Skip to main content
SpringerLink
Log in

Additional row of outer hair cells — The unique pattern of the Corti organ in a subterranean rodent, the Gansu zokor (Eospalax cansus)

  • Original investigation
  • Published:
Mammalian Biology Aims and scope Submit manuscript

Abstract

Acoustic conditions in burrows are different from those aboveground and restrict hearing of subterranean mammals to low frequencies, which is reflected in the ear morphology. While low-frequency adaptations of the middle ear attracted more attention of researches, the inner ear remained rather understudied. Here, we examined the cochlea of the inner ear of the Gansu zokor (Eospalax cansus), a subterranean rodent from the Tibetan Plateau. We focused on the quantitative parameters of the organ of Corti, which are assumed to determine hearing sensitivity and frequency tuning. Apart from the morphological traits common to the ear of subterranean rodents studied thus far, the Gansu zokor shows two unique features: the presence of a fourth row of outer hair cells along 20% to 50% of the basilar membrane length and almost constant width of the organ of Corti over more than 10% of its spiral length. Both these anomalies occur in the middle of the cochlear spiral. These features are unusual in comparative morphology of the organ of Corti and presumably are reflected in the functional specialization. They are expected to affect sensitivity and/or resolution of hearing in the frequency range registered in the given cochlear segment. The Gansu zokor thus profiles to an interesting candidate for hearing research which might provide further insight not only into morpho-functional adaptations in subterranean mammals in particular but also in the function of outer hair cells in general.

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.

Similar content being viewed by others

References

  • Burda, H., Nevo, E., Bruns, V., 1990b. Adaptive differentiation of ear structures in subterranean mole-rats of the Spalax ehrenbergi superspecies in Israel. Zool. Jb. Syst. 8 (3), 369–382.

    Google Scholar 

  • Bednářová, R., Hrouzková-Knotková, E., Burda, H., Sedlácek, F., šumbera, R., 2013. Vocalizations of the giant mole-rat (Fukomys mechowii), a subterranean rodent with the richest vocal repertoire. Bioacoustics 22 (2), 87–107.

    Google Scholar 

  • Begall, S., Burda, H., 2006. Acoustic communication and burrow acoustics are reflected in the ear morphology of the coruro (Spalacopus cyanus, Octodontidae), a social fossorial rodent. J. Morph. 267, 382–390.

    PubMed  Google Scholar 

  • Begall, S., Burda, H., Schneider, B., 2004. Hearing in coruros (Spalacopus cyanus): special audiogram features of a subterranean rodent. J. Comp. Physiol. A 190, 963–969.

    Google Scholar 

  • Begall, S., Lange, S., Schleich, C.E., Burda, H., 2007. Acoustics, audition and auditory system. In: Begall, S., Burda, H., Schleich, C.E. (Eds.), Subterranean Rodents: News from Underground. Springer Verlag, Berlin.

    Google Scholar 

  • Brückmann, G., Burda, H., 1997. Hearing in blind subterranean Zambian mole-rats (Cryptomys sp.) collective behavioural audiogram in a highly social rodent. J. Comp. Physiol. A 181, 83–88.

    PubMed  Google Scholar 

  • Bruns, V., Schmieszek, E., 1980. Cochlear innervation in the greater horseshoe bat - demonstration of an acoustic fovea. Hear. Res. 3 (1), 27–43.

    CAS  PubMed  Google Scholar 

  • Bruns, V., Múller, M., Hofer, W., Heth, G., Nevo, E., 1988. Inner ear structure electrophysiological audiograms of the subterranean mole rat, Spalax ehrenbergi. Hear. Res. 33, 1–9.

    CAS  PubMed  Google Scholar 

  • Burda, H., 1978. Population der Haarzellen des Cortischen Organs der Spitzmáuse. Zeitschrift fur mikroskopisch-anatomische Forschung 92, 514–552.

    CAS  PubMed  Google Scholar 

  • Burda, H., 1979. Morphology of the middle and inner ear in some species of shrews (Insectivora, Soricidae). Acta Sc. Nat. Brno 13 (4), 1–48.

