Plasticity in the adult mammalian brain can occur after damage to peripheral nerves and has also been described in the auditory system. Acoustic trauma, resulting in a loss of cochlear sensitivity, can lead to elevated levels of spontaneous activity, that is hyperactivity, in central nuclei such as the inferior colliculus. The current view is that this hyperactivity is centrally generated as a result of altered input. We investigated acute and chronic effects of acoustic trauma on cochlear sensitivity and development of hyperactivity in the inferior colliculus of guinea pigs. In addition, we investigated whether hyperactivity in the inferior colliculus, once established, is dependent on neural activity in the cochlea. Acoustic trauma (1 h continuous, 10 kHz tone at 124 dB SPL) resulted in a small but permanent, frequency restricted threshold loss in the cochlea up to 6 weeks post-exposure (maximum recovery time used). This was accompanied by hyperactivity in restricted frequency areas of the inferior colliculus, broadly corresponding to the cochlear threshold loss. We found that hyperactivity in the inferior colliculus depended on neural activity in the cochlea at all recovery times, since it disappeared after cochlear ablation and treatments blocking spontaneous firing of primary afferents. We suggest that the dependency of the central hyperactivity on the integrity of the peripheral receptor indicates hyperexcitability within the CNS resulting in greater neuronal firing in response to normal levels of peripheral spontaneous activity.