Advertisement

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

  • Clare V. H. BakerEmail author
Chapter
Part of the Springer Handbook of Auditory Research book series (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.

Keywords

Ampullary organ Electroreception Electrosensory Hair cell Mechanosensory Neuromast Placode Presynaptic ribbon Ribbon synapse RNA sequencing Tuberous organ 

Notes

Compliance with Ethics Requirements

Clare Baker declares that she has no conflict of interest.

References

  1. 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 22:377–390PubMedPubMedCentralCrossRefGoogle Scholar
  2. Amemiya F, Kishida R, Goris RC, Onishi H, Kusunoki T (1985) Primary vestibular projections in the hagfish, Eptatretus burgeri. Brain Res 337:73–79PubMedCrossRefPubMedCentralGoogle Scholar
  3. Andermann P, Ungos J, Raible DW (2002) Neurogenin1 defines zebrafish cranial sensory ganglia precursors. Dev Biol 251:45–58PubMedCrossRefPubMedCentralGoogle Scholar
  4. 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 17:744–757PubMedCrossRefPubMedCentralGoogle Scholar
  5. Baker CVH, Modrell MS (2018) Insights into electroreceptor development and evolution from molecular comparisons with hair cells. Integr Comp Biol 58:329–340PubMedCrossRefPubMedCentralGoogle Scholar
  6. Baker CVH, Modrell MS, Gillis JA (2013) The evolution and development of vertebrate lateral line electroreceptors. J Exp Biol 216:2515–2522PubMedPubMedCentralCrossRefGoogle Scholar
  7. Barry MA, White RL, Bennett MVL (1988) The elasmobranch spiracular organ. II. Physiological studies. J Comp Physiol A 163:93–98PubMedCrossRefPubMedCentralGoogle Scholar
  8. 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:e30241PubMedPubMedCentralCrossRefGoogle Scholar
  9. Bedore CN, Kajiura SM (2013) Bioelectric fields of marine organisms: voltage and frequency contributions to detectability by electroreceptive predators. Physiol Biochem Zool 86:298–311PubMedCrossRefPubMedCentralGoogle Scholar
  10. 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 68–111CrossRefGoogle Scholar
  11. 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):17–31CrossRefGoogle Scholar
  12. Bellono NW, Leitch DB, Julius D (2017) Molecular basis of ancestral vertebrate electroreception. Nature 543:391–396PubMedPubMedCentralCrossRefGoogle Scholar
  13. Bellono NW, Leitch DB, Julius D (2018) Molecular tuning of electroreception in sharks and skates. Nature 558:122–126PubMedPubMedCentralCrossRefGoogle Scholar
  14. Bennett MVL, Obara S (1986) Ionic mechanisms and pharmacology of electroreceptors. In: Bullock TH, Heiligenberg W (eds) Electroreception. Wiley, New York, pp 157–181Google Scholar
  15. 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 17:162PubMedPubMedCentralCrossRefGoogle Scholar
  16. 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 655–678Google Scholar
  17. 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 132–153CrossRefGoogle Scholar
  18. Bodznick D, Preston DG (1983) Physiological characterization of electroreceptors in the lampreys Ichthyomyzon unicuspis and Petromyzon marinus. J Comp Physiol A 152:209–217CrossRefGoogle Scholar
  19. Braun CB (1996) The sensory biology of the living jawless fishes: a phylogenetic assessment. Brain Behav Evol 48:262–276PubMedCrossRefPubMedCentralGoogle Scholar
  20. Braun CB, Northcutt RG (1997) The lateral line system of hagfishes (Craniata: Myxinoidea). Acta Zool (Stockh) 78:247–268CrossRefGoogle Scholar
  21. 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 287:25–46CrossRefGoogle Scholar
  22. Burighel P, Caicci F, Manni L (2011) Hair cells in non-vertebrate models: lower chordates and molluscs. Hear Res 273:14–24PubMedCrossRefPubMedCentralGoogle Scholar
