Behavioral tinnitus in gerbils is associated with reduced spontaneous rates in single auditory-nerve fibers

Tinnitus is often initiated by damage to the peripheral auditory system, for example by overexposure to loud sounds. Animal studies have shown that such noise-induced tinnitus is related to increased spontaneous activity in the brainstem dorsal cochlear nucleus as well as further along the central auditory pathway. However, the role of spontaneous activity of the auditory nerve, connecting the peripheral and central auditory systems, in tinnitus and brainstem hyperactivity remains unknown. In the current study, tinnitus was induced by exposing anesthetized Mongolian gerbils to a 115-dB SPL narrowband noise. After one day of recovery, animals were behaviorally tested for gap detection deficits using a gap-prepulse inhibition of the acoustic startle reflex (GPIAS) paradigm, indicative of tinnitus. Ipsilateral noise-induced threshold shifts did not differ between animals with and without signs of tinnitus. Interestingly, single auditory nerve fibers that were recorded from animals with signs of tinnitus had significantly reduced spontaneous rates compared to both noise-exposed animals without signs of tinnitus and sham-exposed animals. Furthermore, spontaneous rate reduction was specific to fibers with a best frequency within the frequency bands that showed gap detection deficits. On the other hand, inter-spike interval variability and bursting behavior increased in fibers from noise-exposed compared to sham-exposed animals but did not differ with gap detection deficits. These findings suggest that tinnitus-related central hyperactivity may be provoked by reduced spontaneous rates of its innervating auditory nerve fibers. This is consistent with current models explaining the central manifestation of tinnitus, such as the stochastic resonance and central gain models, and allows for a more detailed definition of specifically tinnitus-related deafferentation.