Skip to main content
SpringerLink
Log in

The Development and Evolution of Lateral Line Electroreceptors: Insights from Comparative Molecular Approaches

  • Chapter
  • First Online:
Electroreception: Fundamental Insights from Comparative Approaches

Part of the book series: Springer Handbook of Auditory Research ((SHAR,volume 70))

Abstract

In the jawless lampreys, most nonteleost jawed fishes, and aquatic-stage amphibians, the lateral line system has a mechanosensory division responding to local water movement (“distant touch”) and an electrosensory division responding to low-frequency cathodal (exterior-negative) electric stimuli, such as the weak electric fields surrounding other animals. The electrosensory division was lost in the ancestors of teleost fishes and their closest relatives and in the ancestors of frogs and toads. However, anodally sensitive lateral line electroreception evolved independently at least twice within teleosts, most likely via modification of the mechanosensory division. This chapter briefly reviews this sensory system and describes our current understanding of the development of nonteleost lateral line electroreceptors, both in terms of their embryonic origin from lateral line placodes and at the molecular level. Gene expression analysis, using candidate genes and more recent unbiased transcriptomic (differential RNA sequencing) approaches, suggests a high degree of conservation between nonteleost electroreceptors and mechanosensory hair cells both in their development and in aspects of their physiology, including transmission mechanisms at the ribbon synapse. Taken together, these support the hypothesis that electroreceptors evolved in the vertebrate ancestor via the diversification of lateral line hair cells.

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

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 149.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Hardcover Book
USD 199.99
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

Similar content being viewed by others

References

  • Ahmed M, Wong EYM, Sun J, Xu J, Wang F, Xu P-X (2012) Eya1-Six1 interaction is sufficient to induce hair cell fate in the cochlea by activating Atoh1 expression in cooperation with Sox2. Dev Cell 22:377–390

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Amemiya F, Kishida R, Goris RC, Onishi H, Kusunoki T (1985) Primary vestibular projections in the hagfish, Eptatretus burgeri. Brain Res 337:73–79

    Article  CAS  PubMed  Google Scholar 

  • Andermann P, Ungos J, Raible DW (2002) Neurogenin1 defines zebrafish cranial sensory ganglia precursors. Dev Biol 251:45–58

    Article  CAS  PubMed  Google Scholar 

  • Arendt D, Musser JM, Baker CVH, Bergman A, Cepko C, Erwin DH, Pavlicev M, Schlosser G, Widder S, Laubichler MD, Wagner GP (2016) The origin and evolution of cell types. Nat Rev Genet 17:744–757

    Article  CAS  PubMed  Google Scholar 

  • Baker CVH, Modrell MS (2018) Insights into electroreceptor development and evolution from molecular comparisons with hair cells. Integr Comp Biol 58:329–340

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baker CVH, Modrell MS, Gillis JA (2013) The evolution and development of vertebrate lateral line electroreceptors. J Exp Biol 216:2515–2522

    Article  PubMed  Google Scholar 

  • Barry MA, White RL, Bennett MVL (1988) The elasmobranch spiracular organ. II. Physiological studies. J Comp Physiol A 163:93–98

    Article  CAS  PubMed  Google Scholar 

  • Becker L, Schnee ME, Niwa M, Sun W, Maxeiner S, Talaei S, Kachar B, Rutherford MA, Ricci AJ (2018) The presynaptic ribbon maintains vesicle populations at the hair cell afferent fiber synapse. eLife 7:e30241

    Article  PubMed  PubMed Central  Google Scholar 

  • Bedore CN, Kajiura SM (2013) Bioelectric fields of marine organisms: voltage and frequency contributions to detectability by electroreceptive predators. Physiol Biochem Zool 86:298–311

    Article  PubMed  Google Scholar 

  • Bell CC, Maler L (2005) Central neuroanatomy of electrosensory systems in fish. In: Bullock TH, Hopkins CD, Popper AN, Fay RR (eds) Electroreception. Springer, New York, pp 68–111

