The outer spiral network and its innervation by the olivocochlear system

Abstract

Outer hair cells (OHCs) are key elements of the mammalian hearing system, which amplify sound-evoked signals transmitted into the inner ear. OHCs are innervated by peripheral projections of olivocochlear (OC) and type-II spiral ganglion neurons. Type-II neurons innervate up to 100 OHCs, but their function is unknown. It has been suggested that type-II neurons interconnect neighboring OHCs through reciprocal synapses, which are bi-directional (afferent and efferent) synaptic interactions (Nadol, 1981). Since reciprocal synapses on the OHCs have been shown to be prevalent only in aged primates, they were thought to be a pathological finding. In addition to their interactions with OHCs, type-II neurons are also innervated by OC neurons. Synapses between OC and type-II neurons (OC/type-II synapses) have been described (Smith and Rasmussen, 1963), but these interactions have not been characterized in detail. Serial and semi-serial section transmission electron microscopy were used to study the synaptic interactions of type-II neurons with OHCs and OC neurons in a young human and in adult cats. A high prevalence of nerve terminals with reciprocal synapses was observed in the young human and in adult cats. These reciprocal terminals were processes of type-IIs, and not of OC neurons. Reciprocal type-II terminals were found in all frequency regions studied in cats, but were most prevalent below 4,000Hz. All the type-II fibers traced to more than one OHC in an adult cat had reciprocal interactions with OHCs. Type-II fibers/terminals were heavily innervated by OC neurons, which preferentially targeted terminals with reciprocal synapses that were predominantly afferent in an adult cat.

(cont.) The innervation patterns of type-IIs and OC neurons in the cat were similar to that found in comparable frequency regions of primates. 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.