Central Gain Restores Auditory Processing following Near-Complete Cochlear Denervation

• Normal sound detection persists in the absence of peripheral markers of hearing
• Faster and more complete recovery from cochlear denervation in cortex than midbrain
• Enhanced cortical gain supports features encoded by spike rate, not spike timing
• Recovery is more complete after unilateral denervation than bilateral denervation

SummarySensory organ damage induces a host of cellular and physiological changes in the periphery and the brain. Here, we show that some aspects of auditory processing recover after profound cochlear denervation due to a progressive, compensatory plasticity at higher stages of the central auditory pathway. Lesioning >95% of cochlear nerve afferent synapses, while sparing hair cells, in adult mice virtually eliminated the auditory brainstem response and acoustic startle reflex, yet tone detection behavior was nearly normal. As sound-evoked responses from the auditory nerve grew progressively weaker following denervation, sound-evoked activity in the cortex—and, to a lesser extent, the midbrain—rebounded or surpassed control levels. Increased central gain supported the recovery of rudimentary sound features encoded by firing rate, but not features encoded by precise spike timing such as modulated noise or speech. These findings underscore the importance of central plasticity in the perceptual sequelae of cochlear hearing impairment.Video Abstract To view the video inline, enable JavaScript on your browser. However, you can download and view the video by clicking on the icon belowHelp with MP4 filesOptionsDownload video (54337 K)