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Research Articles, Systems/Circuits

Noise Trauma-Induced Behavioral Gap Detection Deficits Correlate with Reorganization of Excitatory and Inhibitory Local Circuits in the Inferior Colliculus and Are Prevented by Acoustic Enrichment

Joshua J. Sturm, Ying-Xin Zhang-Hooks, Hannah Roos, Tuan Nguyen and Karl Kandler
Journal of Neuroscience 28 June 2017, 37 (26) 6314-6330; DOI: https://doi.org/10.1523/JNEUROSCI.0602-17.2017
Joshua J. Sturm
1Department of Otolaryngology and
2Department of Neurobiology, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania 15213,
3Medical Scientist Training Program, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania 15261,
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Ying-Xin Zhang-Hooks
1Department of Otolaryngology and
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Hannah Roos
1Department of Otolaryngology and
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Tuan Nguyen
4Department of Physics, The College of New Jersey, Ewing, New Jersey 08628, and
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Karl Kandler
1Department of Otolaryngology and
2Department of Neurobiology, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania 15213,
5Department of Bioengineering, Swanson School of Engineering, and
6Center for the Neural Basis of Cognition, University of Pittsburgh, Pittsburgh, Pennsylvania 15213
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Abstract

Hearing loss leads to a host of cellular and synaptic changes in auditory brain areas that are thought to give rise to auditory perception deficits such as temporal processing impairments, hyperacusis, and tinnitus. However, little is known about possible changes in synaptic circuit connectivity that may underlie these hearing deficits. Here, we show that mild hearing loss as a result of brief noise exposure leads to a pronounced reorganization of local excitatory and inhibitory circuits in the mouse inferior colliculus. The exact nature of these reorganizations correlated with the presence or absence of the animals' impairments in detecting brief sound gaps, a commonly used behavioral sign for tinnitus in animal models. Mice with gap detection deficits (GDDs) showed a shift in the balance of synaptic excitation and inhibition that was present in both glutamatergic and GABAergic neurons, whereas mice without GDDs showed stable excitation–inhibition balances. Acoustic enrichment (AE) with moderate intensity, pulsed white noise immediately after noise trauma prevented both circuit reorganization and GDDs, raising the possibility of using AE immediately after cochlear damage to prevent or alleviate the emergence of central auditory processing deficits.

SIGNIFICANCE STATEMENT Noise overexposure is a major cause of central auditory processing disorders, including tinnitus, yet the changes in synaptic connectivity underlying these disorders remain poorly understood. Here, we find that brief noise overexposure leads to distinct reorganizations of excitatory and inhibitory synaptic inputs onto glutamatergic and GABAergic neurons and that the nature of these reorganizations correlates with animals' impairments in detecting brief sound gaps, which is often considered a sign of tinnitus. Acoustic enrichment immediately after noise trauma prevents circuit reorganizations and gap detection deficits, highlighting the potential for using sound therapy soon after cochlear damage to prevent the development of central processing deficits.

  • midbrain
  • noise trauma
  • tinnitus
  • uncaging
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The Journal of Neuroscience: 37 (26)
Journal of Neuroscience
Vol. 37, Issue 26
28 Jun 2017
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Noise Trauma-Induced Behavioral Gap Detection Deficits Correlate with Reorganization of Excitatory and Inhibitory Local Circuits in the Inferior Colliculus and Are Prevented by Acoustic Enrichment
Joshua J. Sturm, Ying-Xin Zhang-Hooks, Hannah Roos, Tuan Nguyen, Karl Kandler
Journal of Neuroscience 28 June 2017, 37 (26) 6314-6330; DOI: 10.1523/JNEUROSCI.0602-17.2017

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Noise Trauma-Induced Behavioral Gap Detection Deficits Correlate with Reorganization of Excitatory and Inhibitory Local Circuits in the Inferior Colliculus and Are Prevented by Acoustic Enrichment
Joshua J. Sturm, Ying-Xin Zhang-Hooks, Hannah Roos, Tuan Nguyen, Karl Kandler
Journal of Neuroscience 28 June 2017, 37 (26) 6314-6330; DOI: 10.1523/JNEUROSCI.0602-17.2017
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Keywords

  • midbrain
  • noise trauma
  • tinnitus
  • uncaging

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