Skip to main content

Advertisement

SpringerLink
Log in

The Frog Inner Ear: Picture Perfect?

  • Research Article
  • Published:
Journal of the Association for Research in Otolaryngology Aims and scope Submit manuscript

Abstract

Many recent accounts of the frog peripheral auditory system have reproduced Wever’s (1973) schematic cross-section of the ear of a leopard frog. We sought to investigate to what extent this diagram is an accurate and representative depiction of the anuran inner ear, using three-dimensional reconstructions made from serial sections of Rana pipiens, Eleutherodactylus limbatus and Xenopus laevis. In Rana, three discrete contact membranes were found to separate the posterior otic (=endolymphatic) labyrinth from the periotic (=perilymphatic) system: those of the amphibian and basilar recesses and the contact membrane of the saccule. The amphibian ‘tegmentum vasculosum’ was distinguishable as a thickened epithelial lining within a posterior recess of the superior saccular chamber. These features were also identified in Eleutherodactylus, but in this tiny frog the relative proportions of the semicircular canals and saccule resemble those of ranid tadpoles. There appeared to be a complete fluid pathway between the right and left periotic labyrinths in this species, crossing the cranial cavity. Xenopus lacks a tegmentum vasculosum and a contact membrane of the saccule; the Xenopus ear is further distinguished by a lateral passage separating stapes from periotic cistern and a more direct connection between periotic cistern and basilar recess. The basilar and lagenar recesses are conjoined in this species. Wever’s diagram of the inner ear of Rana retains its value for diagrammatic purposes, but it is not anatomically accurate or representative of all frogs. Although Wever identified the contact membrane of the saccule, most recent studies of frog inner ear anatomy have overlooked both this and the amphibian tegmentum vasculosum. These structures deserve further attention.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

FIG. 1
FIG. 2
FIG. 3
FIG. 4
FIG. 5
FIG. 6
FIG. 7
FIG. 8
FIG. 9
FIG. 10
FIG. 11
FIG. 12

Similar content being viewed by others

References

  • Baird IL (1974) Anatomical features of the inner ear in submammalian vertebrates. In: Keidel WD, Neff WD (eds) Handbook of sensory physiology, volume V/1: auditory system. Springer, Berlin, pp 159–212

    Google Scholar 

  • Bernard C, Ferrary E, Sterkers O (1986) Production of endolymph in the semicircular canal of the frog Rana esculenta. J Physiol 371:17–28

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Bever MM, Jean YY, Fekete DM (2003) Three-dimensional morphology of inner ear development in Xenopus laevis. Dev Dyn 227:422–430

    Article  PubMed  Google Scholar 

  • Birkmann K (1940) Morphologisch-anatomische Untersuchungen zur Entwicklung des häutigen Labyrinthes der Amphibien. Zeitschrift für Anatomie und Entwicklungsgeschichte 110:443–488

    Article  Google Scholar 

  • Blood DC, Studdert VP (1999) Saunders comprehensive veterinary dictionary, 2nd edn. W.B. Saunders, Edinburgh

    Google Scholar 

  • Burnham JA, Stirling CE (1984) Quantitative localization of Na-K pump site in frog inner ear dark cells. Hear Res 13:261–268

    Article  CAS  PubMed  Google Scholar 

  • Deiters O (1862) Ueber das innere Gehörorgan der Amphibien. Archiv für Anatomie. Physiologie und Wissenschaftliche Medicin 1862:262–275, 277-310

    Google Scholar 

  • Dubois A (2007) Naming taxa from cladograms: a cautionary tale. Mol Phylogenet Evol 42:317–330

    Article  PubMed  Google Scholar 

  • Duellman WE, Trueb L (1986) Biology of amphibians. The Johns Hopkins University Press, Baltimore

    Google Scholar 

  • Fay RR, Popper AN (1985) The octavolateralis system. In: Hildebrand M, Bramble DM, Liem KF, Wake DB (eds) Functional vertebrate morphology. Belknap, London, pp 291–316

    Google Scholar 

  • Frishkopf LS, Goldstein MH (1963) Responses to acoustic stimuli from single units in the eighth nerve of the bullfrog. J Acoust Soc Am 35:1219–1228

    Article  Google Scholar 

  • Gaupp E (1904) A. Ecker’s und R. Wiedersheim’s Anatomie des Frosches, part 3, 2nd edn. Druck und Verlag von Friedrich Vieweg und Sohn, Braunschweig

