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BioMed Research International
Volume 2014 (2014), Article ID 367939, 8 pages
http://dx.doi.org/10.1155/2014/367939
Review Article

Kölliker’s Organ and the Development of Spontaneous Activity in the Auditory System: Implications for Hearing Dysfunction

1Department of Physiology, Faculty of Medical and Health Sciences, The University of Auckland, Private Bag 92019, Auckland 1142, New Zealand
2Centre for Brain Research, Faculty of Medical and Health Sciences, The University of Auckland, Private Bag 92019, Auckland 1142, New Zealand
3Section of Audiology, Faculty of Medical and Health Sciences, The University of Auckland, Private Bag 92019, Auckland 1142, New Zealand

Received 30 May 2014; Accepted 7 August 2014; Published 20 August 2014

Academic Editor: Jonathan Gale

Copyright © 2014 M. W. Nishani Dayaratne et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. V. Hensen, “Zur morphologie der schnecke des menschen und der säugethiere,” Zeitschrift für Wissenschaftliche Zoologie, vol. 13, pp. 481–512, 1863. View at Google Scholar
  2. A. Kölliker, Handbuch der Gewebelehre des Menschen, Engelmann, 1902.
  3. D. J. Lim and M. Anniko, “Developmental morphology of the mouse inner ear. A scanning electron microscopic observation,” Acta Oto-Laryngologica, vol. 422, pp. 1–69, 1985. View at Google Scholar · View at Scopus
  4. L. Simonneau, M. Gallego, and R. Pujol, “Comparative expression patterns of T-, N-, E-cadherins, β-catenin, and polysialic acid neural cell adhesion molecule in rat cochlea during development: implications for the nature of Kölliker's organ,” The Journal of Comparative Neurology, vol. 459, no. 2, pp. 113–126, 2003. View at Publisher · View at Google Scholar · View at Scopus
  5. R. Pujol, M. Lavigne-Rebillard, and M. Lenoir, “Development of sensory and neural structures in the mammalian cochlea,” in Development of the Auditory System, E. W. Rubel, A. N. Popper, and R. R. Fay, Eds., vol. 9 of Springer Handbook of Auditory Research, pp. 146–192, Springer, New York, NY, USA, 1998. View at Google Scholar
  6. P. Majumder, G. Crispino, L. Rodriguez et al., “ATP-mediated cell-cell signaling in the organ of Corti: the role of connexin channels,” Purinergic Signalling, vol. 6, no. 2, pp. 167–187, 2010. View at Publisher · View at Google Scholar · View at Scopus
  7. W. Giebel and N. Wei, “The early postnatal development of the hamster cochlea,” Laryngo- Rhino- Otologie, vol. 80, no. 12, pp. 725–730, 2001. View at Publisher · View at Google Scholar · View at Scopus
  8. R. Hinojosa, “A note on development of Corti's organ,” Acta Oto-Laryngologica, vol. 84, no. 3-4, pp. 238–251, 1977. View at Google Scholar · View at Scopus
  9. D. J. Lim and M. Anniko, “Developmental morphology of the mouse inner ear. A scanning electron microscopic observation,” Acta Oto-Laryngologica, vol. 99, no. 422, 1985. View at Google Scholar · View at Scopus
  10. A. Zine and R. Romand, “Development of the auditory receptors of the rat: a SEM study,” Brain Research, vol. 721, no. 1-2, pp. 49–58, 1996. View at Publisher · View at Google Scholar · View at Scopus
  11. A. Uziel, J. Gabrion, M. Ohresser, and C. Legrand, “Effects of hypothyroidism on the structural development of the organ of Corti in the rat,” Acta Oto-Laryngologica, vol. 92, no. 5-6, pp. 469–480, 1981. View at Google Scholar · View at Scopus
  12. M. Anniko, “Embryogenesis of the mammalian middle ear. III. Formation of the tectorial membrane of the CBA/CBA mouse in vivo and in vitro,” Anatomy and Embryology, vol. 160, no. 3, pp. 301–313, 1980. View at Publisher · View at Google Scholar · View at Scopus
  13. M. Cohen-Salmon, F. J. del Castillo, and C. Petit, “Connexins responsible for hereditary deafness—the tale unfolds,” in Gap Junctions in Development and Disease, P. D. E. Winterhager, Ed., pp. 111–134, Springer, Berlin, Germany, 2005. View at Google Scholar
