Cochlear nerve projections to the small cell shell of the cochlear nucleus: The neuroanatomy of extremely thin sensory axons

Abstract

Labeling cochlear nerve fibers in the inner ear of chinchillas with biotinylated dextran polyamine was used to trace the thin fibers (Type II), which likely innervate outer hair cells. These axons, 0. 1-0.5 microm in diameter, were distinguished from the thicker Type I, fibers innervating inner hair cells, and traced to small-cell clusters in the cochlear nucleus. This study provided two major new insights into the outer hair cell connections in the cochlear nucleus and the potential significance of very thin axons and synaptic nests, which are widespread in the CNS. 1) EM serial reconstructions of labeled and unlabeled material revealed that Type II axons rarely formed synapses with conventional features (vesicles gathered at junctions). Rather, their endings contained arrays of endoplasmic reticulum and small spherical vesicles without junctions. 2) Type II axons projected predominantly to synaptic nests, where they contacted other endings and dendrites of local interneurons (small stellate and mitt cells, but not granule cells). Synaptic nests lacked intrinsic glia and, presumably, their high-affinity amino acid transporters. As functional units, nests and their Type II inputs from outer hair cells may contribute to an analog processing mode, which is slower, more diffuse, longer-lasting, and potentially more plastic than the digital processors addressed by inner hair cells.

Synaptic nests lack glutamate transporters in the cochlear nucleus of the mouse

“…These macronests occur within the core of the cochlear nucleus as well as being concentrated in the small cell shell. These findings agree with those for cat (Kane, 1973(Kane, , 1974 and chinchilla (Hutson and Morest, 1996;Hurd et al, 1999). Typically, the nest contains many synaptic endings, whose nonjunctional surfaces directly contact each other and share a common extracellular space devoid of glial processes.…”

Fine structure of degeneration in the cochlear nucleus of the chinchilla after acoustic overstimulation

“…The same four cytological types of synaptic endings occur in the PVCN‐A in the chinchilla as described previously in the anteroventral cochlear nucleus (Josephson and Morest, 1998). Type 1 endings with large round vesicles and highly asymmetric synaptic junctions presumably represent the cochlear nerve endings, as demonstrated previously with tracers labeling the cochlear nerve of cats and chinchillas (Jones et al, 1992; Hurd et al, 1999). Synaptic terminals characteristic of mossy fiber endings, filled with swarms of well‐distributed if rather irregularly clustered, round, but smaller vesicles, have been described previously in the small cell shell of the chinchilla cochlear nucleus (Hutson and Morest, 1996; Hurd et al, 1999) and in the dorsal cochlear nucleus (e.g., Kane, 1974a; Rubio and Juiz, 1998).…”

“…Some of these endings shared features described for the glutamatergic synaptic endings of Type II cochlear nerve fibers in the chinchilla (e.g., Fig. 5 and 6; PTA) (Hurd et al, 1999), but most must represent endings of central interneurons. In the present study, we have not attempted to distinguish varieties of this ending type.…”

Organization of inhibitory feed-forward synapses from the dorsal to the ventral cochlear nucleus in the cat: a quantitative analysis of endings by vesicle morphology

“…The very small round type includes type two cochlear nerve endings (Hurd et al, 1999), which are glutamatergic endings (Jones et al, 1984). The examples labeled in the present findings would result from the retrograde/ anterograde sequence similar to that seen for the type one cochlear nerve endings.…”