Functional interactions among neurons within single columns of macaque V1

  1. Ethan B Trepka
  2. Shude Zhu  Is a corresponding author
  3. Ruobing Xia
  4. Xiaomo Chen
  5. Tirin Moore
  1. Stanford University, United States
  2. Howard Hughes Medical Institute, Stanford University, United States
  3. University of California, Davis, United States

Abstract

Recent developments in high-density neurophysiological tools now make it possible to record from hundreds of single neurons within local, highly interconnected neural networks. Among the many advantages of such recordings is that they dramatically increase the quantity of identifiable, functional interactions between neurons thereby providing an unprecedented view of local circuits. Using high-density, Neuropixels recordings from single neocortical columns of primary visual cortex in nonhuman primates, we identified 1000s of functionally interacting neuronal pairs using established crosscorrelation approaches. Our results reveal clear and systematic variations in the synchrony and strength of functional interactions within single cortical columns. Despite neurons residing within the same column, both measures of interactions depended heavily on the vertical distance separating neuronal pairs, as well as on the similarity of stimulus tuning. In addition, we leveraged the statistical power afforded by the large numbers of functionally interacting pairs to categorize interactions between neurons based on their crosscorrelation functions. These analyses identified distinct, putative classes of functional interactions within the full population. These classes of functional interactions were corroborated by their unique distributions across defined laminar compartments and were consistent with known properties of V1 cortical circuitry, such as the lead-lag relationship between simple and complex cells. Our results provide a clear proof-of-principle for the use of high-density neurophysiological recordings to assess circuit-level interactions within local neuronal networks.

Data availability

All the raw data generated as part of this study are publicly accessible. All the raw code generated for analyzing the data has already been deposited to GitHub and is currently freely accessible (https://github.com/et22/functional_connections_macaque_v1).

The following data sets were generated

Article and author information

Author details

  1. Ethan B Trepka

    Neurosciences Program, Stanford University, Stanford, United States
    Competing interests
    No competing interests declared.
  2. Shude Zhu

    Department of Neurobiology, Howard Hughes Medical Institute, Stanford University, Stanford, United States
    For correspondence
    shude@stanford.edu
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8674-9607
  3. Ruobing Xia

    Department of Neurobiology, Howard Hughes Medical Institute, Stanford University, Stanford, United States
    Competing interests
    No competing interests declared.
  4. Xiaomo Chen

    Department of Neurobiology, Physiology, and BehaviorDepartment of Neurobiology, University of California, Davis, Davis, United States
    Competing interests
    No competing interests declared.
  5. Tirin Moore

    Neurobiology, Howard Hughes Medical Institute, Stanford University, Stanford, United States
    Competing interests
    Tirin Moore, Senior editor, eLife.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3345-2930

Funding

National Eye Institute (Research Project (R01),EY014924)

  • Tirin Moore

National Institute of Neurological Disorders and Stroke (NS116623)

  • Tirin Moore

National Eye Institute (Career transition award (K99),EY029759)

  • Xiaomo Chen

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

Reviewing Editor

  1. Martin Vinck, Ernst Strüngmann Institute (ESI) for Neuroscience in Cooperation with Max Planck Society, Germany

Ethics

Animal experimentation: All experimental procedures were in accordance with National Institutes of Health Guide for the Care and Use of Laboratory Animals, the Society for Neuroscience Guidelines and Policies, and with approved Institutional Animal Care and Use Committee (IACUC) protocol (#APLAC-9900) of Stanford University.

Version history

  1. Preprint posted: February 21, 2022 (view preprint)
  2. Received: April 7, 2022
  3. Accepted: October 30, 2022
  4. Accepted Manuscript published: November 2, 2022 (version 1)
  5. Version of Record published: November 14, 2022 (version 2)

Copyright

© 2022, Trepka 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. Ethan B Trepka
  2. Shude Zhu
  3. Ruobing Xia
  4. Xiaomo Chen
  5. Tirin Moore
(2022)
Functional interactions among neurons within single columns of macaque V1
eLife 11:e79322.
https://doi.org/10.7554/eLife.79322

Share this article

https://doi.org/10.7554/eLife.79322

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