    Chapter  Google Scholar 

  • Bell C, Bodznick D, Montgomery J, Bastian J (1997) The generation and subtraction of sensory expectations within cerebellum-like structures. Brain Behav Evol 50(Suppl 1):17–31

    Article  PubMed  Google Scholar 

  • Bellono NW, Leitch DB, Julius D (2017) Molecular basis of ancestral vertebrate electroreception. Nature 543:391–396

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bellono NW, Leitch DB, Julius D (2018) Molecular tuning of electroreception in sharks and skates. Nature 558:122–126

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bennett MVL, Obara S (1986) Ionic mechanisms and pharmacology of electroreceptors. In: Bullock TH, Heiligenberg W (eds) Electroreception. Wiley, New York, pp 157–181

    Google Scholar 

  • Betancur-R R, Wiley EO, Arratia G, Acero A, Bailly N, Miya M, Lecointre G, Ortí G (2017) Phylogenetic classification of bony fishes. BMC Evol Biol 17:162

    Article  PubMed  PubMed Central  Google Scholar 

  • Bodznick D (1989) Comparisons between electrosensory and mechanosensory lateral line systems. In: Coombs S, Görner P, Münz H (eds) The Mechanosensory lateral line. Neurobiology and evolution. Springer, New York, pp 655–678

    Google Scholar 

  • Bodznick D, Montgomery JC (2005) The physiology of low-frequency electrosensory systems. In: Bullock TH, Hopkins CD, Popper AN, Fay RR (eds) Electroreception. Springer, New York, pp 132–153

    Chapter  Google Scholar 

  • Bodznick D, Preston DG (1983) Physiological characterization of electroreceptors in the lampreys Ichthyomyzon unicuspis and Petromyzon marinus. J Comp Physiol A 152:209–217

    Article  Google Scholar 

  • Braun CB (1996) The sensory biology of the living jawless fishes: a phylogenetic assessment. Brain Behav Evol 48:262–276

    Article  CAS  PubMed  Google Scholar 

  • Braun CB, Northcutt RG (1997) The lateral line system of hagfishes (Craniata: Myxinoidea). Acta Zool (Stockh) 78:247–268

    Article  Google Scholar 

  • Bullock TH, Bodznick DA, Northcutt RG (1983) The phylogenetic distribution of electroreception: evidence for convergent evolution of a primitive vertebrate sense modality. Brain Res Rev 287:25–46

    Article  CAS  Google Scholar 

  • Burighel P, Caicci F, Manni L (2011) Hair cells in non-vertebrate models: lower chordates and molluscs. Hear Res 273:14–24

    Article  CAS  PubMed  Google Scholar 

  • Carrisoza-Gaytán R, Wang L, Schreck C, Kleyman TR, Wang W-H, Satlin LM (2017) The mechanosensitive BKα/β1 channel localizes to cilia of principal cells in rabbit cortical collecting duct (CCD). Am J Physiol Renal Physiol 312:F143–F156

    Article  PubMed  CAS  Google Scholar 

  • Chagnaud BP, Coombs S (2014) Information encoding and processing by the peripheral lateral line system. In: Coombs SC, Bleckmann H, Fay RR, Popper AN (eds) The lateral line system. Springer, New York, pp 151–194

    Google Scholar 

  • Costa A, Powell LM, Lowell S, Jarman AP (2017) Atoh1 in sensory hair cell development: constraints and cofactors. Semin Cell Dev Biol 65:60–68

    Article  CAS  PubMed  Google Scholar 

  • Cunningham CL, Müller U (2019) Molecular structure of the hair cell mechanoelectrical transduction complex. Cold Spring Harb Perspect Med 9:a033167

    Article  PubMed  PubMed Central  Google Scholar 

  • Czech-Damal NU, Dehnhardt G, Manger P, Hanke W (2013) Passive electroreception in aquatic mammals. J Comp Physiol A 199:555–563

    Article  Google Scholar 

  • Dabdoub A, Puligilla C, Jones JM, Fritzsch B, Cheah KS, Pevny LH, Kelley MW (2008) Sox2 signaling in prosensory domain specification and subsequent hair cell differentiation in the developing cochlea. Proc Natl Acad Sci U S A 105:18396–18401

