The Postsynaptic Function of Type II Cochlear Afferents

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 (IHCs) 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 caliber axons, have made them the subject of much speculation, but little experimental progress for the past 50 years. Here we record from Type II fibers near their terminal arbors under OHCs to show that these receive excitatory glutamatergic synaptic input. The Type II peripheral arbor conducts action potentials, but the small and infrequent glutamatergic excitation implies a requirement for strong acoustic stimulation. Further, we show that Type II neurons are excited by adenosine tri-phosphate (ATP). Exogenous ATP depolarized Type II neurons both directly, and by evoking glutamatergic synaptic input 5. The present 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 signaling from that of Type I afferents.