  • Gridi-Papp M, Narins PM (2010) Seismic detection and communication in amphibians. In: O’Connell-Rodwell CE (ed) The use of vibrations in communication: properties, mechanisms and function across Taxa. Research Signpost, Kerala, pp 69–83

    Google Scholar 

  • Hagmann B, Giebel W (1978) Enzymhistochemische Untersuchungen am Innenohr des Frosches (Rana temporaria). Archives Oto-Rhino-Laryngol 220:89–103

    Article  CAS  Google Scholar 

  • Harrison HS (1902) On the perilymphatic spaces of the amphibian ear. Int Monatsschrift für Anatomie Physiol 19:221–261

    Google Scholar 

  • Hasse C (1868) Das Gehörorgan der Frösche, Reprinted from Zeitschrift für wissenschaftliche Zoologie, Bd, 18th edn. Verlag von Wilhelm Engelmann, Leipzig

    Google Scholar 

  • Henson OW (1974) Comparative anatomy of the middle ear. In: Keidel WD, Neff WD (eds) Handbook of sensory physiology, volume V/1: auditory system. Springer, Berlin, pp 39–110

    Google Scholar 

  • Hillis DM (2007) Constraints in naming parts of the tree of life. Mol Phylogenet Evol 42:331–338

    Article  PubMed  Google Scholar 

  • Hoegg S, Vences M, Brinkmann H, Meyer A (2004) Phylogeny and comparative substitution rates of frogs inferred from sequences of three nuclear genes. Mol Biol Evol 21:1188–1200

    Article  CAS  PubMed  Google Scholar 

  • Hossler FE, Olson KR, Musil G, McKamey MI (2002) Ultrastructure and blood supply of the tegmentum vasculosum in the cochlea of the duckling. Hear Res 164:155–165

    Article  PubMed  Google Scholar 

  • Jørgensen MB, Kanneworff M (1998) Middle ear transmission in the grass frog, Rana temporaria. J Comp Physiol A 182:59–64

    PubMed  Google Scholar 

  • Kuhn (1880) Ueber das häutige Labyrinth der Amphibien. Arch Mikrosk Anat 17:479–550

    Article  Google Scholar 

  • Lewis ER (1976) Surface morphology of the bullfrog amphibian papilla. Brain Behav Evol 13:196–215

    Article  CAS  PubMed  Google Scholar 

  • Lewis ER (1984) On the frog amphibian papilla. Scanning Electron Microscopy 1984 (IV):1899–1913

  • Lewis ER, Narins PM (1999) The acoustic periphery of amphibians: anatomy and physiology. In: Fay RR, Popper AN (eds) Comparative hearing: fish and amphibians. Springer, New York, pp 101–154

    Chapter  Google Scholar 

  • Lewis ER, Leverenz EL, Bialek WS (1985) The vertebrate inner ear. CRC Press, Inc., Boca Raton

    Google Scholar 

  • Lombard RE (1977) Comparative morphology of the inner ear in salamanders (Caudata: Amphibia). S. Karger, Basel

    Google Scholar 

  • Mason MJ, Narins PM (2002) Vibrometric studies of the middle ear of the bullfrog Rana catesbeiana. I. The extrastapes. J Exp Biol 205:3153–3165

    PubMed  Google Scholar 

  • Mason MJ, Wang M, Narins PM (2009) Structure and function of the middle ear apparatus of the aquatic frog, Xenopus laevis. Proc Inst Acoustics 31:13–21

    Google Scholar 

  • Moody D, Lozanoff S (1998) SURFdriver: A practical computer program for generating three-dimensional models of anatomical structures using a PowerMac. Clin Anat 11:132

  • Paterson NF (1949) The development of the inner ear of Xenopus laevis. Proc Zool Soc London 119:269–291

  • Paterson NF (1960) The inner ear of some members of the Pipidae (Amphibia). Proc Zool Soc London 134:509–546

    Article  Google Scholar 

  • Pauly GB, Hillis DM, Cannatella DC (2009) Taxonomic freedom and the role of official lists of species names. Herpetologica 65:115–128

    Article  Google Scholar 

  • Purgue AP, Narins PM (2000a) A model for energy flow in the inner ear of the bullfrog (Rana catesbeiana). J Comp Physiol A 186:489–495

    Article  CAS  PubMed  Google Scholar 

  • Purgue AP, Narins PM (2000b) Mechanics of the inner ear of the bullfrog (Rana catesbeiana): the contact membranes and the periotic canal. J Comp Physiol A 186:481–488

