Fast-spiking GABA circuit dynamics in the auditory cortex predict recovery of sensory processing following peripheral nerve damage

  1. Jennifer Resnik  Is a corresponding author
  2. Daniel B Polley  Is a corresponding author
  1. Massachusetts Eye and Ear Infirmary, United States

Abstract

Cortical neurons remap their receptive fields and rescale sensitivity to spared peripheral inputs following sensory nerve damage. To address how these plasticity processes are coordinated over the course of functional recovery, we tracked receptive field reorganization, spontaneous activity, and response gain from individual principal neurons in the adult mouse auditory cortex over a 50-day period surrounding either moderate or massive auditory nerve damage. We related the day-by-day recovery of sound processing to dynamic changes in the strength of intracortical inhibition from parvalbumin-expressing (PV) inhibitory neurons. Whereas the status of brainstem-evoked potentials did not predict the recovery of sensory responses to surviving nerve fibers, homeostatic adjustments in PV-mediated inhibition during the first days following injury could predict the eventual recovery of cortical sound processing weeks later. These findings underscore the potential importance of self-regulated inhibitory dynamics for the restoration of sensory processing in excitatory neurons following peripheral nerve injuries.

Article and author information

Author details

  1. Jennifer Resnik

    Eaton-Peabody Laboratories, Massachusetts Eye and Ear Infirmary, Boston, United States
    For correspondence
    Jennifer_Resnik@MEEI.HARVARD.EDU
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0573-0008
  2. Daniel B Polley

    Eaton-Peabody Laboratories, Massachusetts Eye and Ear Infirmary, Boston, United States
    For correspondence
    Daniel_Polley@meei.harvard.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5120-2409

Funding

European Molecular Biology Organization (Long term postdoctoral fellowship)

  • Jennifer Resnik

National Institute on Deafness and Other Communication Disorders (RO1 DC009836)

  • Daniel B Polley

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Animal experimentation: All procedures were approved by the Animal Care and Use Committee at the Massachusetts Eye and Ear Infirmary (protocol number 10-03-006) and followed guidelines established by the National Institutes of Health for the care and use of laboratory animals. All surgeries were performed under ketamine and xylazine, and every effort was made to minimize suffering.

Copyright

© 2017, Resnik & Polley

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Jennifer Resnik
  2. Daniel B Polley
(2017)
Fast-spiking GABA circuit dynamics in the auditory cortex predict recovery of sensory processing following peripheral nerve damage
eLife 6:e21452.
https://doi.org/10.7554/eLife.21452

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https://doi.org/10.7554/eLife.21452

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