Central Gain Restores Auditory Processing following Near-Complete Cochlear Denervation

Anna R. Chambers, Jennifer Resnik, Yasheng Yuan, Jonathon P. Whitton, Albert S. Edge, M. Charles Liberman, Daniel B. Polley

Research output: Contribution to journalArticlepeer-review

144 Scopus citations

Abstract

Sensory 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: Removing 95% of cochlear afferent synapses eliminates sound-evoked brainstem responses and acoustic reflexes, yet sound detection remains normal. Chambers and colleagues describe a cortical amplifier that recovers sound feature representations supported by neural rate-coding, but not precise spike timing.

Original languageEnglish
Pages (from-to)867-879
Number of pages13
JournalNeuron
Volume89
Issue number4
DOIs
StatePublished - 17 Feb 2016
Externally publishedYes

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