  14. A. Uziel, “Periods of sensitivity to thyroid hormone during the development of the organ of Corti,” Acta Oto-Laryngologica, vol. 102, no. 429, pp. 23–27, 1986. View at Google Scholar · View at Scopus
  15. C. Legrand, A. Bréhier, M. C. Clavel, M. Thomasset, and A. Rabié, “Cholecalcin (28-kDa CaBP) in the rat cochlea. Development in normal and hypothyroid animals. An immunocytochemical study,” Brain Research, vol. 466, no. 1, pp. 121–129, 1988. View at Google Scholar · View at Scopus
  16. A. N. Drury and A. Szent-Györgyi, “The physiological activity of adenine compounds with especial reference to their action upon the mammalian heart,” The Journal of Physiology, vol. 68, no. 3, pp. 213–237, 1929. View at Google Scholar
  17. G. Burnstock, “Purinergic receptors,” Journal of Theoretical Biology, vol. 62, no. 2, pp. 491–503, 1976. View at Publisher · View at Google Scholar · View at Scopus
  18. G. D. Housley, A. Bringmann, and A. Reichenbach, “Purinergic signaling in special senses,” Trends in Neurosciences, vol. 32, no. 3, pp. 128–141, 2009. View at Publisher · View at Google Scholar · View at Scopus
  19. G. Burnstock and C. Kennedy, “Is there a basis for distinguishing two types of P2-purinoceptor?” General Pharmacology: The Vascular System, vol. 16, no. 5, pp. 433–440, 1985. View at Google Scholar · View at Scopus
  20. M. P. Abbracchio, G. Burnstock, A. Verkhratsky, and H. Zimmermann, “Purinergic signalling in the nervous system: an overview,” Trends in Neurosciences, vol. 32, no. 1, pp. 19–29, 2009. View at Publisher · View at Google Scholar · View at Scopus
  21. A. Verkhratsky, “Physiology and pathophysiology of the calcium store in the endoplasmic reticulum of neurons,” Physiological Reviews, vol. 85, no. 1, pp. 201–279, 2005. View at Publisher · View at Google Scholar · View at Scopus
  22. M. P. Abbracchio, G. Burnstock, J.-M. Boeynaems et al., “International Union of Pharmacology LVIII: update on the P2Y G protein-coupled nucleotide receptors: from molecular mechanisms and pathophysiology to therapy,” Pharmacological Reviews, vol. 58, no. 3, pp. 281–341, 2006. View at Publisher · View at Google Scholar · View at Scopus
  23. L.-C. Huang, P. R. Thorne, S. M. Vlajkovic, and G. D. Housley, “Differential expression of P2Y receptors in the rat cochlea during development,” Purinergic Signalling, vol. 6, no. 2, pp. 231–248, 2010. View at Publisher · View at Google Scholar · View at Scopus
  24. L.-C. Huang, D. Greenwood, P. R. Thorne, and G. D. Housley, “Developmental regulation of neuron-specific P2X3 receptor expression in the rat cochlea,” Journal of Comparative Neurology, vol. 484, no. 2, pp. 133–143, 2005. View at Publisher · View at Google Scholar · View at Scopus
  25. K. Mou, C. L. Hunsberger, J. M. Cleary, and R. L. Davis, “Synergistic effects of BDNF and NT-3 on postnatal spiral ganglion neurons,” Journal of Comparative Neurology, vol. 386, no. 4, pp. 529–539, 1997. View at Publisher · View at Google Scholar
  26. U. Pirvola and J. Ylikoski, “Neurotrophic factors during inner ear development,” Current Topics in Developmental Biology, vol. 57, pp. 207–223, 2003. View at Google Scholar
  27. D. Greenwood, D. J. Jagger, L. Huang et al., “P2X receptor signaling inhibits BDNF-mediated spiral ganglion neuron development in the neonatal rat cochlea,” Development, vol. 134, no. 7, pp. 1407–1417, 2007. View at Publisher · View at Google Scholar · View at Scopus
  28. P. Nikolic, G. D. Housley, and P. R. Thorne, “Expression of the P2X7 receptor subunit of the adenosine 5′-triphosphate-gated ion channel in the developing and adult rat cochlea,” Audiology & Neuro-Otology, vol. 8, no. 1, pp. 28–37, 2003. View at Google Scholar · View at Scopus
