL, Werner LA et al (2003) Developmental differences in susceptibility to neomycin-induced hair cell death in the lateral line neuromasts of zebrafish (Danio rerio). Hear Res 186:47–56

    Article  CAS  PubMed  Google Scholar 

  • Myrberg AA, Ha SJ, Shamblott MJ (1993) The sounds of bicolor damselfish (Pomacentrus partitus): predictors of body size and a spectral basis for individual recognition and assessment. J Acoust Soc Am 94:3067–3070

    Article  Google Scholar 

  • Nicolson T (2005) The genetics of hearing and balance in zebrafish. Annu Rev Genet 39:9–22

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Olivari FA, Hernández PP, Allende ML (2008) Acute copper exposure induces oxidative stress and cell death in lateral line hair cells of zebrafish larvae. Brain Res 1244:1–12

    Article  CAS  PubMed  Google Scholar 

  • Ou HC, Santos F, Raible DW et al (2006) c-Jun N-terminal kinase inhibition blocks aminoglycoside but not cisplatin-induced hair cell death in the zebrafish lateral line. Midwinter Research Meeting of the Association for Research in Otolaryngology

    Google Scholar 

  • Ou HC, Raible DW, Rubel EW (2007) Cisplatin-induced hair cell loss in zebrafish (Danio rerio) lateral line. Hear Res 233:46–53

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ou HC, Santos F, Raible DW et al (2010) Drug screening for hearing loss: using the zebrafish lateral line to screen for drugs that prevent and cause hearing loss. Drug Discov Today 15:265–271

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ou H, Simon JA, Rubel EW et al (2012) Screening for chemicals that affect hair cell death and survival in the zebrafish lateral line. Hear Res 288:58–66

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Owens KN, Santos F, Roberts B et al (2008) Identification of genetic and chemical modulators of zebrafish mechanosensory hair cell death. PLoS Genet 4(2), e1000020

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Parkes G, Hatton L (1986) The marine seismic source. D. Reidel Publishing Company, Dordrecht

    Book  Google Scholar 

  • Parmentier E, Lagardere JP, Vandewalle P, Fine ML (2005) Geographical variation in sound production in the anemonefish Amphiprion akkallopisos. Proc R Soc Lond B Biol Sci 272:1697–1703

    Article  CAS  Google Scholar 

  • Pickles JO (1996) An introduction to the physiology of hearing, 2nd edn. Academic, San Diego

    Google Scholar 

  • Pitcher T, Partridge B, Wardle C (1976) A blind fish can school. Science 194:963–965

    Article  CAS  PubMed  Google Scholar 

  • Popper AN, Clarke NL (1976) The auditory system of the goldfish (Carassius auratus): effects of intense acoustic stimulation. Comp Biochem Physiol A 53:11–18

    Article  CAS  PubMed  Google Scholar 

  • Popper AN, Fay RR (1999) The auditory periphery in fishes. In: Fay RR, Popper AN (eds) Comparative hearing: fish and amphibians. Springer, New York, pp 43–100

    Chapter  Google Scholar 

  • Popper AN, Fay RR (2011) Rethinking sound detection by fishes. Hear Res 273:25–36

    Article  PubMed  Google Scholar 

  • Popper AN, Hastings MC (2009) The effects of anthropogenic sources of sound on fishes. J Fish Biol 75:455–489

    Article  CAS  PubMed  Google Scholar 

  • Popper AN, Hoxter B (1984) Growth of a fish ear: I. Quantitative analysis of sensory hair cell and ganglion cell proliferation. Hear Res 15:133–142

    Article  CAS  PubMed  Google Scholar 

  • Popper AN, Fewtrell J, Smith ME et al (2004) Anthropogenic sound: effects on the behavior and physiology of fishes. Mar Technol Soc J 37:35–40

    Article  Google Scholar 

  • Popper AN, Smith ME, Cott PA et al (2005) Effects of exposure to seismic airgun use on hearing of three fish species. J Acoust Soc Am 117:3958–3971

    Article  PubMed  Google Scholar 

  • Popper AN, Halvorsen MB, Kane A et al (2007) The effects of high-intensity, low-frequency active sonar on rainbow trout. J Acoust Soc Am 122:623–635

    Article  PubMed  Google Scholar 

  • Purser J, Radford AN (2011) Acoustic noise induces attention shifts and reduces foraging performance in three-spined sticklebacks (Gasterosteus aculeatus). PLoS One 6, e17478

