Diversity of axonal ramifications belonging to single lateral and medial olivocochlear neurons

A classification of olivocochlear (OC) neurons based on their location in either the lateral or medial region of the superior olivary complex provides a powerful tool for predicting their terminations beneath the inner (IHC) or outer hair cells (OHC) of the cochlea, respectively. Yet the morphology of axonal terminations belonging to single lateral OC (LOC) and medial OC (MOC) neurons, which can provide clues about the functional capabilities of individual efferent neurons, has been relatively unexplored. Following injections of biotinylated dextran amine into regions containing OC neurons in the rat, we reconstructed 19 LOC and 15 MOC axons in surface preparations of the cochlea. Confirming previous studies, LOC axons could be classified as either intrinsic or shell based on the length (short versus long) of their terminal ramifications beneath the IHC. However, intrinsic LOC axons were of two types, those that traveled to the organ of Corti without branching (simple intrinsic) and those that had three or more branches that converged on the same discrete patch of IHCs (converging intrinsic). Regarding shell neurons, we found that they may have as many as four intraganglionic branches that could innervate as much as 41% of cochlear length. Lastly, we found that MOC neurons were extremely diverse, not only in the number of their tunnel-crossing fibers (1-15), but also in both the number of boutons they formed (1-48) and in their basal-apical spans (1-45%). Analysis revealed that the number of tunnel-crossing fibers formed by a given axon was closely related to the total number of its terminal boutons, but not to its cochlear span. Analysis further suggested the existence of two distinct subtypes of MOC neurons on the basis of the number of tunnel-crossing fibers and boutons each possessed: the more common sparsely-branched and the quite rare highly-branched MOC neurons. In conclusion, the variety of axonal ramifications of individual LOC and MOC neurons has functional implications and raises the question of whether the various types of efferent neurons might be subject to selective control by ascending and descending central auditory and possibly non-auditory pathways.