  29. P. Nikolic, G. D. Housley, L. Luo, A. F. Ryan, and P. R. Thorne, “Transient expression of P2X1 receptor subunits of ATP-gated ion channels in the developing rat cochlea,” Developmental Brain Research, vol. 126, no. 2, pp. 173–182, 2001. View at Publisher · View at Google Scholar · View at Scopus
  30. N. X. Tritsch and D. E. Bergles, “Developmental regulation of spontaneous activity in the Mammalian cochlea,” Journal of Neuroscience, vol. 30, no. 4, pp. 1539–1550, 2010. View at Publisher · View at Google Scholar · View at Scopus
  31. S. L. Johnson, S. Kuhn, C. Franz et al., “Presynaptic maturation in auditory hair cells requires a critical period of sensory-independent spiking activity,” Proceedings of the National Academy of Sciences of the United States of America, vol. 110, no. 21, pp. 8720–8725, 2013. View at Publisher · View at Google Scholar · View at Scopus
  32. L. T. Landmesser and M. J. O'Donovan, “Activation patterns of embryonic chick hind limb muscles recorded in ovo and in an isolated spinal cord preparation,” The Journal of Physiology, vol. 347, pp. 189–204, 1984. View at Google Scholar · View at Scopus
  33. A. J. Watt, H. Cuntz, M. Mori, Z. Nusser, P. J. Sjöström, and M. Häusser, “Traveling waves in developing cerebellar cortex mediated by asymmetrical Purkinje cell connectivity,” Nature Neuroscience, vol. 12, no. 4, pp. 463–473, 2009. View at Publisher · View at Google Scholar · View at Scopus
  34. Y. Ben-Ari, E. Cherubini, R. Corradetti, and J.-L. Gaiarsa, “Giant synaptic potentials in immature rat CA3 hippocampal neurones,” The Journal of Physiology, vol. 416, pp. 303–325, 1989. View at Google Scholar · View at Scopus
  35. N. X. Tritsch, E. Yi, J. E. Gale, E. Glowatzki, and D. E. Bergles, “The origin of spontaneous activity in the developing auditory system,” Nature, vol. 450, no. 7166, pp. 50–55, 2007. View at Publisher · View at Google Scholar · View at Scopus
  36. W. R. Lippe, “Rhythmic spontaneous activity in the developing avian auditory system,” Journal of Neuroscience, vol. 14, no. 3, pp. 1486–1495, 1994. View at Google Scholar · View at Scopus
  37. T. A. Jones, S. M. Jones, and K. C. Paggett, “Primordial rhythmic bursting in embryonic cochlear ganglion cells,” The Journal of Neuroscience, vol. 21, no. 20, pp. 8129–8135, 2001. View at Google Scholar · View at Scopus
  38. M. Sonntag, B. Englitz, C. Kopp-Scheinpflug, and R. Rübsamen, “Early postnatal development of spontaneous and acoustically evoked discharge activity of principal cells of the medial nucleus of the trapezoid body: an in vivo study in mice,” The Journal of Neuroscience, vol. 29, no. 30, pp. 9510–9520, 2009. View at Publisher · View at Google Scholar · View at Scopus
  39. N. Dale, “Dynamic ATP signalling and neural development,” The Journal of Physiology, vol. 586, no. 10, pp. 2429–2436, 2008. View at Publisher · View at Google Scholar · View at Scopus
  40. C. J. Kros, J. P. Ruppersberg, and A. Rüsch, “Expression of a potassium current inner hair cells during development of hearing in mice,” Nature, vol. 394, no. 6690, pp. 281–284, 1998. View at Publisher · View at Google Scholar · View at Scopus
  41. N. X. Tritsch, Y. Zhang, G. Ellis-Davies, and D. E. Bergles, “ATP-induced morphological changes in supporting cells of the developing cochlea,” Purinergic Signalling, vol. 6, no. 2, pp. 155–166, 2010. View at Publisher · View at Google Scholar · View at Scopus
  42. S. L. Johnson, H. J. Kennedy, M. C. Holley, R. Fettiplace, and W. Marcotti, “The resting transducer current drives spontaneous activity in prehearing mammalian cochlear inner hair cells,” Journal of Neuroscience, vol. 32, no. 31, pp. 10479–10483, 2012. View at Publisher · View at Google Scholar · View at Scopus
  43. S. L. Johnson, T. Eckrich, S. Kuhn et al., “Position-dependent patterning of spontaneous action potentials in immature cochlear inner hair cells,” Nature Neuroscience, vol. 14, no. 6, pp. 711–717, 2011. View at Publisher · View at Google Scholar · View at Scopus
