Properties of auditory nerve responses in absence of outer hair cells.

1. Recordings were made from chinchilla auditory nerve fibers after portions of the cochlear outer hair cell (OHC) population were destroyed with the antibiotic kanamycin. In most cases the inner hair cell (IHC) population was completely preserved as determined by phase-contrast microscopy. We presume that the remaining IHCs are functionally normal, and thus that recordings obtained from fibers originating from the lesioned cochlear segment reflect IHC behavior. 2. Behavioral thresholds were measured for all animals both before and after the production of the cochlear lesion. The audiograms and the histological evaluation of the ears were the basis for assessing whether a particular fiber originated in a normal, pathological (shifted threshold; IHC only), or border region. These criteria also identified the animals that sustained IHC damage together with the destruction of part of the OHC population. Only the data obtained from those fibers which probably originated from the OHC-free segment of the cochlea are considered in detail. 3. Fibers whose characteristic frequency (CF) identified them as belonging to the normal (audiometrically and histologically) region, were found to be normal in all respects. 4. Fibers from the border region (where the audiogram has a steep slope between normal and hearing-loss regions probably corresponding to the segment where OHC loss progresses from less than 10% to more than 90%) had very complex response patterns. Their frequency threshold curves (FTC) showed great variability. In general, the closer the fiber was to the fully developed lesion, the more abnormal its FTC became. 5. Those units that were concluded to have originated from the OHC-free part of the cochlea could be divided into three categories on the basis of the shape of their FTCs. A small fraction had very broad tuning (9%). The majority (53%) had approximately normal tail segment, normal bandwidth of the tip segment, and highly elevated threshold at CF. A group of fibers (38%) could not be assigned a CF. Probably the FTC of most of these latter fibers are similar to those of the previous group, but the sharply tuned short tip segment was either missed or was not reachable on account of its extremely high threshold level. 6. Such indexes of fiber response as latency, spontaneous rate, and time pattern (PST histograms) were not affected by the loss of OHCs. 7. On the basis of the data and of the assumptions made it was suggested that outer hair cells provide a frequency-dependent sensitizing influence to the inner hair cells. The frequency dependence could best be expressed as a flat-topped band pass characteristic.