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The origin of spontaneous activity in the developing auditory system

Author

Listed:
  • Nicolas X. Tritsch

    (The Solomon H. Snyder Department of Neuroscience,)

  • Eunyoung Yi

    (The Center for Hearing and Balance, Johns Hopkins School of Medicine, Baltimore, Maryland 21205, USA)

  • Jonathan E. Gale

    (University College London)

  • Elisabeth Glowatzki

    (The Solomon H. Snyder Department of Neuroscience,
    The Center for Hearing and Balance, Johns Hopkins School of Medicine, Baltimore, Maryland 21205, USA)

  • Dwight E. Bergles

    (The Solomon H. Snyder Department of Neuroscience,
    The Center for Hearing and Balance, Johns Hopkins School of Medicine, Baltimore, Maryland 21205, USA)

Abstract

Spontaneous activity in the developing auditory system is required for neuronal survival as well as the refinement and maintenance of tonotopic maps in the brain. However, the mechanisms responsible for initiating auditory nerve firing in the absence of sound have not been determined. Here we show that supporting cells in the developing rat cochlea spontaneously release ATP, which causes nearby inner hair cells to depolarize and release glutamate, triggering discrete bursts of action potentials in primary auditory neurons. This endogenous, ATP-mediated signalling synchronizes the output of neighbouring inner hair cells, which may help refine tonotopic maps in the brain. Spontaneous ATP-dependent signalling rapidly subsides after the onset of hearing, thereby preventing this experience-independent activity from interfering with accurate encoding of sound. These data indicate that supporting cells in the organ of Corti initiate electrical activity in auditory nerves before hearing, pointing to an essential role for peripheral, non-sensory cells in the development of central auditory pathways.

Suggested Citation

  • Nicolas X. Tritsch & Eunyoung Yi & Jonathan E. Gale & Elisabeth Glowatzki & Dwight E. Bergles, 2007. "The origin of spontaneous activity in the developing auditory system," Nature, Nature, vol. 450(7166), pages 50-55, November.
    • Handle: RePEc:nat:nature:v:450:y:2007:i:7166:d:10.1038_nature06233
    DOI: 10.1038/nature06233
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    Cited by:

    1. Chao Chen & Linlin Sun & Avital Adler & Hang Zhou & Licheng Zhang & Lihai Zhang & Junhao Deng & Yang Bai & Jinhui Zhang & Guang Yang & Wen-Biao Gan & Peifu Tang, 2023. "Synchronized activity of sensory neurons initiates cortical synchrony in a model of neuropathic pain," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    2. A. Catalina Vélez-Ortega & Ruben Stepanyan & Stephanie E. Edelmann & Sara Torres-Gallego & Channy Park & Desislava A. Marinkova & Joshua S. Nowacki & Ghanshyam P. Sinha & Gregory I. Frolenkov, 2023. "TRPA1 activation in non-sensory supporting cells contributes to regulation of cochlear sensitivity after acoustic trauma," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    3. Barbara Trattner & Céline Marie Gravot & Benedikt Grothe & Lars Kunz, 2013. "Metabolic Maturation of Auditory Neurones in the Superior Olivary Complex," PLOS ONE, Public Library of Science, vol. 8(6), pages 1-14, June.

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