Coordinated neuronal ensembles in primary auditory cortical columns

  1. Jermyn Z See
  2. Craig A Atencio
  3. Vikaas S Sohal
  4. Christoph E Schreiner  Is a corresponding author
  1. University of California, San Francisco, United States

Abstract

Synchronous activity of groups of neurons is increasingly thought to be important in cortical information processing and transmission. However, most studies of processing in the primary auditory cortex (AI) have viewed neurons as independent filters; little is known about how coordinated AI neuronal activity is expressed throughout cortical columns and how it might enhance the processing of auditory information. To address this, we recorded from populations of neurons in AI cortical columns of anesthetized rats and, using dimensionality reduction techniques, identified multiple coordinated neuronal ensembles (cNEs), i.e. groups of neurons with reliable synchronous activity. We show that cNEs reflect local network configurations with enhanced information encoding properties that cannot be accounted for by stimulus-driven synchronization alone. Furthermore, similar cNEs were identified in both spontaneous and evoked activity, indicating that columnar cNEs are stable functional constructs that may represent principal units of information processing in AI.

Data availability

Single-unit extracellular electrophysiological data have been deposited in CRCNS.org under DOI citation http://dx.doi.org/10.6080/K09021X1

The following data sets were generated
    1. See JZ
    2. Atencio CA
    3. Schreiner
    4. CE
    (2018) High-density extracellular recordings from the primary auditory cortex in anesthetized rats listening to dynamic broadband stimuli.
    Publicly available at the Collaborative Research in Computational Neuroscience data sharing website (http://crcns.org/).

Article and author information

Author details

  1. Jermyn Z See

    UCSF Center for Integrative Neuroscience, University of California, San Francisco, San Francisco, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8372-0753
  2. Craig A Atencio

    UCSF Center for Integrative Neuroscience, University of California, San Francisco, San Francisco, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Vikaas S Sohal

    UCSF Center for Integrative Neuroscience, University of California, San Francisco, San Francisco, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2238-4186
  4. Christoph E Schreiner

    UCSF Center for Integrative Neuroscience, University of California, San Francisco, San Francisco, United States
    For correspondence
    chris@phy.ucsf.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4571-4328

Funding

National Institute on Deafness and Other Communication Disorders (DC02260)

  • Craig A Atencio
  • Christoph E Schreiner

Coleman Memorial Fund

  • Craig A Atencio
  • Christoph E Schreiner

Hearing Research Incorporate, San Francisco

  • Craig A Atencio
  • Christoph E Schreiner

Agency for Science, Technology and Research, Singapore (National Science Scholarship)

  • Jermyn Z See

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 (#100-17) of the University of California, San Francisco. The protocol was approved by the IACUC of the University of California, San Francisco (Protocol Number: AN165706-02). All surgery was performed under ketamine/xylazine anesthesia, and every effort was made to minimize suffering.

Reviewing Editor

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

Version history

  1. Received: February 1, 2018
  2. Accepted: June 3, 2018
  3. Accepted Manuscript published: June 5, 2018 (version 1)
  4. Version of Record published: June 25, 2018 (version 2)

Copyright

© 2018, See 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. Jermyn Z See
  2. Craig A Atencio
  3. Vikaas S Sohal
  4. Christoph E Schreiner
(2018)
Coordinated neuronal ensembles in primary auditory cortical columns
eLife 7:e35587.
https://doi.org/10.7554/eLife.35587

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