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Presynaptic maturation in auditory hair cells requires a critical period of sensory-independent spiking activity
Stuart L. Johnson, Stephanie Kuhn, Christoph Franz, Neil Ingham, David N. Furness, Marlies Knipper, Karen P. Steel, John P. Adelman, Matthew C. Holley and Walter Marcotti
Proceedings of the National Academy of Sciences of the United States of America
Vol. 110, No. 21 (May 21, 2013), pp. 8720-8725
Published by: National Academy of Sciences
Stable URL: http://www.jstor.org/stable/42656789
Page Count: 6
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The development of neural circuits relies on spontaneous electrical activity that occurs during immature stages of development. In the developing mammalian auditory system, spontaneous calcium action potentials are generated by inner hair cells (IHCs), which form the primary sensory synapse. It remains unknown whether this electrical activity is required for the functional maturation of the auditory system. We found that sensory-independent electrical activity controls synaptic maturation in IHCs. We used a mouse model in which the potassium channel SK2 is normally overexpressed, but can be modulated in vivo using doxycycline. SK2 overexpression affected the frequency and duration of spontaneous action potentials, which prevented the development of the Ca²⁺-sensitivity of vesicle fusion at IHC ribbon synapses, without affecting their morphology or general cell development. By manipulating the in vivo expression of SK2 channels, we identified the "critical period" during which spiking activity influences IHC synaptic maturation. Here we provide direct evidence that IHC development depends upon a specific temporal pattern of calcium spikes before sound-driven neuronal activity.
Proceedings of the National Academy of Sciences of the United States of America © 2013 National Academy of Sciences