Topographic Organization of Inner Hair Cell Synapses and Cochlear Spiral Ganglion Projections to the Ventral Cochlear Nucleus

Abstract

In the mammalian cochlea, the somata of the primary afferent auditory neurons are arranged in an irregular spiral channel (Rosenthal’s canal) within the bone of the modiolus, and comprise the spiral ganglion. The spiral organization of the ganglion parallels that of the basilar membrane. Approximately 95% of the cells are myelinated type I ganglion cells which exclusively innervate the inner hair cells of the organ of Corti (Spoendlin,’ 71; Spoendlin,’ 83). Each inner hair cell receives up to 30 afferent terminals, with each terminal connecting via an unbranched radial nerve fiber to a single spiral ganglion cell (Spoendlin,’ 71; Spoendlin,’ 73; Kiang et al.,’ 82; Kiang et al.,’ 84; Liberman et al.,’ 90). The central axons of the bipolar type I spiral ganglion cells come together within the core of the modiolus to form the auditory nerve, which projects in a highly organized manner to each subdivision of the cochlear nuclear complex (Lorente de No,’ 81; Powell and Cowan,’ 62; Arnesen and Osen,’ 78). Within the ventral cochlear nucleus (VCN), auditory nerve fibers from the base of the cochlea project dorsally, and progressively more apical cochlear sectors project more ventrally, thus providing the morphological basis for the tonotopic organization of the VCN which is well-known from electrophysiological recording experiments. That is, neurons in the dorsal part of the anteroventral cochlear nucleus (AVCN) respond best to high-frequency tonal stimuli, while those in progressively more ventral areas respond maximally to progressively lower frequencies (Rose et al.,’ 60; Bourk et al.,’ 81). A detailed map of the AVCN frequency organization was provided by Bourk et al.’ 81, and their data suggested that the AVCN is organized in “isofrequency laminae.” Each isofrequency lamina comprises a thin sheet that extends across the AVCN to its boundaries and presumably receives selective input from a spatially restricted cochlear sector. A number of morphological studies have supported this concept of a laminar organization of the VCN, demonstrating that auditory nerve fibers arising from restricted cochlear sectors project in laminae in the VCN in an orderly and sequential arrangement based on cochlear location (i.e., frequency), (Osen,’ 70; Webster,’ 71; Webster et al.,’ 78; Ryan et al.,’ 82; Nudo and Masterton,’ 84).