  23. 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–F156PubMedCrossRefPubMedCentralGoogle Scholar
  24. 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 151–194Google Scholar
  25. Costa A, Powell LM, Lowell S, Jarman AP (2017) Atoh1 in sensory hair cell development: constraints and cofactors. Semin Cell Dev Biol 65:60–68PubMedCrossRefPubMedCentralGoogle Scholar
  26. Cunningham CL, Müller U (2019) Molecular structure of the hair cell mechanoelectrical transduction complex. Cold Spring Harb Perspect Med 9:a033167PubMedCrossRefPubMedCentralGoogle Scholar
  27. Czech-Damal NU, Dehnhardt G, Manger P, Hanke W (2013) Passive electroreception in aquatic mammals. J Comp Physiol A 199:555–563CrossRefGoogle Scholar
  28. 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 105:18396–18401PubMedPubMedCentralCrossRefGoogle Scholar
  29. 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 8:205PubMedPubMedCentralCrossRefGoogle Scholar
  30. Dalle Nogare D, Chitnis AB (2017) A framework for understanding morphogenesis and migration of the zebrafish posterior lateral line primordium. Mech Dev 148:69–78PubMedCrossRefPubMedCentralGoogle Scholar
  31. DeCaen PG, Delling M, Vien TN, Clapham DE (2013) Direct recording and molecular identification of the calcium channel of primary cilia. Nature 504:315–318PubMedPubMedCentralCrossRefGoogle Scholar
  32. 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 90:2022–2028PubMedCrossRefPubMedCentralGoogle Scholar
  33. Delling M, DeCaen PG, Doerner JF, Febvay S, Clapham DE (2013) Primary cilia are specialized calcium signalling organelles. Nature 504:311–314PubMedPubMedCentralCrossRefGoogle Scholar
  34. Dijkgraaf S (1963) The functioning and significance of the lateral-line organs. Biol Rev 38:51–105PubMedCrossRefPubMedCentralGoogle Scholar
  35. 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:e33988PubMedPubMedCentralCrossRefGoogle Scholar
  36. 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:e0180855PubMedPubMedCentralCrossRefGoogle Scholar
  37. 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 6:8549PubMedPubMedCentralCrossRefGoogle Scholar
  38. Fettiplace R, Fuchs PA (1999) Mechanisms of hair cell tuning. Annu Rev Physiol 61:809–834PubMedCrossRefPubMedCentralGoogle Scholar
  39. Fields RD, Bullock TH, Lange GD (1993) Ampullary sense organs, peripheral, central and behavioral electroreception in chimeras (Hydrolagus, Holocephali, Chondrichthyes). Brain Behav Evol 41:269–289PubMedCrossRefPubMedCentralGoogle Scholar
  40. Flock Å (1965) Transducing mechanisms in the lateral line canal organ receptors. Cold Spring Harb Symp Quant Biol 30:133–145PubMedCrossRefPubMedCentralGoogle Scholar
  41. Flowers GP, Crews CM (2015) Generating and identifying axolotls with targeted mutations using Cas9 RNA-guided nuclease. Methods Mol Biol 1290:279–295PubMedCrossRefPubMedCentralGoogle Scholar
  42. Fritzsch B, Elliott KL (2017) Gene, cell, and organ multiplication drives inner ear evolution. Dev Biol 431:3–15PubMedPubMedCentralCrossRefGoogle Scholar
  43. Gelman S, Ayali A, Tytell ED, Cohen AH (2007) Larval lampreys possess a functional lateral line system. J Comp Physiol A 193:271–277CrossRefGoogle Scholar
  44. Ghysen A, Dambly-Chaudière C (2004) Development of the zebrafish lateral line. Curr Opin Neurobiol 14:67–73PubMedCrossRefPubMedCentralGoogle Scholar
  45. Gibbs MA, Northcutt RG (2004a) Development of the lateral line system in the shovelnose sturgeon. Brain Behav Evol 64:70–84PubMedCrossRefPubMedCentralGoogle Scholar
  46. Gibbs MA, Northcutt RG (2004b) Retinoic acid repatterns axolotl lateral line receptors. Int J Dev Biol 48:63–66PubMedCrossRefPubMedCentralGoogle Scholar
  47. 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 139:3142–3146PubMedPubMedCentralCrossRefGoogle Scholar