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dai W, Zou M, Yang L, Du K, Chen W, Shen Y, Mayden RL, He S (2018) Phylogenomic perspective on the relationships and evolutionary history of the major otocephalan lineages. Sci Rep 8:205

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Dalle Nogare D, Chitnis AB (2017) A framework for understanding morphogenesis and migration of the zebrafish posterior lateral line primordium. Mech Dev 148:69–78

    Article  CAS  PubMed  Google Scholar 

  • DeCaen PG, Delling M, Vien TN, Clapham DE (2013) Direct recording and molecular identification of the calcium channel of primary cilia. Nature 504:315–318

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Delgado R, Saavedra MV, Schmachtenberg O, Sierralta J, Bacigalupo J (2003) Presence of Ca2+−dependent K+ channels in chemosensory cilia support a role in odor transduction. J Neurophysiol 90:2022–2028

    Article  CAS  PubMed  Google Scholar 

  • Delling M, DeCaen PG, Doerner JF, Febvay S, Clapham DE (2013) Primary cilia are specialized calcium signalling organelles. Nature 504:311–314

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dijkgraaf S (1963) The functioning and significance of the lateral-line organs. Biol Rev 38:51–105

    Article  CAS  PubMed  Google Scholar 

  • Dow E, Jacobo A, Hossain S, Siletti K, Hudspeth AJ (2018) Connectomics of the zebrafish’s lateral-line neuromast reveals wiring and miswiring in a simple microcircuit. eLife 7:e33988

    Article  PubMed  PubMed Central  Google Scholar 

  • Ebeid M, Sripal P, Pecka J, Beisel KW, Kwan K, Soukup GA (2017) Transcriptome-wide comparison of the impact of Atoh1 and miR-183 family on pluripotent stem cells and multipotent otic progenitor cells. PLoS One 12:e0180855

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Elkon R, Milon B, Morrison L, Shah M, Vijayakumar S, Racherla M, Leitch CC, Silipino L, Hadi S, Weiss-Gayet M, Barras E, Schmid CD, Ait-Lounis A, Barnes A, Song Y, Eisenman DJ, Eliyahu E, Frolenkov GI, Strome SE, Durand B, Zaghloul NA, Jones SM, Reith W, Hertzano R (2015) RFX transcription factors are essential for hearing in mice. Nat Commun 6:8549

    Article  CAS  PubMed  Google Scholar 

  • Fettiplace R, Fuchs PA (1999) Mechanisms of hair cell tuning. Annu Rev Physiol 61:809–834

    Article  CAS  PubMed  Google Scholar 

  • Fields RD, Bullock TH, Lange GD (1993) Ampullary sense organs, peripheral, central and behavioral electroreception in chimeras (Hydrolagus, Holocephali, Chondrichthyes). Brain Behav Evol 41:269–289

    Article  CAS  PubMed  Google Scholar 

  • Flock Å (1965) Transducing mechanisms in the lateral line canal organ receptors. Cold Spring Harb Symp Quant Biol 30:133–145

    Article  CAS  PubMed  Google Scholar 

  • Flowers GP, Crews CM (2015) Generating and identifying axolotls with targeted mutations using Cas9 RNA-guided nuclease. Methods Mol Biol 1290:279–295

    Article  PubMed  Google Scholar 

  • Fritzsch B, Elliott KL (2017) Gene, cell, and organ multiplication drives inner ear evolution. Dev Biol 431:3–15

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gelman S, Ayali A, Tytell ED, Cohen AH (2007) Larval lampreys possess a functional lateral line system. J Comp Physiol A 193:271–277

    Article  CAS  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 

  • Gibbs MA, Northcutt RG (2004a) Development of the lateral line system in the shovelnose sturgeon. Brain Behav Evol 64:70–84

    Article  PubMed  Google Scholar 

  • Gibbs MA, Northcutt RG (2004b) Retinoic acid repatterns axolotl lateral line receptors. Int J Dev Biol 48:63–66

