The present study was conducted to examine the re-establishment of IHC/VIII nerve synapses following kainic acid (KA) excitotoxicity and to discern if the re-organized afferent could render not only a normal auditory threshold but also a normal supra-threshold function. KA (60 mM) applied to the intact round window membrane in chinchilla destroyed postsynaptic endings of the auditory nerve, depressed the input-output (I/O) functions of auditory evoked potentials (EVP) and produced an average loss of sensitivity of over 80 dB at 4, 8, and 16 kHz, with less substantial losses (40-60 dB) at lower frequencies. However, there was no significant difference in 2f1-f2 distortion-product otoacoustic emissions (DPOAE) before and after the application of KA. The nerve endings went through a sequence of swelling, degeneration and recovery over a 3-5 day period at higher frequency. Auditory sensitivity and supra-threshold response returned accordingly. In contrast, complete recovery at lower frequencies (1 and 2 kHz) required more than 5 days. The results provide strong evidence that (1) excitotoxically damaged cochlear afferent neurons can recover and render both a normal EVP threshold and EVP I/O function and (2) afferent innervation to IHCs is not necessary for DPOAE generation.