Outer hair cells (OHCs) are key elements of the mammalian hearing system, since they enable signal amplification and frequency discrimination. OHCs are innervated by olivocochlear (OC) and type-II spiral ganglion neurons.

The function of type-IIs is unknown. It has been suggested that they interconnect neighboring OHCs through reciprocal synapses, which are bi-directional (afferent and efferent) synapses between terminals and OHCs. Such interconnection among neighboring OHCs has never been demonstrated and was thought to be limited to primates. Type-IIs are also innervated by OC neurons (OC/type-II synapses), but this innervation has not been well characterized.

Serial section transmission electron microscopy was used to study the synapses of type-II neurons with OHCs and OC neurons. We analyzed humans and also cats, which are frequently used as experimental model of human hearing.

Nerve terminals with reciprocal synapses were processes of type-IIs, and not of OC neurons. Reciprocal type-II terminals were found in all studied frequency regions in the cat, but were most prevalent below 4,000Hz. Reciprocal synapses varied between predominantly afferent or efferent, and all the type-II fibers traced to more than one OHC in the cat presented reciprocal synapses. OC/type-II synapses were prevalent.

Type-II neurons have reciprocal synaptic interactions with OHCs and form an “outer spiral network”, which may functionally integrate the OHCs. The OC system may modulate this network through OC/type-II synapses. The outer spiral network and its innervation by the OC system seem to be relevant to OHC function, and further research is needed to determine their role in hearing.