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.

Reviewing Editor

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

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.

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.

Metrics

  • 3,760
    views
  • 568
    downloads
  • 41
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  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

Share this article

https://doi.org/10.7554/eLife.35587

Further reading

    1. Neuroscience
    Amanda Chu, Nicholas T Gordon ... Michael A McDannald
    Research Article

    Pavlovian fear conditioning has been extensively used to study the behavioral and neural basis of defensive systems. In a typical procedure, a cue is paired with foot shock, and subsequent cue presentation elicits freezing, a behavior theoretically linked to predator detection. Studies have since shown a fear conditioned cue can elicit locomotion, a behavior that - in addition to jumping, and rearing - is theoretically linked to imminent or occurring predation. A criticism of studies observing fear conditioned cue-elicited locomotion is that responding is non-associative. We gave rats Pavlovian fear discrimination over a baseline of reward seeking. TTL-triggered cameras captured 5 behavior frames/s around cue presentation. Experiment 1 examined the emergence of danger-specific behaviors over fear acquisition. Experiment 2 examined the expression of danger-specific behaviors in fear extinction. In total, we scored 112,000 frames for nine discrete behavior categories. Temporal ethograms show that during acquisition, a fear conditioned cue suppresses reward seeking and elicits freezing, but also elicits locomotion, jumping, and rearing - all of which are maximal when foot shock is imminent. During extinction, a fear conditioned cue most prominently suppresses reward seeking, and elicits locomotion that is timed to shock delivery. The independent expression of these behaviors in both experiments reveal a fear conditioned cue to orchestrate a temporally organized suite of behaviors.

    1. Neuroscience
    Salima Messaoudi, Ada Allam ... Isabelle Caille
    Research Article

    The fragile X syndrome (FXS) represents the most prevalent form of inherited intellectual disability and is the first monogenic cause of autism spectrum disorder. FXS results from the absence of the RNA-binding protein FMRP (fragile X messenger ribonucleoprotein). Neuronal migration is an essential step of brain development allowing displacement of neurons from their germinal niches to their final integration site. The precise role of FMRP in neuronal migration remains largely unexplored. Using live imaging of postnatal rostral migratory stream (RMS) neurons in Fmr1-null mice, we observed that the absence of FMRP leads to delayed neuronal migration and altered trajectory, associated with defects of centrosomal movement. RNA-interference-induced knockdown of Fmr1 shows that these migratory defects are cell-autonomous. Notably, the primary Fmrp mRNA target implicated in these migratory defects is microtubule-associated protein 1B (MAP1B). Knocking down MAP1B expression effectively rescued most of the observed migratory defects. Finally, we elucidate the molecular mechanisms at play by demonstrating that the absence of FMRP induces defects in the cage of microtubules surrounding the nucleus of migrating neurons, which is rescued by MAP1B knockdown. Our findings reveal a novel neurodevelopmental role for FMRP in collaboration with MAP1B, jointly orchestrating neuronal migration by influencing the microtubular cytoskeleton.