Silent Damage of Noise on Cochlear Afferent Innervation in Guinea Pigs and the Impact on Temporal Processing

Abstract

Noise-exposure at levels low enough to avoid a permanent threshold shift has been found to cause a massive, delayed degeneration of spiral ganglion neurons (SGNs) in mouse cochleae. Damage to the afferent innervation was initiated by a loss of synaptic ribbons, which is largely irreversible in mice. A similar delayed loss of SGNs has been found in guinea pig cochleae, but at a reduced level, suggesting a cross-species difference in SGN sensitivity to noise. Ribbon synapse damage occurs “silently” in that it does not affect hearing thresholds as conventionally measured, and the functional consequence of this damage is not clear. In the present study, we further explored the effect of noise on cochlear afferent innervation in guinea pigs by focusing on the dynamic changes in ribbon counts over time, and resultant changes in temporal processing. It was found that (1) contrary to reports in mice, the initial loss of ribbons largely recovered within a month after the noise exposure, although a significant amount of residual damage existed; (2) while the response threshold fully recovered in a month, the temporal processing continued to be deteriorated during this period.

Noise-induced damage to ribbon synapses without permanent threshold shifts in neonatal mice

“…Thus, the present study examined the effects of noise-induced silent damage on ribbon synapses in neonatal mice during the early onset of hearing. The present results demonstrated that noise exposure shortly after birth resulted in similar but less marked damage to the ribbon synapses than has been observed in previous studies conducted in adult mice (Kujawa and Liberman, 2009;Lin et al, 2011;Liu et al, 2012;Shi et al, 2013). However, in contrast to adult animals, the loss of ribbon synapses progressed continuously in the young mice for more than 1 month following exposure to noise.…”

“…The floor of the cage was 60 cm below the horns of one low-frequency woofer and one high-frequency tweeter, and electrical Gaussian noise was delivered through the two loudspeakers after power amplification. The acoustic spectrum of the sound was distributed mainly below 20 kHz, as described previously (Liu et al, 2012), and the frequency range for sound density 10 dB below the peak was between 3 and 14 kHz. The noise level was monitored using a 0.25-inch microphone linked to a sound level meter (microphone: 2520, sound level meter: 824, Larson Davis; Depew, NY, USA).…”

“…While the damaging effects of noise on ribbon synapses between spiral ganglion neurons (SGNs) and cochlear hair cells (HCs), particularly inner hair cells (IHCs), have also been assessed by previous studies, (Puel et al, 1997;Pujol and Puel, 1999), this type of damage was largely considered to be repairable and, therefore, not important. More recently, however, quantitative studies have demonstrated the development of permanent noise-induced damage in ribbon synapses, which suggests that the repair of these synapses following such damage is incomplete (Kujawa and Liberman, 2009;Lin et al, 2011;Liu et al, 2012;Shi et al, 2013).…”

“…For example, in adult rodents (both mice and guinea pigs), brief exposure to relatively low-level noise that does not cause a permanent threshold shift (PTS) in hearing can produce massive damage to the ribbon synapses (Kujawa and Liberman, 2009;Lin et al, 2011;Liu et al, 2012;Shi et al, 2013). Without a PTS, this type of damage would likely go unnoticed by human subjects and would almost certainly be missed during routine audiology evaluations that focus primarily on hearing threshold levels.…”

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Recently, ribbon synapses to the hair cells (HCs) in the cochlea have become a novel site of interest in the investigation of noise-induced cochlear lesions in adult rodents (Kujawa and Liberman, 2009;Lin et al, 2011;Liu et al, 2012;Shi et al, 2013). Permanent noise-induced damage to this type of synapse can result in subsequent degeneration of spiral ganglion neurons (SGNs) in the absence of permanent changes to hearing sensitivity.

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