    Google Scholar 

  • Burda, H., 1984. Guinea pig cochlear hair cell density: its relation to frequency discrimination. Hear. Res. 14, 315–317.

    CAS  PubMed  Google Scholar 

  • Burda, H., 1985. Qualitative assessment of postnatal maturation of the organ of Corti in two rat strains. Hear. Res. 17, 201–208.

    CAS  PubMed  Google Scholar 

  • Burda, H., 2006. Ear and eye in subterranean mole-rats, Fukomys anselli (Bathyergidae) and Spalax ehrenbergi (Spalacidae): progressive specialisation or regressive degeneration? Anim. Biol. 56, 475–486.

    Google Scholar 

  • Burda, H., Braniš, M., 1988. Postnatal development of the organ of Corti in the wild house mouse, laboratory mouse, and their hybrid. Hear. Res. 36, 97–106.

    CAS  PubMed  Google Scholar 

  • Burda, H., Voldřich, L., 1980. Correlation between the hair cell density and the auditory treshold in the white rat. Hear. Res. 3, 91–93.

    CAS  PubMed  Google Scholar 

  • Burda, H., Voldrich, L., 1984. The mechanics of the organ of Corti in the mammalian ear. Acta Zool. Fenn. 171, 119–122.

    Google Scholar 

  • Burda, H., Ballast, L., Bruns, V., 1988a. Cochlea in old world mice and rats (Muridae). J. Morph. 198, 269–285.

    CAS  PubMed  Google Scholar 

  • Burda, H., Múller, M., Bruns, V., 1988b. The auditory system in subterranean mammals. In: Eisner, N., Barth, F.G. (Eds.), Sense Organs between Environment and Behaviour. G. Thieme, Stuttgart.

    Google Scholar 

  • Burda, H., Bruns, V., Nevo, E., 1989. Middle ear and cochlear receptors in the subterranean mole-rat, Spalax ehrenbergi. Hear. Res. 39, 225–230.

    CAS  PubMed  Google Scholar 

  • Burda, H., Bruns, V., Múller, M., 1990a. Sensory adaptations in subterranean mammals. In: Nevo, E., Reig, O.A. (Eds.), Evolution of Subterranean Mammals at the Organismal and Molecular Levels. Alan R. Liss, Inc.: Progr. Clin. Biol. Res., New York, pp. 269–293, 335.

    Google Scholar 

  • Burda, H., Bruns, V., Hickman, G., 1992. The ear in subterranean Insectivora and Rodentia in comparison with ground-dwelling representatives. I. Sound conducting system of the middle ear. J. Morph. 214, 49–61.

    CAS  PubMed  Google Scholar 

  • Chen, G.D., Tanaka, C., Henderson, D., 2008. Relation between outer hair cell loss and hearing loss in rats exposed to styrene. Hear. Res. 243, 28–34.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Credner, S., Burda, H., Ludescher, F., 1997. Acoustic communication underground: Vocalization characteristics in subterranean social mole-rats (Cryptomys sp., Bathyergidae. J. Comp. Physiol. A 180, 245–255.

    CAS  PubMed  Google Scholar 

  • Crumpton, N., Kardjilov, N., Asher, R.J., 2015. Convergence vs. Specialization in the ear region of moles (Mammalia). J. Morph. 276 (8), 900–914.

    PubMed  Google Scholar 

  • Dallos, P., 1992. The active cochlea. J. Neurosci. 12, 4575–4585.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dallos, P., Harris, D., 1978. Properties of auditory nerve responses in absence of outer hair cells. J. Neurophysiol. 41, 365–383.

    CAS  PubMed  Google Scholar 

  • Davis, H., 1983. An active process in cochlear mechanics. Hear. Res. 9, 79–90.