    Article  CAS  PubMed  Google Scholar 

  • Gillis JA, Modrell MS, Northcutt RG, Catania KC, Luer CA, Baker CVH (2012) Electrosensory ampullary organs are derived from lateral line placodes in cartilaginous fishes. Development 139:3142–3146

    Article  CAS  PubMed  Google Scholar 

  • Gilmour D, Knaut H, Maischein HM, Nüsslein-Volhard C (2004) Towing of sensory axons by their migrating target cells in vivo. Nat Neurosci 7:491–492

    Article  CAS  PubMed  Google Scholar 

  • Hams N, Padmanarayana M, Qiu W, Johnson CP (2017) Otoferlin is a multivalent calcium-sensitive scaffold linking SNAREs and calcium channels. Proc Natl Acad Sci U S A 114:8023–8028

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Haque A, Engel J, Teichmann SA, Lönnberg T (2017) A practical guide to single-cell RNA-sequencing for biomedical research and clinical applications. Genome Med 9:75

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hatakeyama J, Kageyama R (2004) Retinal cell fate determination and bHLH factors. Semin Cell Dev Biol 15:83–89

    Article  CAS  PubMed  Google Scholar 

  • Heller S, Bell AM, Denis CS, Choe Y, Hudspeth AJ (2002) Parvalbumin 3 is an abundant Ca2+ buffer in hair cells. J Assoc Res Otolaryngol 3:488–498

    Article  PubMed  PubMed Central  Google Scholar 

  • Hertzano R, Dror AA, Montcouquiol M, Ahmed ZM, Ellsworth B, Camper S, Friedman TB, Kelley MW, Avraham KB (2007) Lhx3, a LIM domain transcription factor, is regulated by Pou4f3 in the auditory but not in the vestibular system. Eur J Neurosci 25:999–1005

    Article  PubMed  Google Scholar 

  • Holder N, Hill J (1991) Retinoic acid modifies development of the midbrain-hindbrain border and affects cranial ganglion formation in zebrafish embryos. Development 113:1159–1170

    CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jahan I, Pan N, Kersigo J, Fritzsch B (2010) Neurod1 suppresses hair cell differentiation in ear ganglia and regulates hair cell subtype development in the cochlea. PLoS One 5:e11661

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Jean P, Lopez de la Morena D, Michanski S, Jaime Tobón LM, Chakrabarti R, Picher MM, Neef J, Jung S, Gültas M, Maxeiner S, Neef A, Wichmann C, Strenzke N, Grabner C, Moser T (2018) The synaptic ribbon is critical for sound encoding at high rates and with temporal precision. eLife 7:e29275

    Article  PubMed  PubMed Central  Google Scholar 

  • Jørgensen JM (1982) Fine structure of the ampullary organs of the bichir Polypterus senegalus Cuvier, 1829 (Pisces: Brachiopterygii) with some notes on the phylogenetic development of electroreceptors. Acta Zool (Stockh) 63:211–217

    Article  Google Scholar 

  • Jørgensen JM (2005) Morphology of electroreceptive sensory organs. In: Bullock TH, Hopkins CD, Popper AN, Fay RR (eds) Electroreception. Springer, New York, pp 47–67

    Chapter  Google Scholar 

  • Jørgensen JM (2011) Morphology of electroreceptive sensory organs. In: Farrell AP (ed) Encyclopedia of fish physiology: from genome to environment. Academic, San Diego, pp 350–358

    Chapter  Google Scholar 

  • Kirschbaum F, Denizot J-P (2011) Development of electroreceptors and electric organs. In: Farrell AP (ed) Encyclopedia of fish physiology: from genome to environment. Academic, San Diego

    Google Scholar 

  • Kniss JS, Jiang L, Piotrowski T (2016) Insights into sensory hair cell regeneration from the zebrafish lateral line. Curr Opin Genet Dev 40:32–40

    Article  CAS  PubMed  Google Scholar 

  • Köster RW, Kühnlein RP, Wittbrodt J (2000) Ectopic Sox3 activity elicits sensory placode formation. Mech Dev 95:175–187