  48. Gilmour D, Knaut H, Maischein HM, Nüsslein-Volhard C (2004) Towing of sensory axons by their migrating target cells in vivo. Nat Neurosci 7:491–492PubMedCrossRefPubMedCentralGoogle Scholar
  49. 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 114:8023–8028PubMedPubMedCentralCrossRefGoogle Scholar
  50. 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 9:75PubMedPubMedCentralCrossRefGoogle Scholar
  51. Hatakeyama J, Kageyama R (2004) Retinal cell fate determination and bHLH factors. Semin Cell Dev Biol 15:83–89PubMedCrossRefPubMedCentralGoogle Scholar
  52. 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 3:488–498PubMedPubMedCentralCrossRefGoogle Scholar
  53. 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 25:999–1005PubMedCrossRefPubMedCentralGoogle Scholar
  54. Holder N, Hill J (1991) Retinoic acid modifies development of the midbrain-hindbrain border and affects cranial ganglion formation in zebrafish embryos. Development 113:1159–1170PubMedPubMedCentralGoogle Scholar
  55. 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 74:2407–2411PubMedPubMedCentralCrossRefGoogle Scholar
  56. 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:e11661PubMedPubMedCentralCrossRefGoogle Scholar
  57. 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:e29275PubMedPubMedCentralCrossRefGoogle Scholar
  58. 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) 63:211–217CrossRefGoogle Scholar
  59. Jørgensen JM (2005) Morphology of electroreceptive sensory organs. In: Bullock TH, Hopkins CD, Popper AN, Fay RR (eds) Electroreception. Springer, New York, pp 47–67CrossRefGoogle Scholar
  60. Jørgensen JM (2011) Morphology of electroreceptive sensory organs. In: Farrell AP (ed) Encyclopedia of fish physiology: from genome to environment. Academic, San Diego, pp 350–358CrossRefGoogle Scholar
  61. 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 DiegoGoogle Scholar
  62. Kniss JS, Jiang L, Piotrowski T (2016) Insights into sensory hair cell regeneration from the zebrafish lateral line. Curr Opin Genet Dev 40:32–40PubMedCrossRefPubMedCentralGoogle Scholar
  63. Köster RW, Kühnlein RP, Wittbrodt J (2000) Ectopic Sox3 activity elicits sensory placode formation. Mech Dev 95:175–187PubMedCrossRefPubMedCentralGoogle Scholar
  64. 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:e36287PubMedPubMedCentralCrossRefGoogle Scholar
  65. 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 7:401–412PubMedCrossRefPubMedCentralGoogle Scholar
  66. 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 5:85–101CrossRefGoogle Scholar
  67. 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 15:2784–2795PubMedPubMedCentralCrossRefGoogle Scholar
  68. 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 35:1098–1114PubMedPubMedCentralCrossRefGoogle Scholar
  69. McCormick CA (1982) The organization of the octavolateralis area in actinopterygian fishes: a new interpretation. J Morphol 171:159–181PubMedCrossRefPubMedCentralGoogle Scholar
  70. Metscher BD, Northcutt RG, Gardiner DM, Bryant SV (1997) Homeobox genes in axolotl lateral line placodes and neuromasts. Dev Genes Evol 207:287–295PubMedCrossRefPubMedCentralGoogle Scholar
  71. 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:e31013PubMedPubMedCentralCrossRefGoogle Scholar
  72. 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 134:295–305PubMedCrossRefPubMedCentralGoogle Scholar
  73. Modrell MS, Baker CVH (2012) Evolution of electrosensory ampullary organs: conservation of Eya4 expression during lateral line development in jawed vertebrates. Evol Dev 14:277–285PubMedPubMedCentralCrossRefGoogle Scholar
  74. 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 2:496PubMedPubMedCentralCrossRefGoogle Scholar