    CAS  PubMed  Google Scholar 

  • Dong, W., Olson, E.S., 2013. Detection of cochlear amplification and its activation. Biophys. J. 105, 1067–1078.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dvořáková, V., Hrouzková, E., Šumbera, R., 2016. Vocal repertoire of the social Mashona mole-rat (Fukomys darlingi) and how it compares with other mole-rats. Bioacoustics 25 (3), 253–266.

    Google Scholar 

  • Echteler, S.M., Fay, R.R., Popper, A.N., 1994. Structure of the mammalian cochlea. In: Fay, R.R., Popper, A.N. (Eds.), Comparative Hearing: Mammals. Springer Verlag, New York.

    Google Scholar 

  • Ehret, G., Frankenreiter, M., 1977. Quantitative analysis of cochlear structures in house mouse in relation to mechanisms of acoustical information-processing. J. Comp. Physiol. 122, 65–85.

    Google Scholar 

  • Ekdale, E.G., 2016. Form and function of the mammalian inner ear. J. Anat. 228, 324–337.

    PubMed  Google Scholar 

  • Fernandez, C., 1962. Dimensions of the cochlea (guinea pig). J. Acoust. Soc. Am. 24 (5), 519–523.

    Google Scholar 

  • Flynn, L.J., 2009. The antiquity of Rhizomys and independent acquisition of fossorial traits in subterranean muroids. Bull. Am. Mus. Nat. Hist. 331 (1), 128–156.

    Google Scholar 

  • Gerhardt, P., Henning, Y., Begall, S., Malkemper, P., 2017. Audiograms of three subterranean rodent species (genus Fukomys) determined by auditory brainstem responses reveal extremely poor high-frequency cut-offs. J. Exp. Biol. 220, 4377–4382.

    PubMed  Google Scholar 

  • Glueckert, R., Pfaller, It., Kinnefors, A., Rask-Andersen, H., Schrott-Fischer, A., 2005. Ultrastructure of the normal human organ of Corti. New anatomicalflndings in surgical specimens. Acta Otolaryngol. 125, 534–539.

    PubMed  Google Scholar 

  • Heffner, H.E., Heffner, R.S., 1985. Hearing in two cricetid rodents: wood rat (Neotomafloridana) and Grasshopper Mouse (Onychomys leucogaster). J. Comp. Psychol. 99, 275–288.

    CAS  PubMed  Google Scholar 

  • Heffner, R.S., Heffner, H.E., 1990. Vestigial hearing in a fossorial mammal, the pocket gopher (Geomys bursarius). Hear. Res. 46, 239–252.

    CAS  PubMed  Google Scholar 

  • Heffner, R.S., Heffner, H.E., 1992. Hearing and sound localization in blind mole rats (Spalax ehrenbergi). Hear. Res. 62, 206–216.

    CAS  PubMed  Google Scholar 

  • Heffner, R.S., Heffner, H.E., 1993. Degenerate hearing and sound localization in naked mole rats (Heterocephalus glaber), with an overview of central auditory structures. J. Comp. Neurol. 331, 418–433.

    CAS  PubMed  Google Scholar 

  • Heffner, R.S., Heffner, H.E., Contos, C., Kearns, D., 1994a. Hearing in prairie dogs: transition between surface and subterranean rodents. Hear. Res. 73, 185–189.

    CAS  PubMed  Google Scholar 

  • Heffner, H.E., Heffner, R.S., Contos, C., Ott, T., 1994b. Audiogram of the hooded Norway rat. Hear. Res. 73, 244–247.

    CAS  PubMed  Google Scholar 

  • Heffner, R.S., Koay, G., Heffner, H.E., 2001. Audiogram of five species of rodents: implications for the evolution of hearing and the perception pitch. Hear. Res. 157, 138–152.

    CAS  PubMed  Google Scholar 

  • Heth, G., Frankenberg, E., Nevo, E., 1986. Adaptive optimal sound for vocal communication in tunnels of subterranean mammal (Spalax ehrenbergi). Experientia 42, 1287–1289.