    Article  PubMed  Google Scholar 

  • Lavoué S, Miya M, Arnegard ME, Sullivan JP, Hopkins CD, Nishida M (2012) Comparable ages for the independent origins of electrogenesis in African and south American weakly electric fishes. PLoS One 7:e36287

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • López-Schier H, Starr CJ, Kappler JA, Kollmar R, Hudspeth AJ (2004) Directional cell migration establishes the axes of planar polarity in the posterior lateral-line organ of the zebrafish. Dev Cell 7:401–412

    Article  PubMed  Google Scholar 

  • Lu X, Sipe CW (2016) Developmental regulation of planar cell polarity and hair-bundle morphogenesis in auditory hair cells: lessons from human and mouse genetics. WIREs Dev Biol 5:85–101

    Article  Google Scholar 

  • Lv C, Stewart WJ, Akanyeti O, Frederick C, Zhu J, Santos-Sacchi J, Sheets L, Liao JC, Zenisek D (2016) Synaptic ribbons require Ribeye for electron density, proper synaptic localization, and recruitment of calcium channels. Cell Rep 15:2784–2795

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Maxeiner S, Luo F, Tan A, Schmitz F, Südhof TC (2016) How to make a synaptic ribbon: RIBEYE deletion abolishes ribbons in retinal synapses and disrupts neurotransmitter release. EMBO J 35:1098–1114

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McCormick CA (1982) The organization of the octavolateralis area in actinopterygian fishes: a new interpretation. J Morphol 171:159–181

    Article  PubMed  Google Scholar 

  • Metscher BD, Northcutt RG, Gardiner DM, Bryant SV (1997) Homeobox genes in axolotl lateral line placodes and neuromasts. Dev Genes Evol 207:287–295

    Article  CAS  PubMed  Google Scholar 

  • Michalski N, Goutman JD, Auclair SM, Boutet de Monvel J, Tertrais M, Emptoz A, Parrin A, Nouaille S, Guillon M, Sachse M, Ciric D, Bahloul A, Hardelin JP, Sutton RB, Avan P, Krishnakumar SS, Rothman JE, Dulon D, Safieddine S, Petit C (2017) Otoferlin acts as a Ca(2+) sensor for vesicle fusion and vesicle pool replenishment at auditory hair cell ribbon synapses. eLife 6:e31013

    Article  PubMed  PubMed Central  Google Scholar 

  • Millimaki BB, Sweet EM, Dhason MS, Riley BB (2007) Zebrafish atoh1 genes: classic proneural activity in the inner ear and regulation by Fgf and Notch. Development 134:295–305

    Article  CAS  PubMed  Google Scholar 

  • Modrell MS, Baker CVH (2012) Evolution of electrosensory ampullary organs: conservation of Eya4 expression during lateral line development in jawed vertebrates. Evol Dev 14:277–285

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Modrell MS, Bemis WE, Northcutt RG, Davis MC, Baker CVH (2011) Electrosensory ampullary organs are derived from lateral line placodes in bony fishes. Nat Commun 2:496

    Article  PubMed  CAS  Google Scholar 

  • Modrell MS, Hockman D, Uy B, Buckley D, Sauka-Spengler T, Bronner ME, Baker CVH (2014) A fate-map for cranial sensory ganglia in the sea lamprey. Dev Biol 385:405–416

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Modrell MS, Lyne M, Carr AR, Zakon HH, Buckley D, Campbell AS, Davis MC, Micklem G, Baker CVH (2017a) Insights into electrosensory organ development, physiology and evolution from a lateral line-enriched transcriptome. eLife 6:e24197

    Article  PubMed  PubMed Central  Google Scholar 

  • Modrell MS, Tidswell ORA, Baker CVH (2017b) Notch and Fgf signaling during electrosensory versus mechanosensory lateral line organ development in a non-teleost ray-finned fish. Dev Biol 431:48–58

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Montgomery J, Bleckmann H, Coombs S (2014) Sensory ecology and neuroethology of the lateral line. In: Coombs SC, Bleckmann H, Fay RR, Popper AN (eds) The lateral line system. Springer, New York, pp 121–150

