Tinnitus and hyperacusis are life-disrupting perceptual abnormalities that are often preceded by acoustic overexposure. Animal models of overexposure have suggested a link between these phenomena and neural hyperactivity, i.e. elevated spontaneous rates (SRs) and soundevoked responses. Prior work has focused on changes in central auditory responses, with less attention paid to the exact nature of the associated peripheral damage. The demonstration that acoustic overexposure can cause cochlear nerve damage without permanent threshold elevation suggests this type of peripheral damage may be a key elicitor of tinnitus and hyperacusis in humans with normal audiograms. We addressed this idea by recording responses in the mouse inferior colliculus (IC) following a bilateral, neuropathic noise exposure. Two wks post-exposure, mean SRs were unchanged in mice recorded while awake, or under anesthesia. SRs were also unaffected by more intense, or unilateral exposures. These results suggest that neither neuropathy nor hair cell loss are sufficient to raise SRs in the IC, at least in mice. However, it's not clear whether our mice had tinnitus. Tone-evoked rate-level functions at the CF were steeper following exposure, specifically in the region of maximal neuropathy. Furthermore, suppression driven by off-CF tones and by ipsilateral noise were also reduced. Both changes were especially pronounced in neurons of awake mice. These findings align with prior reports of elevated acoustic startle in neuropathic mice, and indicate that neuropathy may initiate a compensatory response in the central auditory system leading to the genesis of hyperacusis.