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Radford AN, Kerridge E, Simpson SD (2014) Acoustic communication in a noisy world: can fish compete with anthropogenic sound? Behav Ecol 00:1–9. doi:10.109/beheco/aru029

    Google Scholar 

  • Ramcharitar JU, Brack CL (2010) Physiological dimensions of ototoxic responses in a model fish species. J Clin Neurosci 17:103–106

    Article  CAS  PubMed  Google Scholar 

  • Ramcharitar JU, Selckmann GM (2010) Differential ablation of sensory receptors underlies ototoxin-induced shifts in auditory thresholds of the goldfish (Carassius auratus). J Appl Toxicol 30:536–541

    Article  CAS  PubMed  Google Scholar 

  • Richardson WJ, Green CR Jr, Malme CI et al (1995) Marine mammals and noise. Academic, New York

    Google Scholar 

  • Santos F, MacDonald G, Rubel EW et al (2006) Lateral line hair cell maturation is a determinant of aminoglycoside susceptibility in zebrafish (Danio rerio). Hear Res 213:25–33

    Article  CAS  PubMed  Google Scholar 

  • Scholik AR, Yan HY (2001) Effects of underwater noise on auditory sensitivity of a cyprinid fish. Hear Res 152:17–24

    Article  CAS  PubMed  Google Scholar 

  • Scholik AR, Yan HY (2002a) Effects of boat engine noise on the auditory sensitivity of the fathead minnow, Pimephales promelas. Environ Biol Fish 63:203–209

    Article  Google Scholar 

  • Scholik AR, Yan HY (2002b) The effects of noise on the auditory sensitivity of the bluegill sunfish, Lepomis macrochirus. Comp Biochem Physiol A 133:43–52

    Article  Google Scholar 

  • Schuck JB, Smith ME (2009) Cell proliferation follows acoustically-induced hair cell bundle loss in the zebrafish saccule. Hear Res 253:67–76

    Article  PubMed Central  PubMed  Google Scholar 

  • Schuck JB, Sun H, Penberthy WT et al (2011) Transcriptomic analysis of the zebrafish inner ear points to growth hormone mediated regeneration following acoustic trauma. BMC Neurosci 12:88

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Shin YS, Song SJ, Kang SU et al (2012) A novel synthetic compound, 3-amino-3-(4-fluoro-phenyl)-1H-quinoline-2,4-dione, inhibits cisplatin-induced hearing loss by the suppression of reactive oxygen species: in vitro and in vivo study. Neuroscience 14:1–12

    Google Scholar 

  • Skalski JR, Pearson WH, Malme CI (1992) Effects of sounds from a geophysical survey device on catch-per-unit-effort in a hook-and-line fishery for rockfish (Sebastes spp.). Can J Fish Aquat Sci 49:1357–1365

    Article  Google Scholar 

  • Slabbekoorn H, Bouton N, van Opzeeland I, Coers A et al (2010) A noisy spring: the impact of globally rising underwater sound levels on fish. Trends Ecol Evol 25:419–427

    Article  PubMed  Google Scholar 

  • Smith ME (2012) Predicting hearing loss in fishes. Adv Exp Med Biol 730:259–262

    Article  PubMed  Google Scholar 

  • Smith ME (2016) The relationship between hair cell loss and hearing loss in fishes. In: Popper AN, Hawkins A (eds) The Effects of Noise on Aquatic Life II. Advances in Experimental Medicine and Biology, Springer-Verlag, New York, pp. 1079–1086

    Google Scholar 

  • Smith ME, Fuiman LA (2004) Behavioral performance of wild-caught and laboratory-reared red drum Sciaenops ocellatus (Linnaeus) larvae. J Exp Mar Biol Ecol 302:17–33

    Article  Google Scholar 

  • Smith ME, Rajadinakaran G (2013) The transcriptomics to proteomics of hair cell regeneration: looking for a hair cell in a haystack. Microarrays 2:186–207

    Article  CAS  Google Scholar 

  • Smith ME, Kane AS, Popper AN (2004a) Noise-induced stress response and hearing loss in goldfish (Carassius auratus). J Exp Biol 207:427–435

    Article  PubMed  Google Scholar 

  • Smith ME, Kane AS, Popper AN (2004b) Acoustical stress and hearing sensitivity in fishes: does the linear threshold hypothesis hold water? J Exp Biol 207:3591–3602

