Efferent innervation of the inner hair cell region: origins and terminations of two lateral olivocochlear systems

Abstract

The projections of lateral olivocochlear neurons (LOC), which terminate beneath inner hair cells (IHCs), were investigated by injecting biotinylated dextran amine into the lateral superior olivary nucleus (LSO) and the surrounding region in the rat. This region has been definitively shown to contain two types of olivocochlear neurons: small cells within the LSO (intrinsic neurons) and large cells (shell neurons) surrounding it (Vetter, D.E., Mugnaini, E., 1992. Distribution and dendritic features of three groups of rat olivocochlear neurons. Anat. Embryol. 185, 1-16). Labeled efferent axons were studied by light microscopy in whole mounts and radial sections of the organ of Corti (OC). It was found that injections confined to the LSO, which presumably affected mainly intrinsic neurons, labeled a cluster of axons in the osseous spiral lamina that entered the inner spiral bundle (ISB) and terminated in one or more dense patches that, in total basal-apical extent, spanned no more than 10-20% (1-2 mm) of the total length of the OC (10 mm). In contrast, injections affecting shell neurons produced labeled axons that entered the OC over a span of more than 50% of its length and which, as a group, coursed in the ISB for at least 80%, and sometimes more than 95% of total cochlear length. Study of individual axons in the OC revealed that intrinsic axons did not bifurcate upon entering the OC and traveled less than 1 mm before terminating in a discrete, dense arbor. In contrast, shell axons typically bifurcated into basal and apical branches that, in toto, traveled between 1 and 2 mm beneath the IHCs, forming numerous en passant swellings and a few terminal branches en route. The fact that localized injections of intrinsic neurons produced focal peaks of labeling in the cochlea, whereas similar injections of shell neurons produced a diffuse, non-focal projection that could extend for nearly the entire length of the cochlea, suggests that significant differences exist between these two populations in their capacity to influence localized, frequency-specific regions of the OC, and thus in their probable functional roles. The present findings in the rat not only confirm a previous study in the guinea pig which found a similar dual efferent innervation beneath the IHCs (Brown, M.C., 1987. Morphology of labeled efferent fibers in the guinea pig cochlea. J. Comp. Neurol. 260, 605-618), but extend those observations by linking two axonal types beneath the IHCs to their respective cell bodies of origin in the lateral zone of the superior olivary complex.