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Parallel pathways for sound processing and functional connectivity among layer 5 and 6 auditory corticofugal neurons

  1. Ross S Williamson  Is a corresponding author
  2. Daniel B Polley
  1. Massachusetts Eye and Ear Infirmary, United States
Research Article
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Cite this article as: eLife 2019;8:e42974 doi: 10.7554/eLife.42974

Abstract

Cortical layers (L) 5 and 6 are populated by intermingled cell-types with distinct inputs and downstream targets. Here, we made optogenetically guided recordings from L5 corticofugal (CF) and L6 corticothalamic (CT) neurons in the auditory cortex of awake mice to discern differences in sensory processing and underlying patterns of functional connectivity. Whereas L5 CF neurons showed broad stimulus selectivity with sluggish response latencies and extended temporal non-linearities, L6 CTs exhibited sparse selectivity and rapid temporal processing. L5 CF spikes lagged behind neighboring units and imposed weak feedforward excitation within the local column. By contrast, L6 CT spikes drove robust and sustained activity, particularly in local fast-spiking interneurons. Our findings underscore a duality among sub-cortical projection neurons, where L5 CF units are canonical broadcast neurons that integrate sensory inputs for transmission to distributed downstream targets, while L6 CT neurons are positioned to regulate thalamocortical response gain and selectivity.

Data availability

All data generated or analyzed during this study are included in the manuscript and supporting files. Source data has been provided for Figures 2-7.

Article and author information

Author details

  1. Ross S Williamson

    Eaton-Peabody Laboratories, Massachusetts Eye and Ear Infirmary, Boston, United States
    For correspondence
    rsw@pitt.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5633-7337
  2. Daniel B Polley

    Eaton-Peabody Laboratories, Massachusetts Eye and Ear Infirmary, Boston, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5120-2409

Funding

National Institutes of Health (R01 DC017078)

  • Daniel B Polley

National Institutes of Health (F32 DC015376)

  • Ross S Williamson

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

Ethics

Animal experimentation: Animal experimentation: All procedures were approved by the Animal Care and Use Committee at the Massachusetts Eye and Ear Infirmary (protocol number 10-03-006) and followed guidelines established by the National Institutes of Health for the care and use of laboratory animals. All surgeries were performed under isoflurane, or ketamine and xylazine, and every effort was made to minimize suffering.

Reviewing Editor

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

Publication history

  1. Received: October 18, 2018
  2. Accepted: February 6, 2019
  3. Accepted Manuscript published: February 8, 2019 (version 1)
  4. Version of Record published: February 21, 2019 (version 2)
  5. Version of Record updated: February 25, 2019 (version 3)

Copyright

© 2019, Williamson & Polley

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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