  44. G. Sendin, J. Bourien, F. Rassendren, J.-L. Puel, and R. Nouvian, “Spatiotemporal pattern of action potential firing in developing inner hair cells of the mouse cochlea,” Proceedings of the National Academy of Sciences, vol. 111, no. 5, pp. 1999–2004, 2014. View at Publisher · View at Google Scholar
  45. A. Forge, D. Becker, S. Casalotti, J. Edwards, N. Marziano, and G. Nevill, “Gap junctions in the inner ear: comparison of distribution patterns in different vertebrates and assessement of connexin composition in mammals,” Journal of Comparative Neurology, vol. 467, no. 2, pp. 207–231, 2003. View at Publisher · View at Google Scholar · View at Scopus
  46. H. B. Zhao, “Connexin26 is responsible for anionic molecule permeability in the cochlea for intercellular signalling and metabolic communications,” European Journal of Neuroscience, vol. 21, no. 7, pp. 1859–1868, 2005. View at Publisher · View at Google Scholar · View at Scopus
  47. F. Anselmi, V. H. Hernandez, G. Crispino et al., “ATP release through connexin hemichannels and gap junction transfer of second messengers propagate Ca2+ signals across the inner ear,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 48, pp. 18770–18775, 2008. View at Publisher · View at Google Scholar · View at Scopus
  48. D. C. Spray, Z. C. Ye, and B. R. Ransom, “Functional connexin “hemichannels”: a critical appraisal,” Glia, vol. 54, no. 7, pp. 758–773, 2006. View at Publisher · View at Google Scholar · View at Scopus
  49. X. Wang, M. Streeter, Y. Liu, and H. Zhao, “Identification and characterization of pannexin expression in the mammalian cochlea,” Journal of Comparative Neurology, vol. 512, no. 3, pp. 336–346, 2009. View at Publisher · View at Google Scholar · View at Scopus
  50. Y. Tamagawa, K. Kitamura, T. Ishida et al., “A gene for a dominant form of non-syndromic sensorineural deafness (DFNA11) maps within the region containing the DFNB2 recessive deafness gene,” Human Molecular Genetics, vol. 5, no. 6, pp. 849–852, 1996. View at Publisher · View at Google Scholar · View at Scopus
  51. J. E. Gale, V. Piazza, C. D. Ciubotaru, and F. Mammano, “A mechanism for sensing noise damage in the inner ear,” Current Biology, vol. 14, no. 6, pp. 526–529, 2004. View at Publisher · View at Google Scholar · View at Scopus
  52. V. Piazza, C. D. Ciubotaru, J. E. Gale, and F. Mammano, “Purinergic signalling and intercellular Ca2+ wave propagation in the organ of Corti,” Cell Calcium, vol. 41, no. 1, pp. 77–86, 2007. View at Publisher · View at Google Scholar · View at Scopus
  53. J. F. Ashmore and H. Ohmori, “Control of intracellular calcium by ATP in isolated outer hair cells of the guinea-pig cochlea,” The Journal of Physiology, vol. 428, pp. 109–131, 1990. View at Google Scholar · View at Scopus
  54. L. Lagostena, J. F. Ashmore, B. Kachar, and F. Mammano, “Purinergic control of intracellular communication between Hensen's cells of the guinea-pig cochlea,” Journal of Physiology, vol. 531, no. 3, pp. 693–706, 2001. View at Publisher · View at Google Scholar · View at Scopus
  55. S. M. Vlajkovic, P. R. Thorne, G. D. Housley, D. J. B. Muñoz, and I. S. Kendrick, “Ecto-nucleotidases terminate purinergic signalling in the cochlear endolymphatic compartment,” NeuroReport, vol. 9, no. 7, pp. 1559–1565, 1998. View at Google Scholar · View at Scopus
  56. Y. Zhu and H. Zhao, “ATP activates P2X receptors to mediate gap junctional coupling in the cochlea,” Biochemical and Biophysical Research Communications, vol. 426, no. 4, pp. 528–532, 2012. View at Publisher · View at Google Scholar · View at Scopus
  57. H. M. Sobkowicz, J. M. Loftus, and S. M. Slapnick, “Tissue culture of the organ of Corti,” Acta Oto-Laryngologica, vol. 502, pp. 3–36, 1993. View at Google Scholar · View at Scopus