    CAS  PubMed  Google Scholar 

  • Hudspeth, A.J., 2008. Making an effort to listen: mechanical amplification in the ear. Neuron 59, 530–545.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Knotková, E., Veitl, S., šumbera, R., SedláČek, F., Burda, H., 2009. Vocalization of the solitary bathyergid, silvery mole-rat (Heliophobius argenteocinereus). Bioacoustics 18, 241–257.

    Google Scholar 

  • Kössl, M., Frank, G., Burda, H., Müller, M., 1996. Acoustic distortion products from the cochlea of the blind African mole rat, Cryptomys spec. J. Comp. Physiol. A 178, 427–434.

    PubMed  Google Scholar 

  • Lange, S., Burda, H., 2005. Comparative and functional morphology of the middle ear in Zambezian mole-rats (Coetomys-Cryptomys, Bathyergidae). Belgian J. Zoology 135 (Suppl), 5–10.

    Google Scholar 

  • Lange, S., Stalleicken, J., Burda, H., 2004. Functional morphology of the ear in fossorial rodents, Microtus arvalis and Arvicola terrestris.. Morph. 262, 770–779.

    Google Scholar 

  • Lange, S., Burda, H., Wegner, R.E., Dammann, P., Begall, S., Kawalika, M., 2007. Living in a “stethoscope”: burrow acoustics promote auditory specializations in subterranean rodents. Naturwissenschaften 94, 134–138.

    CAS  PubMed  Google Scholar 

  • Liberman, M., 1982. The cochlear frequency map for the cat: labeling auditory-nerve fibers of known characteristic frequency. J. Acoust. Soc. Am. 72 (5), 1441–1449.

    CAS  PubMed  Google Scholar 

  • Lovell, J.M., Harper, G.M., 2007. The morphology of the inner ear from the domestic pig (Sus scrofa).. Microsc. 228 (3), 345–357.

    CAS  Google Scholar 

  • Mason, M.J., 2001. Middle ear structures in fossorial mammals: A comparison with non- fossorial species. J. Zool. (Lond.) 255, 467–486.

    Google Scholar 

  • Mason, M.J., Lai, F.W.S., Li, J.G., Nevo, E., 2010. Middle ear structure and bone conduction in Spalax, Eospaiax, and Tachyoryctes Mole-rats (Rodentia: Spalacidae). J. Morph, 462–472.

    Google Scholar 

  • Mason, M.J., Cornwall, H.L., Smith, E.S.J., 2016. Ear structures of the naked mole-rat, Heterocephalus glaber, and its relatives (Rodentia: Bathyergidae). PLoS One (12), e0167079, https://doi.org/10.1371/journal.pone.0167079.

    Google Scholar 

  • Müller, M., 1996. The cochlear place-frequency map of the adult and developing Mongolian gerbil. Hear. Res. 94, 148–156.

    PubMed  Google Scholar 

  • Müller, M., Burda, H., 1989. Restricted hearing range in a subterranean rodent, Cryptomys hottentotus (Bathyergidae). Naturwissenschaften 76, 134–135.

    PubMed  Google Scholar 

  • Müller, M., Laube, B., Burda, H., Bruns, V., 1992. Structure and function of the cochlea in the African mole rat (Cryptomys hottentotus): evidence for a low frequency acoustic fovea. J. Comp. Physiol. 171, 469–476.

    Google Scholar 

  • Musser, G.G., Carleton, M.D., 2005. Superfamily muroidea. In: Wilson, D.E., Reeder, D.M. (Eds.), Mammal Species of the World: ATaxonomic and Geographic Reference. The Johns Hopkins University Press, Baltimore, p. 2142.

    Google Scholar 

  • Nevo, E., 1979. Adaptive convergence and divergence of subterranean mammals. Annu. Rev. Ecol. Syst. 10, 269–308.

    Google Scholar 

  • Nevo, E., 1999. Mosaic Evolution of Subterranean Mammals (Regression, Progression and Convergence). Oxford University Press, Oxford.

    Google Scholar 

  • Nienhuys, T.G.W., Clark, G.M., 1978. Frequency discrimination following the selective destruction of cochlear inner and outer hair cells. Science 199, 1356–1357.

