Neuron
Volume 109, Issue 6, 17 March 2021, Pages 984-996.e4
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Article
Cochlear neural degeneration disrupts hearing in background noise by increasing auditory cortex internal noise

https://doi.org/10.1016/j.neuron.2021.01.015Get rights and content
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Highlights

  • Cochlear neural degeneration (CND) in mice causes sound detection deficits in noise

  • CND induces distinct plasticity in cortical excitatory and inhibitory neurons

  • Cortical hyperexcitability after CND disrupts neural adaptation to background noise

  • Random surges of hypersynchronized activity precede behavioral miss trials in noise

Summary

Correlational evidence in humans suggests that selective difficulties hearing in noisy, social settings may reflect premature auditory nerve degeneration. Here, we induced primary cochlear neural degeneration (CND) in adult mice and found direct behavioral evidence for selective detection deficits in background noise. To identify central determinants for this perceptual disorder, we tracked daily changes in ensembles of layer 2/3 auditory cortex parvalbumin-expressing inhibitory neurons and excitatory pyramidal neurons with chronic two-photon calcium imaging. CND induced distinct forms of plasticity in cortical excitatory and inhibitory neurons that culminated in net hyperactivity, increased neural gain, and reduced adaptation to background noise. Ensemble activity measured while mice detected targets in noise could accurately decode whether individual behavioral trials were hits or misses. After CND, random surges of hypercorrelated cortical activity occurring just before target onset reliably predicted impending detection failures, revealing a source of internal cortical noise underlying perceptual difficulties in external noise.

Keywords

parvalbumin
two-photon calcium imaging
hidden hearing loss
nerve damage
synaptopathy
neuropathy
spiral ganglion
hearing in noise
homeostatic plasticity
auditory cortex

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Present address: Department of Life Sciences, Ben-Gurion University of the Negev, Beersheba, Israel

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