Discharge properties of pigeon single auditory nerve fibers after recovery from severe acoustic trauma

Abstract

The time course of recovery of compound action potential (CAP) thresholds was observed in individual adult pigeons after severe acoustic trauma. Each bird had electrodes implanted on the round window of both ears. One ear was exposed to a tone of 0.7 kHz at 136–142 dB SPL for 1 hr under general anesthesia. Recovery of CAP audiograms was monitored twice a week after trauma. Single unit recordings from auditory nerve fibers were made after 3 weeks and after 4 or more months of the exposure. The CAP was abolished immediately after overstimulation in all animals. Based on the temporal patters of functional recovery of the CAP three groups of animals were identified. The first group was characterized by fast functional recovery starting immediately after trauma followed by a return to pre-exposure values within 3 weeks. In the second group, slow functional recovery of threshold started 1–2 weeks after trauma followed by a return to pre-exposure values by 4–5 weeks. A mean residual hearing loss of 26.3 dB at 2 kHz remained. The third group consisted of animals that did not recover after trauma. Three weeks after the exposure, tuning curves of single auditory nerve fibers were very broad and sometimes irregular in shape. Their thresholds hovered around 120 dB SPL. Spontaneous firing rate and driven rate were much reduced. Four or more months after exposure, the thresholds and sharpness of tuning of many single units were almost completely recovered. Spontaneous firing rate and driven rate were comparable to those of control animals. In the slow recovery group neuronal tuning properties showed less recovery, especially at frequencies above the exposure frequency. Thresholds and sharpness of tuning were normal at frequencies below the exposure frequency, but were much poorer at frequencies above the exposure. Spontaneous firing rate was much reduced in fibers with high characteristic frequencies. In fast recovering animals, the papilla was repopulated with hair cells after 4 months. In slow recovering animals, short (abneural) hair cells were still missing over large parts of the papilla after 4 months of recovery. Residual short (abneural) hair cell loss was largest at two areas, one more basal and the other more apical to the characteristic place of the traumatizing frequency. The results show that, in adult birds, functional recovery from severe damage to both short (abneural) and tall (neural) hair cells occurs. However, the onset of recovery is delayed and the time course is slower than after destruction of short (abneural) hair cells alone. Also, recovery is incomplete, both functionally and morphologically. There is residual permanent hearing loss, and regeneration of short (abneural) hair cells is incomplete.