Contextual and cross-modality modulation of auditory cortical processing through pulvinar mediated suppression

Abstract

Lateral posterior nucleus (LP) of thalamus, the rodent homologue of primate pulvinar, projects extensively to sensory cortices. However, its functional role in sensory cortical processing remains largely unclear. Here, bidirectional activity modulations of LP or its projection to the primary auditory cortex (A1) in awake mice reveal that LP improves auditory processing in A1 supragranular-layer neurons by sharpening their receptive fields and frequency tuning, as well as increasing the signal-to-noise ratio (SNR). This is achieved through a subtractive-suppression mechanism, mediated largely by LP-to-A1 axons preferentially innervating specific inhibitory neurons in layer 1 and superficial layers. LP is strongly activated by specific sensory signals relayed from the superior colliculus (SC), contributing to the maintenance and enhancement of A1 processing in the presence of auditory background noise and threatening visual looming stimuli respectively. Thus, a multisensory bottom-up SC-pulvinar-A1 pathway plays a role in contextual and cross-modality modulation of auditory cortical processing.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files. Source data files have been provided for all figures.

Article and author information

Author details

  1. Xiao-lin Chou

    Zilkha Neurogenetic Institute, University of Southern California, Los Angeles, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Qi Fang

    Zilkha Neurogenetic Institute, University of Southern California, Los Angeles, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Linqing Yan

    Zilkha Neurogenetic Institute, University of Southern California, Los Angeles, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Wen Zhong

    Zilkha Neurogenetic Institute, University of Southern California, Los Angeles, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Bo Peng

    Zilkha Neurogenetic Institute, University of Southern California, Los Angeles, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Haifu Li

    Zilkha Neurogenetic Institute, University of Southern California, Los Angeles, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Jinxing Wei

    Zilkha Neurogenetic Institute, University of Southern California, Los Angeles, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. Huizhong W Tao

    Zilkha Neurogenetic Institute, University of Southern California, Los Angeles, United States
    For correspondence
    htao@usc.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3660-0513
  9. Li I Zhang

    Zilkha Neurogenetic Institute, University of Southern California, Los Angeles, United States
    For correspondence
    liizhang@usc.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0275-8651

Funding

National Institutes of Health (R01DC008983)

  • Li I Zhang

National Institutes of Health (RF1MH114112)

  • Li I Zhang

National Institutes of Health (EY019049)

  • Huizhong W Tao

National Institutes of Health (EY022478)

  • Huizhong W Tao

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

Reviewing Editor

  1. Brice Bathellier, CNRS, France

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) protocol (protocol number: 21109) of the University of Southern California.

Version history

  1. Received: December 4, 2019
  2. Accepted: March 5, 2020
  3. Accepted Manuscript published: March 6, 2020 (version 1)
  4. Version of Record published: March 18, 2020 (version 2)

Copyright

© 2020, Chou 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. Xiao-lin Chou
  2. Qi Fang
  3. Linqing Yan
  4. Wen Zhong
  5. Bo Peng
  6. Haifu Li
  7. Jinxing Wei
  8. Huizhong W Tao
  9. Li I Zhang
(2020)
Contextual and cross-modality modulation of auditory cortical processing through pulvinar mediated suppression
eLife 9:e54157.
https://doi.org/10.7554/eLife.54157

Share this article

https://doi.org/10.7554/eLife.54157

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