    CAS  PubMed  Google Scholar 

  • Ou, H.C., Harding, G.W., Bohne, B.A., 2000. An anatomically based frequency-place map for the mouse cochlea. Hear. Res. 145, 123–129.

    CAS  PubMed  Google Scholar 

  • Pepper, J.W., Braude, S.H., Lacey, E.A., Sherman, P.W., 1991. Vocalizations of the naked mole-rat. In: Sherman, P.W., Jarvis, J.U.M., Alexander, R.D. (Eds.), The Biology of the Naked Mole-Rat. Princeton University Press, Princeton, pp. 243–274.

    Google Scholar 

  • Pleštilová, L., Hrouzková, E., Burda, H., šumbera, R., 2016. Does the morphology of the ear of the Chinese bamboo rat (Rhizomys sinensis) show ‘subterranean’ characteristics? J. Morph. 277 (5), 575–584.

    PubMed  Google Scholar 

  • Pye, A., 1977. Structure of cochlea in some myomorph and caviomorph rodents. J. Zool., 309–321.

    Google Scholar 

  • Raphael, Y., Lenoir, M., Wroblewski, R., Pujol, R., 1991. The sensory epithelium and its innervation in the mole rat cochlea. J. Comp. Neurol. 314, 367–382.

    CAS  PubMed  Google Scholar 

  • Ren, T., Gillespie, P.G., 2007. A mechanism for active hearing. Curr. Opin. Neurobiol. 17(4), 498–503.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Robles, L., Ruggero, M.A., 2001. Mechanics of the mammalian cochlea. Physiol. Rev. 81 (3), 1305–1352.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Russell, I.J., Kössl, M., 1999. Micromechanical responses to tones in the auditory fovea of the greater mustached bat’s cochlea. J. Neurophysiol. 82 (2), 676–686.

    CAS  PubMed  Google Scholar 

  • Ryan, A., Dallos, P., 1975. Effect of absence of cochlear outer hair cells on behavioural auditory threshold. Nature 253, 44–46.

    CAS  PubMed  Google Scholar 

  • Salvi, R., Sun, W., Ding, D.L., Chen, G.D., Lobarinas, E., Wang, J., Radziwon, It, Auerbach, B.D., 2017. Inner hair cell loss disrupts hearing and cochlear function leading to sensory deprivation and enhanced central auditory gain. Front. Neurosci. 10, 621.

    PubMed  PubMed Central  Google Scholar 

  • Schleich, C.E., Busch, C., 2004. Functional morphology of the middle ear of Ctenomys taiarum (Rodentia: Octodontidae). J. Mammal. 85, 290–295.

    Google Scholar 

  • Schleich, C.E., Begall, S., Burda, H., 2006. Morpho-functional parameters of the inner ear in Ctenomys taiarum; Rodentia, Ctenomyidae. Folia Zool. 55, 264–272.

    Google Scholar 

  • Slepecky, N.B., 1996. Structure of the mammalian cochlea. In: Dallos, P., Popper, A.N., Fay, R.R. (Eds.), The Cochlea. Springer Handbook of Auditory Research. Springer, New York.

    Google Scholar 

  • Smith, A.T., Xie, Y., 2008. A Guide to the Mammals of China. Princeton University Press, Princeton.

    Google Scholar 

  • Teudt, I.G., Richter, C.P., 2007. The hemicochlea preparation of the guinea pig and other mammalian cochleae. J. Neurosci. Methods 162, 187–197.

    PubMed  Google Scholar 

  • Vanden Hole, C., Van Daele, P.A.A.G., Desmet, N., Devos, P., Adriaens, D., 2014. Does sociality imply a complex vocal communication system? A case study for Fukomys micklemi (Bathyergidae, Rodentia). Bioacoustics 23 (2), 143–160.

    Google Scholar 

  • Vater, M., Kössl, M., 2011. Comparative aspects of cochlear functional organization in mammals. Hear. Res. 273, 89–99.