    Article  PubMed  Google Scholar 

  • Smith ME, Coffin AB, Miller DL et al (2006) Anatomical and functional recovery of the goldfish (Carassius auratus) ear following noise exposure. J Exp Biol 209:4193–4202

    Article  PubMed  Google Scholar 

  • Smith ME, Schuck JB, Gilley RR et al (2011) Structural and functional effects of acoustic exposure in goldfish: evidence for tonotopy in the teleost saccule. BMC Neurosci 12:19

    Article  PubMed Central  PubMed  Google Scholar 

  • Söllner C, Rauch GJ, Siemens J et al (2004) Mutations in cadherin 23 affect tip links in zebrafish sensory hair cells. Nature 428:955–959

    Article  PubMed  CAS  Google Scholar 

  • Solomon KS, Kudoh T, Dawid IB et al (2003) Zebrafish foxi1 mediated otic placode formation and jaw development. Development 130:929–940

    Article  CAS  PubMed  Google Scholar 

  • Song J, Yan HY, Popper AN (1995) Damage and recovery of hair cells in fish canal (but not superficial) neuromasts after gentamicin exposure. Hear Res 91:63–71

    Article  CAS  PubMed  Google Scholar 

  • Song J, Mann DA, Cott PA, Hanna BW, Popper AN (2008) The inner ears of Northern Canadian freshwater fishes following exposure to seismic air gun sounds. J Acoust Soc Am 124:1360–1366

    Article  PubMed Central  PubMed  Google Scholar 

  • Tavolga WN (1971) Sound production and detection. In: Hoar WS, Randall DJ (eds) Fish physiology, vol 5. Academic, New York, pp 135–205

    Google Scholar 

  • Tavolga WN (1977) Mechanisms for directional hearing in the sea catfish (Arius felis). J Exp Biol 67:97–115

    CAS  PubMed  Google Scholar 

  • Thomas AJ, Hailey DW, Stawicki TM et al (2013) Functional mechanotransduction is required for cisplatin-induced hair cell death in the zebrafish lateral line. J Neurosci 33:4405–4414

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ton C, Parng C (2005) The use of zebrafish for assessing ototoxic and otoprotective agents. Hear Res 208:79–88

    Article  CAS  PubMed  Google Scholar 

  • Trapani JG, Nicolson T (2011) Mechanism of spontaneous activity in afferent neurons of the zebrafish lateral-line organ. J Neurosci 31:1614–1623

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Uribe PM, Mueller MA, Gleichman JS et al (2013a) Dimethyl sulfoxide (DMSO) exacerbates cisplatin-induced sensory hair cell death in zebrafish (Danio rerio). PLoS One 8(2), e55359

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Uribe PM, Sun H, Wang K et al (2013b) Aminoglycoside-induced hair cell death of inner ear organs causes functional deficits in adult zebrafish (Danio rerio). PLoS One 8(3), e58755

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Van Trump WJ, Coombs S, Duncan K et al (2010) Gentamicin is ototoxic to all hair cells in the fish lateral line system. Hear Res 261:42–50

    Article  PubMed  CAS  Google Scholar 

  • Vasconcelos RO, Fonseca PJ, Amorim MCP et al (2011) Representation of complex vocalizations in the Lusitanian toadfish auditory system: evidence of fine temporal, frequency and amplitude discrimination. Proc R Soc B 278:826–834

    Article  PubMed Central  PubMed  Google Scholar 

  • Verzijden MN, van Heusden J, Bouton N et al (2010) Sounds of male Lake Victoria cichlids vary within and between species and affect female mate preferences. Behav Ecol 21:548–555

    Article  Google Scholar 

  • Villegas R, Martin SM, O’Donnell KC et al (2012) Dynamics of degeneration and regeneration in developing zebrafish peripheral axons reveals a requirement for extrinsic cell types. Neural Dev 7:19. doi:10.1186/1749-8104-7-19

    Article  PubMed Central  PubMed  Google Scholar 

  • Vlasits AL, Simon JA, Raible DW et al (2012) Screen of FDA-approved drug library reveals compounds that protect hair cells from aminoglycosides and cisplatin. Hear Res 294:153–165

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wardle CS, Carter TJ, Urquhart GG (2001) Effects of seismic air guns on marine fish. Cont Shelf Res 21:1005–1027

    Article  Google Scholar 

  • Weber EH (1820) De Aure et Auditu Hominis et Animalium, Pars I. De Aure Animalium Aquatium, Leipzig

