Intracellular labeling of auditory nerve fibers in guinea pig: central and peripheral projections

Auditory-nerve fibers (ANFs) in the cat have been subdivided according to spontaneous rate (SR), with high-SR fibers showing the lowest thresholds. Cochlear terminals of the three SR groups differ in caliber and synaptic position around the inner hair cell (Liberman [1982b] Science 216:1239-1241); central terminals differ in degree of branching and in which subregions of the cochlear nucleus (CN) are targeted (Liberman [1991] J. Comp. Neurol. 313:240-258). The present study investigates whether these SR-based differences in ANF connections are unique to the cat. Thirty ANFs from 15 guinea pigs were intracellularly labeled after measuring characteristic frequency, threshold, and SR. Labeled cochlear projections showed significant SR-based differences in axonal caliber, with low- and medium-SR fibers 20-40% thinner than those of high-SR fibers for both peripheral and central (modiolar) axons. Spatial segregation in the inner hair cell area could not be assessed; however, the peripheral axons in the osseous spiral lamina showed the same SR-based organization reported for the cat (Kawase and Liberman [1992] J. Comp. Neurol. 319:312-318). Labeled central projections also showed significant SR-based differences. Low- and medium-SR fibers: 1) were more highly branched, 2) sent significantly more terminals to the small-cell cap region of the CN, and 3) produced endbulb terminals (on spherical cells) that were significantly more complex than high-SR fibers. All of these SR-based trends for both central and peripheral projections are analogous to those reported in the cat, and, thus, may represent a fundamental organizational principle of the mammalian ear.