Cochlear aging disrupts the correlation between spontaneous rate and sound level coding in auditory nerve fibers

The spiking activity of auditory nerve fibers (ANFs) transmits information about the acoustic environment from the cochlea to the central auditory system. Increasing age leads to degeneration of cochlear tissues, including the sensory hair cells and stria vascularis. Here, we aim to identify the functional effects of such age-related cochlear pathologies of ANFs. Rate-level functions (RLFs) were recorded from single-unit ANFs of young-adult (n = 52, 3 - 12 months) and quiet-aged (n = 24, > 36 months) Mongolian gerbils of either sex. RLFs were used to determine sensitivity and spontaneous rates (SRs), and were classified into flat-saturating, sloping-saturating, and straight categories, as previously established. A physiologically based cochlear model, adapted for the gerbil, was used to simulate the effects of cochlear degeneration on ANF physiology.In ANFs tuned to low frequencies (< 3.5 kHz), SR was lower in those of aged gerbils, while an age-related loss of low-SR fibers was evident in ANFs tuned to high frequencies. These changes in SR distribution did not affect the typical SR vs. sensitivity correlation. The distribution of RLF types among low-SR fibers, however, shifted towards that of high-SR fibers, specifically showing more fast-saturating and fewer sloping-saturating RLFs. A modeled strial degeneration, which affects the combined inner-hair-cell and synaptic output, reduced SR but left RLF type unchanged. An additional reduced basilar membrane gain, which decreased sensitivity, explained the changed RLF types.Overall, the data indicated age-related changes in the characteristics of single ANFs that blurred the established relationships between SR and RLF type.