Neuron
Volume 82, Issue 4, 21 May 2014, Pages 822-835
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Article
The Precise Temporal Pattern of Prehearing Spontaneous Activity Is Necessary for Tonotopic Map Refinement

https://doi.org/10.1016/j.neuron.2014.04.001Get rights and content
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Highlights

  • Deletion of nicotinic α9 subunit alters spontaneous activity in auditory system

  • α9 KO mice have impaired refinement of an inhibitory tonotopic map

  • Imprecise tonotopy in α9 KO mice is present on functional and structural levels

Summary

Patterned spontaneous activity is a hallmark of developing sensory systems. In the auditory system, rhythmic bursts of spontaneous activity are generated in cochlear hair cells and propagated along central auditory pathways. The role of these activity patterns in the development of central auditory circuits has remained speculative. Here we demonstrate that blocking efferent cholinergic neurotransmission to developing hair cells in mice that lack the α9 subunit of nicotinic acetylcholine receptors (α9 KO mice) altered the temporal fine structure of spontaneous activity without changing activity levels. KO mice showed a severe impairment in the functional and structural sharpening of an inhibitory tonotopic map, as evidenced by deficits in synaptic strengthening and silencing of connections and an absence in axonal pruning. These results provide evidence that the precise temporal pattern of spontaneous activity before hearing onset is crucial for the establishment of precise tonotopy, the major organizing principle of central auditory pathways.

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Co-first author

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Present address: Eaton-Peabody Laboratory, Massachusetts Eye and Ear Infirmary, Department of Otology and Laryngology, Harvard Medical School, Boston, MA 02114, USA

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Present address: Department of Physiology, Center for Integrative Neuroscience, University of California San Francisco, San Francisco, CA 94143-0444, USA