    PubMed  Google Scholar 

  • Vater, M., Feng, A.S., Betz, M., 1985. An HRP-study of the frequency-place map of the horseshoe bat cochlea: morphological correlates of the sharp tuning to a narrow frequency band. J. Comp. Physiol. 157, 671–686.

    CAS  Google Scholar 

  • Veitl, S., Begall, S., Burda, H., 2000. Ecological determinants of vocalisation parameters: The case of the coruro Spalacopus cyanus (Octodontidae), a fossorial social rodent. Bioacoustics 11, 129–148.

    Google Scholar 

  • von Békésy, G., 1960. Experiments in Hearing. McGray-Hill, New York

    Google Scholar 

  • von Békésy, G., 1974. Introduction. In: Keidel, W.D., Neff, W.D. (Eds.), Handbook of Sensory Physiology. Vol. V/I: Auditory System, Anatomy, Physiology (Ear). Springer, Berlin, pp. 1–8.

    Google Scholar 

  • Wang, Z., Li, J., 2011. Hearing range of Myospalax cansu and Microtus oeconomus. Sichuan J. Zool. 30 (4), 612–615.

    Google Scholar 

  • Wang, Y., Steele, C.R., Puria, S., 2016. Cochlear outer-hair-cell power generation and viscous fluid loss. Sci. Rep. 6, 19475.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wannaprasert, T., 2016. Functional morphology of the ear of the lesser bamboo rat (Cannomys badius). Mammal Study 41 (3), 107–117.

    Google Scholar 

  • West, C.D., 1985. The relationship of the spiral turns of the cochlea and the length of the basilar membrane to the range of audible frequencies in ground dwelling mammals. J. Acoust. Soc. Am. 77, 1091–1101.

    CAS  PubMed  Google Scholar 

  • Wilson, D.E., Lácher Jr., T.E., Mittermeier, R.A., (Eds.), 2017. Handbook of the Mammals of the World - Volume 7. Rodents II Lynx Editions in association with Conservation International and IUCN, pp. 1008.

    Google Scholar 

  • Wu, X., Gao, J., Guo, Y., Zuo, J., 2004. Hearing threshold elevation precedes hair-cell loss in prestin knockout mice. Mol. Brain Res. 126, 30–37.

    CAS  PubMed  Google Scholar 

  • Zhang, Y., 2007. The biology and ecology of plateau zokors (eospalaxfontanierii). In: Begall, S., Burda, H., Schleich, C.E. (Eds.), Subterranean Rodents: News from Underground. Springer Verlag, Berlin.

    Google Scholar 

  • Zhang, Y., Zhang, Z., Liu, J., 2003. Burrowing rodents as ecosystem engineers: the ecology and management of plateau zokors Myospalax fontanierii in alpine meadow ecosystems on the Tibetan Plateau. Mammal. Rev. 33 (3), 284–394.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Zoology, Faculty of Science, University of South Bohemia, 37005, České Budějovice, Czech Republic

    Lucie Pleštilová, Ema Hrouzková, Hynek Burda & Radim šumbera

  2. Department of General Zoology, Faculty of Biology, University of Duisburg-Essen, 45117, Essen, Germany

    Hynek Burda

  3. Rangeland Sciences Department, Gansu Agricultural University, 730070, Lanzhou, China

    Limin Hua

  4. University of South Bohemia, Branisovská, 1760, 37005, České Budějovice, Czech Republic

    Lucie Pleštilová

Authors
  1. Lucie Pleštilová
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ema Hrouzková
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Hynek Burda
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Limin Hua
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Radim šumbera
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Lucie Pleštilová.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Pleštilová, L., Hrouzková, E., Burda, H. et al. Additional row of outer hair cells — The unique pattern of the Corti organ in a subterranean rodent, the Gansu zokor (Eospalax cansus). Mamm Biol 94, 11–17 (2019). https://doi.org/10.1016/j.mambio.2018.11.003

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1016/j.mambio.2018.11.003

Keywords

Search

Navigation