    Article  CAS  PubMed  Google Scholar 

  • Retzius G (1881) Das Gehörorgan der Wirbelthiere. morphologisch-Histologische Studien. I. Das Gehörorgan der Fische und Amphibien. Samson & Wallin, Stockholm

    Google Scholar 

  • Simmons DD, Meenderink SWF, Vassilakis PN (2007) Anatomy, physiology, and function of auditory end-organs in the frog inner ear. In: Narins PM, Feng AS, Fay RR, Popper AN (eds) Hearing and sound communication in amphibians. Springer, New York, pp 184–220

    Google Scholar 

  • Smotherman M, Narins P (2004) Evolution of the amphibian ear. In: Manley GA, Popper AN, Fay RR (eds) Evolution of the vertebrate auditory system. Springer, New York, pp 164–199

    Chapter  Google Scholar 

  • Thévenaz P, Ruttimann UE, Unser M (1998) A pyramid approach to subpixel registration based on intensity. IEEE Trans Image Process 7:27–41

    Article  PubMed  Google Scholar 

  • van Dijk P, Mason MJ, Schoffelen RLM, Narins PM, Meenderink SWF (2011) Mechanics of the frog ear. Hear Res 273:46–58

    Article  PubMed Central  PubMed  Google Scholar 

  • Wagner DS (1934) The structure of the inner ear in relation to the reduction of the middle ear in the Liopelmidae (Noble). Anat Anz 79:20–36

    Google Scholar 

  • Werner YL (2003) Mechanical leverage in the middle ear of the American bullfrog, Rana catesbeiana. Hear Res 175:54–65

    Article  PubMed  Google Scholar 

  • Wever EG (1973) The ear and hearing in the frog, Rana pipiens. J Morphol 141:461–477

    Article  CAS  PubMed  Google Scholar 

  • Wever EG (1978) Sound transmission in the salamander ear. Proc Natl Acad Sci U S A 75:529–530

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wever EG (1985) The amphibian ear. Princeton University Press, Princeton

    Book  Google Scholar 

Download references

Acknowledgements

The authors wish to thank Emanuel Mora for his help and support with this project. Dave Simpson kindly provided the Xenopus specimens. The CT scan of Xenopus was made by Alan Heaver of the University of Cambridge Department of Engineering, with thanks going also to Norman Fleck for the use of his equipment. The authors are very grateful to Dolores Bozovic, Alan D. Grinnell, Tammy Hoang, Victoria Sandoval and Felix E. Schweizer for facilitating the Rana CT scan, which was made by Ting-Ling Chang at the UCLA School of Dentistry, Division of Advanced Prosthodontics. Stephan Kamrad helped with translations. The research of JMS and PvD was supported by the Heinsius Houbolt Foundation and is part of the research programme Healthy Ageing and Communication of the Department of Otorhinolaryngology at the University Medical Center Groningen. Finally, the authors wish to thank the reviewers and editors of the manuscript for their very helpful comments.

Conflicts of Interest

The authors declare that they have no conflicts of interest.

Author information

Authors and Affiliations

  1. Department of Physiology, Development and Neuroscience, University of Cambridge, Downing Street, Cambridge, CB2 3EG, UK

    Matthew J. Mason

  2. Department of Otorhinolaryngology, Head and Neck Surgery, University of Groningen, University Medical Center Groningen, P.O. Box 30.001, 9700 RB, Groningen, The Netherlands

    Johannes M. Segenhout & Pim van Dijk

  3. Department of Animal and Human Biology, Havana University, Street 25 No. 455, Havana, CP 10400, Cuba

    Ariadna Cobo-Cuan

  4. Department of Physics and Astronomy, University of California Los Angeles, 1-129 Knudsen Hall, 475 Portola Plaza, Los Angeles, CA, 90095, USA

    Patricia M. Quiñones

  5. Graduate School of Medical Sciences, Research School of Behavioral and Cognitive Neurosciences, University of Groningen, P.O. Box 196, 9700 AD, Groningen, The Netherlands

    Pim van Dijk

Authors
  1. Matthew J. Mason
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Johannes M. Segenhout
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ariadna Cobo-Cuan
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Patricia M. Quiñones
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Pim van Dijk
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Matthew J. Mason.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Mason, M.J., Segenhout, J.M., Cobo-Cuan, A. et al. The Frog Inner Ear: Picture Perfect?. JARO 16, 171–188 (2015). https://doi.org/10.1007/s10162-015-0506-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10162-015-0506-z

Keywords

Search

Navigation