Corticothalamic gating of population auditory thalamocortical transmission in mouse

  1. Baher A Ibrahim
  2. Caitlin A Murphy
  3. Georgiy Yudintsev
  4. Yoshitaka Shinagawa
  5. Matthew I Banks
  6. Daniel A Llano  Is a corresponding author
  1. University of Illinois at Urbana Champaign, United States
  2. University of Wisconsin-Madison, United States
  3. University of Illinois at Urbana-Champaign, United States

Abstract

The mechanisms that govern thalamocortical transmission are poorly understood. Recent data have shown that sensory stimuli elicit activity in ensembles of cortical neurons that recapitulate stereotyped spontaneous activity patterns. Here, we elucidate a possible mechanism by which gating of patterned population cortical activity occurs. In this study, sensory-evoked all-or-none cortical population responses were observed in the mouse auditory cortex in vivo and similar stochastic cortical responses were observed in a colliculo-thalamocortical brain slice preparation. Cortical responses were associated with decreases in auditory thalamic synaptic inhibition and increases in thalamic synchrony. Silencing of corticothalamic neurons in layer 6 (but not layer 5) or the thalamic reticular nucleus linearized the cortical responses, suggesting that layer 6 corticothalamic feedback via the thalamic reticular nucleus was responsible for gating stochastic cortical population responses. These data implicate a corticothalamic-thalamic reticular nucleus circuit that modifies thalamic neuronal synchronization to recruit populations of cortical neurons for sensory representations.

Data availability

All data generated or analyzed during this study are included in the manuscript and supporting files. Source data files have been provided for Figures 1, Figure 2, Figure 2-figure supplement 2, Figure 2-figure supplement 6, Figure 3, Figure 4, Figure 5, Figure 6, Figure 6-figure supplement 1.The datasets are available at Dryad under a DOI (doi:10.5061/dryad.qrfj6q5c4).

The following data sets were generated

Article and author information

Author details

  1. Baher A Ibrahim

    1Department of Molecular and Integrative Physiology, University of Illinois at Urbana Champaign, Urbana, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0062-7589
  2. Caitlin A Murphy

    Department of Anesthesiology, University of Wisconsin-Madison, Madison, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6319-9470
  3. Georgiy Yudintsev

    Neuroscience Program, University of Illinois at Urbana Champaign, Urbana, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Yoshitaka Shinagawa

    University of Illinois at Urbana-Champaign, Urbana, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Matthew I Banks

    Department of Anesthesiology, University of Wisconsin-Madison, Madison, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Daniel A Llano

    University of Illinois at Urbana-Champaign, Urbana, United States
    For correspondence
    d-llano@illinois.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0933-1837

Funding

NIDCD (R01DC013073)

  • Daniel A Llano

NIDCD (R21DC014765)

  • Daniel A Llano

NSF (1515587)

  • Daniel A Llano

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

Ethics

Animal experimentation: This study was performed in strict accordance with the recommendations in the Guide for the Care and Use of Laboratory Animals of the National Institutes of Health. All of the animals were handled according to approved institutional animal care and use committee (IACUC) protocols (#18236) of the University of Illinois at Urbana-Champaign. All surgery was performed under ketamine/xylazine anesthesia, and every effort was made to minimize suffering.

Reviewing Editor

  1. Andrew J King, University of Oxford, United Kingdom

Version history

  1. Received: March 5, 2020
  2. Accepted: May 23, 2021
  3. Accepted Manuscript published: May 24, 2021 (version 1)
  4. Version of Record published: June 8, 2021 (version 2)

Copyright

© 2021, Ibrahim 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. Baher A Ibrahim
  2. Caitlin A Murphy
  3. Georgiy Yudintsev
  4. Yoshitaka Shinagawa
  5. Matthew I Banks
  6. Daniel A Llano
(2021)
Corticothalamic gating of population auditory thalamocortical transmission in mouse
eLife 10:e56645.
https://doi.org/10.7554/eLife.56645

Share this article

https://doi.org/10.7554/eLife.56645

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