    Google Scholar 

  • Münz H, Claas B, Fritzsch B (1984) Electroreceptive and mechanoreceptive units in the lateral line of the axolotl Ambystoma mexicanum. J Comp Physiol A 154:33–44

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Neef J, Gehrt A, Bulankina AV, Meyer AC, Riedel D, Gregg RG, Strenzke N, Moser T (2009) The Ca2+ channel subunit beta2 regulates Ca2+ channel abundance and function in inner hair cells and is required for hearing. J Neurosci 29:10730–10740

    Article  CAS  PubMed  Google Scholar 

  • Nicolson T (2015) Ribbon synapses in zebrafish hair cells. Hear Res 330:170–177

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nicolson T (2017) The genetics of hair-cell function in zebrafish. J Neurogenet 31:102–112

    Article  PubMed  PubMed Central  Google Scholar 

  • Nikaido M, Doi K, Shimizu T, Hibi M, Kikuchi Y, Yamasu K (2007) Initial specification of the epibranchial placode in zebrafish embryos depends on the fibroblast growth factor signal. Dev Dyn 236:564–571

    Article  CAS  PubMed  Google Scholar 

  • Nikaido M, Acedo JN, Hatta K, Piotrowski T (2017) Retinoic acid is required and Fgf, Wnt, and Bmp signaling inhibit posterior lateral line placode induction in zebrafish. Dev Biol 431:215–225

    Article  CAS  PubMed  Google Scholar 

  • Northcutt RG (2005a) Ontogeny of electroreceptors and their neural circuitry. In: Bullock TH, Hopkins CD, Popper AN, Fay RR (eds) Electroreception. Springer, New York, pp 112–131

    Chapter  Google Scholar 

  • Northcutt RG (2005b) The New Head Hypothesis revisited. J Exp Zool B Mol Dev Evol 304B:274–297

    Google Scholar 

  • Northcutt RG, Catania KC, Criley BB (1994) Development of lateral line organs in the axolotl. J Comp Neurol 340:480–514

    Article  CAS  PubMed  Google Scholar 

  • Northcutt RG, Brändle K, Fritzsch B (1995) Electroreceptors and mechanosensory lateral line organs arise from single placodes in axolotls. Dev Biol 168:358–373

    Article  CAS  PubMed  Google Scholar 

  • O’Neill P, McCole RB, Baker CVH (2007) A molecular analysis of neurogenic placode and cranial sensory ganglion development in the shark, Scyliorhinus canicula. Dev Biol 304:156–181

    Article  PubMed  CAS  Google Scholar 

  • O’Neill P, Mak S-S, Fritzsch B, Ladher RK, Baker CVH (2012) The amniote paratympanic organ develops from a previously undiscovered sensory placode. Nat Commun 3:1041

    Article  PubMed  CAS  Google Scholar 

  • Patthey C, Schlosser G, Shimeld SM (2014) The evolutionary history of vertebrate cranial placodes--I: cell type evolution. Dev Biol 389:82–97

    Article  CAS  PubMed  Google Scholar 

  • Petralia RS, Wang Y-X, Mattson MP, Yao PJ (2016) The diversity of spine synapses in animals. NeuroMolecular Med 18:497–539

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pierce ML, Weston MD, Fritzsch B, Gabel HW, Ruvkun G, Soukup GA (2008) MicroRNA-183 family conservation and ciliated neurosensory organ expression. Evol Dev 10:106–113

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Piotrowski T, Baker CVH (2014) The development of lateral line placodes: taking a broader view. Dev Biol 389:68–81

    Article  CAS  PubMed  Google Scholar 

  • Pujol-Martí J, Faucherre A, Aziz-Bose R, Asgharsharghi A, Colombelli J, Trapani JG, López-Schier H (2014) Converging axons collectively initiate and maintain synaptic selectivity in a constantly remodeling sensory organ. Curr Biol 24:2968–2974

    Article  PubMed  CAS  Google Scholar 

  • Raible DW, Kruse GJ (2000) Organization of the lateral line system in embryonic zebrafish. J Comp Neurol 421:189–198