  75. 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 385:405–416PubMedPubMedCentralCrossRefGoogle Scholar
  76. 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:e24197PubMedPubMedCentralCrossRefGoogle Scholar
  77. 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 431:48–58PubMedPubMedCentralCrossRefGoogle Scholar
  78. 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 121–150Google Scholar
  79. Münz H, Claas B, Fritzsch B (1984) Electroreceptive and mechanoreceptive units in the lateral line of the axolotl Ambystoma mexicanum. J Comp Physiol A 154:33–44CrossRefGoogle Scholar
  80. 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 28:8442–8453PubMedPubMedCentralCrossRefGoogle Scholar
  81. 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 29:10730–10740PubMedCrossRefPubMedCentralGoogle Scholar
  82. Nicolson T (2015) Ribbon synapses in zebrafish hair cells. Hear Res 330:170–177PubMedPubMedCentralCrossRefGoogle Scholar
  83. Nicolson T (2017) The genetics of hair-cell function in zebrafish. J Neurogenet 31:102–112PubMedPubMedCentralCrossRefGoogle Scholar
  84. 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 236:564–571PubMedCrossRefPubMedCentralGoogle Scholar
  85. 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 431:215–225PubMedCrossRefPubMedCentralGoogle Scholar
  86. 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 112–131CrossRefGoogle Scholar
  87. Northcutt RG (2005b) The New Head Hypothesis revisited. J Exp Zool B Mol Dev Evol 304B:274–297Google Scholar
  88. Northcutt RG, Catania KC, Criley BB (1994) Development of lateral line organs in the axolotl. J Comp Neurol 340:480–514PubMedCrossRefPubMedCentralGoogle Scholar
  89. Northcutt RG, Brändle K, Fritzsch B (1995) Electroreceptors and mechanosensory lateral line organs arise from single placodes in axolotls. Dev Biol 168:358–373PubMedCrossRefPubMedCentralGoogle Scholar
  90. 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 304:156–181PubMedCrossRefPubMedCentralGoogle Scholar
  91. 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 3:1041PubMedPubMedCentralCrossRefGoogle Scholar
  92. Patthey C, Schlosser G, Shimeld SM (2014) The evolutionary history of vertebrate cranial placodes--I: cell type evolution. Dev Biol 389:82–97PubMedCrossRefPubMedCentralGoogle Scholar
  93. Petralia RS, Wang Y-X, Mattson MP, Yao PJ (2016) The diversity of spine synapses in animals. NeuroMolecular Med 18:497–539PubMedPubMedCentralCrossRefGoogle Scholar
  94. Pierce ML, Weston MD, Fritzsch B, Gabel HW, Ruvkun G, Soukup GA (2008) MicroRNA-183 family conservation and ciliated neurosensory organ expression. Evol Dev 10:106–113PubMedPubMedCentralCrossRefGoogle Scholar
  95. Piotrowski T, Baker CVH (2014) The development of lateral line placodes: taking a broader view. Dev Biol 389:68–81PubMedCrossRefPubMedCentralGoogle Scholar
  96. 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 24:2968–2974PubMedCrossRefPubMedCentralGoogle Scholar
  97. Raible DW, Kruse GJ (2000) Organization of the lateral line system in embryonic zebrafish. J Comp Neurol 421:189–198PubMedCrossRefPubMedCentralGoogle Scholar
  98. Rebay I (2015) Multiple functions of the Eya phosphotyrosine phosphatase. Mol Cell Biol 36:668–677PubMedCrossRefPubMedCentralGoogle Scholar
  99. Riddiford N, Schlosser G (2016) Dissecting the pre-placodal transcriptome to reveal presumptive direct targets of Six1 and Eya1 in cranial placodes. eLife 5:e17666PubMedPubMedCentralCrossRefGoogle Scholar
  100. Riddiford N, Schlosser G (2017) Six1 and Eya1 both promote and arrest neuronal differentiation by activating multiple Notch pathway genes. Dev Biol 431:152–167PubMedCrossRefGoogle Scholar
  101. 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 526:957–971PubMedCrossRefGoogle Scholar
