Auditory cortex shapes sound responses in the inferior colliculus

Abstract

The extensive feedback from the auditory cortex (AC) to the inferior colliculus (IC) supports critical aspects of auditory behavior but has not been extensively characterized. Previous studies demonstrated that activity in IC is altered by focal electrical stimulation and pharmacological inactivation of AC, but these methods lack the ability to selectively manipulate projection neurons. We measured the effects of selective optogenetic modulation of cortico-collicular feedback projections on IC sound responses in mice. Activation of feedback increased spontaneous activity and decreased stimulus selectivity in IC, whereas suppression had no effect. To further understand how microcircuits in AC may control collicular activity, we optogenetically modulated different cortical neuronal subtypes, specifically parvalbumin-positive (PV) and somatostatin-positive (SST) inhibitory interneurons. We found that modulating either type of interneuron did not affect IC sound-evoked activity. Combined, our results identify that activation of excitatory projections, but not inhibition-driven changes in cortical activity, affects collicular sound responses.

Data availability

Original spike data and code are available on Dryad (doi:10.5061/dryad.1t61c80).

The following data sets were generated

Article and author information

Author details

  1. Jennifer M Blackwell

    Department of Otorhinolaryngology, University of Pennsylvania, Philadelphia, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Alexandria MH Lesicko

    Department of Otorhinolaryngology, University of Pennsylvania, Philadelphia, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Winnie Rao

    Department of Otorhinolaryngology, University of Pennsylvania, Philadelphia, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Mariella De Biasi

    Department of Psychiatry, University of Pennsylvania, Philadelphia, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Maria N Geffen

    Department of Otorhinolaryngology, University of Pennsylvania, Philadelphia, United States
    For correspondence
    mgeffen@pennmedicine.upenn.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3022-2993

Funding

National Institute on Deafness and Other Communication Disorders (R03DC013660)

  • Maria N Geffen

National Institute on Deafness and Other Communication Disorders (NIH R01DC014779)

  • Maria N Geffen

National Institute on Deafness and Other Communication Disorders (NIH R01DC015527)

  • Maria N Geffen

Klingenstein Award in Neurosciences

  • Maria N Geffen

Human Frontier in Science

  • Maria N Geffen

Pennsylvania Lions Club Hearing Research Fellowship

  • Maria N Geffen

National Institute on Deafness and Other Communication Disorders (1F32MH120890)

  • Alexandria MH Lesicko

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 animal work was conducted according to the guidelines of University of Pennsylvanian IACUC (protocol number 803266) and the AALAC Guide on Animal Research. Anesthesia by isoflurane and ketamine and euthanasia by CO2 were used. All means were taken to minimize the pain or discomfort of the animals during and following the experiments. All experiments were performed during the animals' dark cycle.

Reviewing Editor

  1. Catherine Emily Carr, University of Maryland, United States

Version history

  1. Received: September 15, 2019
  2. Accepted: January 31, 2020
  3. Accepted Manuscript published: January 31, 2020 (version 1)
  4. Version of Record published: March 9, 2020 (version 2)

Copyright

© 2020, Blackwell et al.

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 M Blackwell
  2. Alexandria MH Lesicko
  3. Winnie Rao
  4. Mariella De Biasi
  5. Maria N Geffen
(2020)
Auditory cortex shapes sound responses in the inferior colliculus
eLife 9:e51890.
https://doi.org/10.7554/eLife.51890

Share this article

https://doi.org/10.7554/eLife.51890

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