    Article  CAS  PubMed  Google Scholar 

  • Rebay I (2015) Multiple functions of the Eya phosphotyrosine phosphatase. Mol Cell Biol 36:668–677

    Article  PubMed  CAS  Google Scholar 

  • Riddiford N, Schlosser G (2016) Dissecting the pre-placodal transcriptome to reveal presumptive direct targets of Six1 and Eya1 in cranial placodes. eLife 5:e17666

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Riddiford N, Schlosser G (2017) Six1 and Eya1 both promote and arrest neuronal differentiation by activating multiple Notch pathway genes. Dev Biol 431:152–167

    Article  CAS  PubMed  Google Scholar 

  • Rigon F, Gasparini F, Shimeld SM, Candiani S, Manni L (2018) Developmental signature, synaptic connectivity and neurotransmission are conserved between vertebrate hair cells and tunicate coronal cells. J Comp Neurol 526:957–971

    Article  CAS  PubMed  Google Scholar 

  • Ronan M (1988) Anatomical and physiological evidence for electroreception in larval lampreys. Brain Res 448:173–177

    Article  CAS  PubMed  Google Scholar 

  • Roth A (2003) Development of catfish lateral line organs: electroreceptors require innervation, although mechanoreceptors do not. Naturwissenschaften 90:251–255

    Article  CAS  PubMed  Google Scholar 

  • Safieddine S, El-Amraoui A, Petit C (2012) The auditory hair cell ribbon synapse: from assembly to function. Annu Rev Neurosci 35:509–528

    Article  CAS  PubMed  Google Scholar 

  • Saint-Jeannet J-P, Moody SA (2014) Establishing the pre-placodal region and breaking it into placodes with distinct identities. Dev Biol 389:13–27

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sarrazin AF, Nuñez VA, Sapède D, Tassin V, Dambly-Chaudière C, Ghysen A (2010) Origin and early development of the posterior lateral line system of zebrafish. J Neurosci 30:8234–8244

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schlosser G (2002a) Development and evolution of lateral line placodes in amphibians I. Development. Zoology (Jena) 105:119–146

    Article  Google Scholar 

  • Schlosser G (2002b) Development and evolution of lateral line placodes in amphibians. II Evolutionary diversification. Zoology (Jena) 105:177–193

    Article  Google Scholar 

  • Schlosser G (2010) Making senses: development of vertebrate cranial placodes. Int Rev Cell Mol Biol 283:129–234

    Article  CAS  PubMed  Google Scholar 

  • Schlosser G (2014) Early embryonic specification of vertebrate cranial placodes. WIREs Dev Biol 3:349–363

    Article  CAS  Google Scholar 

  • Schlosser G, Ahrens K (2004) Molecular anatomy of placode development in Xenopus laevis. Dev Biol 271:439–466

    Article  CAS  PubMed  Google Scholar 

  • Schlosser G, Kintner C, Northcutt RG (1999) Loss of ectodermal competence for lateral line placode formation in the direct developing frog Eleutherodactylus coqui. Dev Biol 213:354–369

    Article  CAS  PubMed  Google Scholar 

  • Schlosser G, Awtry T, Brugmann SA, Jensen ED, Neilson K, Ruan G, Stammler A, Voelker D, Yan B, Zhang C, Klymkowsky MW, Moody SA (2008) Eya1 and Six1 promote neurogenesis in the cranial placodes in a SoxB1-dependent fashion. Dev Biol 320:199–214

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schlosser G, Patthey C, Shimeld SM (2014) The evolutionary history of vertebrate cranial placodes II. Evolution of ectodermal patterning. Dev Biol 389:98–119

    Article  CAS  PubMed  Google Scholar 

  • Schönberger J, Wang L, Shin JT, Kim SD, Depreux FFS, Zhu H, Zon L, Pizard A, Kim JB, Macrae CA, Mungall AJ, Seidman JG, Seidman CE (2005) Mutation in the transcriptional coactivator EYA4 causes dilated cardiomyopathy and sensorineural hearing loss. Nat Genet 37:418–422

