Corticothalamic gating of population auditory thalamocortical transmission in mouse

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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

(2020) Corticothalamic gating of population auditory thalamocortical transmission in mouse
Dryad Digital Repository, doi:10.5061/dryad.qrfj6q5c4.

http://dx.doi.org/10.5061/dryad.qrfj6q5c4

Article and author information

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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.

"This ORCID iD identifies the author of this article:" 0000-0002-0062-7589
Caitlin A Murphy

Department of Anesthesiology, University of Wisconsin-Madison, Madison, United States

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-6319-9470
Georgiy Yudintsev

Neuroscience Program, University of Illinois at Urbana Champaign, Urbana, United States

Competing interests
The authors declare that no competing interests exist.
Yoshitaka Shinagawa

University of Illinois at Urbana-Champaign, Urbana, United States

Competing interests
The authors declare that no competing interests exist.
Matthew I Banks

Department of Anesthesiology, University of Wisconsin-Madison, Madison, United States

Competing interests
The authors declare that no competing interests exist.
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.

"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.

Copyright

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.