Spike-phase coupling patterns reveal laminar identity in primate cortex

  1. Zachary W Davis  Is a corresponding author
  2. Nicholas M Dotson
  3. Tom P Franken
  4. Lyle Muller
  5. John H Reynolds  Is a corresponding author
  1. Salk Institute for Biological Studies, United States
  2. Washington University in St. Louis, United States
  3. Western University, Canada

Abstract

The cortical column is one of the fundamental computational circuits in the brain. In order to understand the role neurons in different layers of this circuit play in cortical function it is necessary to identify the boundaries that separate the laminar compartments. While histological approaches can reveal ground truth they are not a practical means of identifying cortical layers in vivo. The gold standard for identifying laminar compartments in electrophysiological recordings is current-source density (CSD) analysis. However, laminar CSD analysis requires averaging across reliably evoked responses that target the input layer in cortex, which may be difficult to generate in less well studied cortical regions. Further the analysis can be susceptible to noise on individual channels resulting in errors in assigning laminar boundaries. Here, we have analyzed linear array recordings in multiple cortical areas in both the common marmoset and the rhesus macaque. We describe a pattern of laminar spike-field phase relationships that reliably identifies the transition between input and deep layers in cortical recordings from multiple cortical areas in two different non-human primate species. This measure corresponds well to estimates of the location of the input layer using CSDs, but does not require averaging or specific evoked activity. Laminar identity can be estimated rapidly with as little as a minute of ongoing data and is invariant to many experimental parameters. This method may serve to validate CSD measurements that might otherwise be unreliable or to estimate laminar boundaries when other methods are not practical.

Data availability

The source data and code necessary to generate the results in the main figure panels are available at the open source repository: https://github.com/zwdsalk/LaminarPhaseCoupling

Article and author information

Author details

  1. Zachary W Davis

    Salk Institute for Biological Studies, La Jolla, United States
    For correspondence
    zdavis@salk.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4440-9011
  2. Nicholas M Dotson

    Salk Institute for Biological Studies, La Jolla, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Tom P Franken

    Department of Neuroscience, Washington University in St. Louis, St Louis, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7160-5152
  4. Lyle Muller

    Department of Mathematics, Western University, London, Canada
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5165-9890
  5. John H Reynolds

    Salk Institute for Biological Studies, La Jolla, United States
    For correspondence
    reynolds@salk.edu
    Competing interests
    The authors declare that no competing interests exist.

Funding

National Eye Institute (R01-EY028723)

  • John H Reynolds

National Eye Institute (T32 EY020503-06)

  • Zachary W Davis

National Eye Institute (P30 EY019005)

  • John H Reynolds

National Eye Institute (K99 EY031795)

  • Tom P Franken

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

Reviewing Editor

  1. Alicia Izquierdo, University of California, Los Angeles, United States

Ethics

Animal experimentation: All surgical procedures were performed with the monkeys under general anesthesia in an aseptic environment in accordance with the recommendations in the Guide for the Care and Use of Laboratory Animals of the National Institutes of Health. All experimental methods were approved by the Institutional Animal Care and Use Committee (IACUC) of the Salk Institute for Biological Studies and conformed with NIH guidelines (protocol 14-00014).

Version history

  1. Preprint posted: October 27, 2022 (view preprint)
  2. Received: October 27, 2022
  3. Accepted: April 13, 2023
  4. Accepted Manuscript published: April 17, 2023 (version 1)
  5. Version of Record published: May 5, 2023 (version 2)

Copyright

© 2023, Davis 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. Zachary W Davis
  2. Nicholas M Dotson
  3. Tom P Franken
  4. Lyle Muller
  5. John H Reynolds
(2023)
Spike-phase coupling patterns reveal laminar identity in primate cortex
eLife 12:e84512.
https://doi.org/10.7554/eLife.84512

Share this article

https://doi.org/10.7554/eLife.84512

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