    Article  PubMed  CAS  Google Scholar 

  • Shimeld SM, Donoghue PCJ (2012) Evolutionary crossroads in developmental biology: cyclostomes (lamprey and hagfish). Development 139:2091–2099

    Article  CAS  PubMed  Google Scholar 

  • Sillar KT, Picton LD, Heitler WJ (2016) Chapter 6: Electrolocation and electric organs. In: The neuroethology of predation and escape. Wiley, Chichester, pp 140–177

    Chapter  Google Scholar 

  • Soukup GA (2009) Little but loud: small RNAs have a resounding affect on ear development. Brain Res 1277:104–114

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Square T, Romášek M, Jandzik D, Cattell MV, Klymkowsky M, Medeiros DM (2015) CRISPR/Cas9-mediated mutagenesis in the sea lamprey Petromyzon marinus: a powerful tool for understanding ancestral gene functions in vertebrates. Development 142:4180–4187

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thomas ED, Cruz IA, Hailey DW, Raible DW (2015) There and back again: development and regeneration of the zebrafish lateral line system. WIREs Dev Biol 4:1–16

    Article  CAS  Google Scholar 

  • Webb JF (2014) Morphological diversity, development, and evolution of the mechanosensory lateral line system. In: Coombs SC, Bleckmann H, Fay RR, Popper AN (eds) The lateral line system. Springer, New York, pp 17–72

    Google Scholar 

  • Weston MD, Soukup GA (2009) MicroRNAs sound off. Genome Med 1:59

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Weston MD, Pierce ML, Jensen-Smith HC, Fritzsch B, Rocha-Sanchez S, Beisel KW, Soukup GA (2011) MicroRNA-183 family expression in hair cell development and requirement of microRNAs for hair cell maintenance and survival. Dev Dyn 240:808–819

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Weston MD, Tarang S, Pierce ML, Pyakurel U, Rocha-Sanchez SM, McGee J, Walsh EJ, Soukup GA (2018) A mouse model of miR-96, miR-182 and miR-183 misexpression implicates miRNAs in cochlear cell fate and homeostasis. Sci Rep 8:3569

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wullimann MF, Grothe B (2014) The central nervous organization of the lateral line system. In: Coombs SC, Bleckmann H, Fay RR, Popper AN (eds) The lateral line system. Springer, New York, pp 195–251

    Google Scholar 

  • Zanazzi G, Matthews G (2009) The molecular architecture of ribbon presynaptic terminals. Mol Neurobiol 39:130–148

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang T, Xu J, Maire P, Xu P-X (2017) Six1 is essential for differentiation and patterning of the mammalian auditory sensory epithelium. PLoS Genet 13:e1006967

    Article  PubMed  PubMed Central  CAS  Google Scholar 

Download references

Compliance with Ethics Requirements

Clare Baker declares that she has no conflict of interest.

Author information

Authors and Affiliations

  1. Department of Physiology, Development and Neuroscience, University of Cambridge, Cambridge, UK

    Clare V. H. Baker

Authors
  1. Clare V. H. Baker
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Clare V. H. Baker .

Editor information

Editors and Affiliations

  1. Department of Biology, Washington University in St. Louis, St. Louis, MO, USA

    Bruce A. Carlson

  2. Department of Psychology, University of Washington, Seattle, WA, USA

    Joseph A. Sisneros

  3. Department of Biology, University of Maryland, College Park, MD, USA

    Arthur N. Popper

  4. Department of Psychology, Loyola University Chicago, Chicago, IL, USA

    Richard R. Fay

Rights and permissions

Reprints and permissions

Copyright information

© 2019 Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Baker, C.V.H. (2019). The Development and Evolution of Lateral Line Electroreceptors: Insights from Comparative Molecular Approaches. In: Carlson, B., Sisneros, J., Popper, A., Fay, R. (eds) Electroreception: Fundamental Insights from Comparative Approaches. Springer Handbook of Auditory Research, vol 70. Springer, Cham. https://doi.org/10.1007/978-3-030-29105-1_2

Download citation

Publish with us

Policies and ethics

Search

Navigation