  58. T. A. Fiacco and K. D. McCarthy, “Astrocyte calcium elevations: properties, propagation, and effects on brain signaling,” Glia, vol. 54, no. 7, pp. 676–690, 2006. View at Publisher · View at Google Scholar · View at Scopus
  59. R. Glueckert, G. Wietzorrek, K. Kammen-Jolly et al., “Role of class D L-type Ca2+ channels for cochlear morphology,” Hearing Research, vol. 178, no. 1-2, pp. 95–105, 2003. View at Publisher · View at Google Scholar · View at Scopus
  60. A. Brandt, J. Striessnig, and T. Moser, “CaV1.3 channels are essential for development and presynaptic activity of cochlear inner hair cells,” Journal of Neuroscience, vol. 23, no. 34, pp. 10832–10840, 2003. View at Google Scholar · View at Scopus
  61. E. Yi, J. Lee, and C. Lee, “Developmental role of anoctamin-1/TMEM16A in Ca2+-dependent volume change in supporting cells of the mouse Cochlea,” Experimental Neurobiology, vol. 22, no. 4, pp. 322–329, 2013. View at Google Scholar
  62. S. J. Hwang, P. J. A. Blair, F. C. Britton et al., “Expression of anoctamin 1/TMEM16A by interstitial cells of Cajal is fundamental for slow wave activity in gastrointestinal muscles,” Journal of Physiology, vol. 587, no. 20, pp. 4887–4904, 2009. View at Publisher · View at Google Scholar · View at Scopus
  63. J. B. Hochman, T. L. Stockley, D. Shipp, V. Y. W. Lin, J. M. Chen, and J. M. Nedzelski, “Prevalence of Connexin 26 (GJB2) and Pendred (SLC26A4) mutations in a population of adult cochlear implant candidates,” Otology and Neurotology, vol. 31, no. 6, pp. 919–922, 2010. View at Publisher · View at Google Scholar · View at Scopus
  64. Y. Sun, W. Tang, Q. Chang, Y. Wang, W. Kong, and X. Lin, “Connexin30 null and conditional connexin26 null mice display distinct pattern and time course of cellular degeneration in the cochlea,” The Journal of Comparative Neurology, vol. 516, no. 6, pp. 569–579, 2009. View at Publisher · View at Google Scholar · View at Scopus
  65. Y. Takada, L. Beyer, D. Swiderski et al., “Connexin 26 null mice exhibit spiral ganglion degeneration that can be blocked by BDNF gene therapy,” Hearing Research, vol. 309, pp. 124–135, 2014. View at Google Scholar
  66. M. Schütz, P. Scimemi, P. Majumder et al., “The human deafness-associated connexin 30 T5M mutation causes mild hearing loss and reduces biochemical coupling among cochlear non-sensory cells in knock-in mice,” Human Molecular Genetics, vol. 19, no. 24, pp. 4759–4773, 2010. View at Publisher · View at Google Scholar · View at Scopus
  67. L. Rodriguez, E. Simeonato, P. Scimemi et al., “Reduced phosphatidylinositol 4,5-bisphosphate synthesis impairs inner ear Ca2+ signaling and high-frequency hearing acquisition,” Proceedings of the National Academy of Sciences of the United States of America, vol. 109, no. 35, pp. 14013–14018, 2012. View at Publisher · View at Google Scholar · View at Scopus
  68. M. Vanderschueren-Lodeweyckx, F. Debruyne, L. Dooms, E. Eggermont, and R. Eeckels, “Sensorineural hearing loss in sporadic congenital hypothyroidism,” Archives of Disease in Childhood, vol. 58, no. 6, pp. 419–422, 1983. View at Publisher · View at Google Scholar · View at Scopus
  69. F. Brucker-Davis, M. C. Skarulis, A. Pikus et al., “Prevalence and mechanisms of hearing loss in patients with resistance to thyroid hormone,” The Journal of Clinical Endocrinology and Metabolism, vol. 81, no. 8, pp. 2768–2772, 1996. View at Publisher · View at Google Scholar · View at Scopus
  70. F. W. Newell and K. R. Diddie, “Typical monochromacy, congenital deafness, and resistance to intracellular action of thyroid hormone (author's transl),” Klinische Monatsblatter fur Augenheilkunde, vol. 171, no. 5, pp. 731–734, 1977. View at Google Scholar · View at Scopus
  71. L. Ng, M. W. Kelley, and D. Forrest, “Making sense with thyroid hormone-the role of T 3 in auditory development,” Nature Reviews Endocrinology, vol. 9, no. 5, pp. 296–307, 2013. View at Publisher · View at Google Scholar · View at Scopus