  102. Ronan M (1988) Anatomical and physiological evidence for electroreception in larval lampreys. Brain Res 448:173–177PubMedCrossRefGoogle Scholar
  103. Roth A (2003) Development of catfish lateral line organs: electroreceptors require innervation, although mechanoreceptors do not. Naturwissenschaften 90:251–255PubMedCrossRefGoogle Scholar
  104. Safieddine S, El-Amraoui A, Petit C (2012) The auditory hair cell ribbon synapse: from assembly to function. Annu Rev Neurosci 35:509–528PubMedCrossRefPubMedCentralGoogle Scholar
  105. Saint-Jeannet J-P, Moody SA (2014) Establishing the pre-placodal region and breaking it into placodes with distinct identities. Dev Biol 389:13–27PubMedPubMedCentralCrossRefGoogle Scholar
  106. 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 30:8234–8244PubMedPubMedCentralCrossRefGoogle Scholar
  107. Schlosser G (2002a) Development and evolution of lateral line placodes in amphibians I. Development. Zoology (Jena) 105:119–146CrossRefGoogle Scholar
  108. Schlosser G (2002b) Development and evolution of lateral line placodes in amphibians. II Evolutionary diversification. Zoology (Jena) 105:177–193CrossRefGoogle Scholar
  109. Schlosser G (2010) Making senses: development of vertebrate cranial placodes. Int Rev Cell Mol Biol 283:129–234PubMedCrossRefGoogle Scholar
  110. Schlosser G (2014) Early embryonic specification of vertebrate cranial placodes. WIREs Dev Biol 3:349–363CrossRefGoogle Scholar
  111. Schlosser G, Ahrens K (2004) Molecular anatomy of placode development in Xenopus laevis. Dev Biol 271:439–466PubMedCrossRefPubMedCentralGoogle Scholar
  112. 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 213:354–369PubMedCrossRefPubMedCentralGoogle Scholar
  113. 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 320:199–214PubMedPubMedCentralCrossRefGoogle Scholar
  114. Schlosser G, Patthey C, Shimeld SM (2014) The evolutionary history of vertebrate cranial placodes II. Evolution of ectodermal patterning. Dev Biol 389:98–119PubMedCrossRefPubMedCentralGoogle Scholar
  115. 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 37:418–422PubMedCrossRefPubMedCentralGoogle Scholar
  116. Shimeld SM, Donoghue PCJ (2012) Evolutionary crossroads in developmental biology: cyclostomes (lamprey and hagfish). Development 139:2091–2099PubMedCrossRefPubMedCentralGoogle Scholar
  117. Sillar KT, Picton LD, Heitler WJ (2016) Chapter 6: Electrolocation and electric organs. In: The neuroethology of predation and escape. Wiley, Chichester, pp 140–177CrossRefGoogle Scholar
  118. Soukup GA (2009) Little but loud: small RNAs have a resounding affect on ear development. Brain Res 1277:104–114PubMedPubMedCentralCrossRefGoogle Scholar
  119. 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 142:4180–4187PubMedPubMedCentralCrossRefGoogle Scholar
  120. 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 4:1–16CrossRefGoogle Scholar
  121. 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 17–72Google Scholar
  122. Weston MD, Soukup GA (2009) MicroRNAs sound off. Genome Med 1:59PubMedPubMedCentralCrossRefGoogle Scholar
  123. 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 240:808–819PubMedPubMedCentralCrossRefGoogle Scholar
  124. 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 8:3569PubMedPubMedCentralCrossRefGoogle Scholar
  125. 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 195–251Google Scholar
  126. Zanazzi G, Matthews G (2009) The molecular architecture of ribbon presynaptic terminals. Mol Neurobiol 39:130–148PubMedPubMedCentralCrossRefGoogle Scholar
  127. 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:e1006967PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Department of Physiology, Development and NeuroscienceUniversity of CambridgeCambridgeUK

Personalised recommendations