Letter

Nature 461, 1126-1129 (22 October 2009) | doi:10.1038/nature08487; Received 29 May 2009; Accepted 7 September 2009

The postsynaptic function of type II cochlear afferents

Catherine Weisz1, Elisabeth Glowatzki1,2 & Paul Fuchs1,2

  1. The Department of Neuroscience,
  2. The Department of Otolaryngology-Head and Neck Surgery, The Center for Hearing and Balance and the Center for Sensory Biology, Johns Hopkins University School of Medicine, Baltimore, Maryland 21205, USA

Correspondence to: Paul Fuchs1,2 Correspondence and requests for materials should be addressed to P.F. (Email: pfuchs1@jhmi.edu).

The mammalian cochlea is innervated by two classes of sensory neurons. Type I neurons make up 90–95% of the cochlear nerve and contact single inner hair cells to provide acoustic analysis as we know it. In contrast, the far less numerous type II neurons arborize extensively among outer hair cells (OHCs)1, 2 and supporting cells3, 4. Their scarcity and smaller calibre axons have made them the subject of much speculation, but little experimental progress for the past 50 years. Here we record from type II fibres near their terminal arbors under OHCs to show that they receive excitatory glutamatergic synaptic input. The type II peripheral arbor conducts action potentials, but the small and infrequent glutamatergic excitation indicates a requirement for strong acoustic stimulation. Furthermore, we show that type II neurons are excited by ATP. Exogenous ATP depolarized type II neurons, both directly and by evoking glutamatergic synaptic input5. These results prove that type II neurons function as cochlear afferents, and can be modulated by ATP. The lesser magnitude of synaptic drive dictates a fundamentally different role in auditory signalling from that of type I afferents.

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