    Google Scholar 

  • Weiss SA, Zottoli SJ, Do SC et al (2006) Correlation of C-start behaviors with neural activity recorded from the hindbrain in free-swimming goldfish (Carassius auratus). J Exp Biol 209:4788–4801

    Article  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Whitfield TT, Riley BB, Chiang MY et al (2002) Development of the zebrafish inner ear. Dev Dyn 223:427–458

    Article  PubMed  Google Scholar 

  • Whitfield TT, Mburu P, Hardisty-Hughes RE et al (2005) Models of congenital deafness: mouse and zebrafish. Drug Discov Today Dis Models 2:85–92

    Article  CAS  Google Scholar 

  • Winn HE (1964) The biological significance of fish sounds. In: Tavolga WN (ed) Marine bio-acoustics, vol 2. Pergamon Press, New York, pp 213–231

    Google Scholar 

  • Wysocki LE, Ladich F (2005) Effects of noise exposure on click detection and the temporal resolution ability of the goldfish auditory system. Hear Res 201:27–36

    Article  PubMed  Google Scholar 

  • Wysocki LE, Dittami JP, Ladich F (2006) Ship noise and cortisol secretion in European freshwater fishes. Biol Conserv 128:501–508

    Article  Google Scholar 

  • Wysocki LE, Davidson JW, Smith ME et al (2007) Effects of aquaculture production noise on hearing, growth, and disease resistance of rainbow trout Onchohrynchus mykiss. Aquaculture 272:687–697

    Article  Google Scholar 

  • Yan HY (1998) Auditory role of the suprabranchial chamber in gourami fish. J Comp Physiol A 183:325–333

    Article  CAS  PubMed  Google Scholar 

  • Yan HY, Curtsinger WS (2000) The otic gasbladder as an ancillary structure in a mormyrid fish. J Comp Physiol A 186:595–600

    Article  CAS  PubMed  Google Scholar 

  • Yan HY, Saidel WM, Chang JS et al (1991) Sensory hair cells of the fish ear: evidence of multiple types based on ototoxicity sensitivity. Proc R Soc Lond B 245:133–138

    Article  CAS  Google Scholar 

  • Yan HY, Fine ML, Horn NS et al (2000) Variability in the role of the gasbladder in fish audition. J Comp Physiol A 186:435–445

    Article  CAS  PubMed  Google Scholar 

  • Zeddies DG, Fay RR (2005) Development of the acoustically evoked behavioral response in zebrafish to pure tones. J Exp Biol 208:1363–1372

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

The authors express their gratitude to both Arthur N. Popper and Richard R. Fay for their many years of exceptional research on fish hearing and bioacoustics and their leadership and mentoring in this field. MES thanks Art Popper for his first postdoctoral job and for the wise advice, friendship, and consummate mentoring at the University of Maryland, where the author began his career in fish hearing research and started examining the effects of sound on fishes. Art provided numerous career development opportunities to present research at conferences, to receive specific training, e.g., a course on Acoustic Communication in Denmark, to team-teach courses, to collaborate on broader lab projects, and to network with other researchers in the field of fish hearing. Of course, Dick Fay was one of those colleagues that Art introduced MES to and he is grateful for Dick’s advice on projects, particularly the work on the tonotopic organization of the goldfish saccule. MES thanks numerous undergraduate researchers, former graduate students Julie Schuck, Chia-Hui Lin, Yajie Wang, Gopinath Rajadinakaran, and Bethany Coffey, and former postdoctoral researchers Todd Penberthy and Huifang Sun, for their many hours of auditory evoked potential recordings and inner ear dissections to examine hair cell and hearing loss in fishes.

Research in the Smith lab was supported by the National Institute of General Medical Sciences of the NIH (P20 RR-16481, 8 P20 GM103436-12, 2 P20 GM103436-14), a Kentucky Science and Engineering Foundation Research & Development Excellence Grant (KSEF-148-502-14-325), and an NSF SOMAS Award (DUE-0426266). We thank Drs. Allison Coffin and Joseph Sisneros for helpful comments on an earlier draft of this manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Michael E. Smith .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2016 Springer International Publishing Switzerland

About this chapter

Cite this chapter

Smith, M.E., Monroe, J.D. (2016). Causes and Consequences of Sensory Hair Cell Damage and Recovery in Fishes. In: Sisneros, J. (eds) Fish Hearing and Bioacoustics. Advances in Experimental Medicine and Biology, vol 877. Springer, Cham. https://doi.org/10.1007/978-3-319-21059-9_17

Download citation

Publish with us

Policies and ethics