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.

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).

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.

Metrics

  • 1,736
    views
  • 246
    downloads
  • 11
    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. 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

Further reading

    1. Neuroscience
    Yanqi Liu, Pol Bech ... Carl CH Petersen
    Research Article

    Long-range axonal projections of diverse classes of neocortical excitatory neurons likely contribute to brain-wide interactions processing sensory, cognitive and motor signals. Here, we performed light-sheet imaging of fluorescently labeled axons from genetically defined neurons located in posterior primary somatosensory barrel cortex and supplemental somatosensory cortex. We used convolutional networks to segment axon-containing voxels and quantified their distribution within the Allen Mouse Brain Atlas Common Coordinate Framework. Axonal density was analyzed for different classes of glutamatergic neurons using transgenic mouse lines selectively expressing Cre recombinase in layer 2/3 intratelencephalic projection neurons (Rasgrf2-dCre), layer 4 intratelencephalic projection neurons (Scnn1a-Cre), layer 5 intratelencephalic projection neurons (Tlx3-Cre), layer 5 pyramidal tract projection neurons (Sim1-Cre), layer 5 projection neurons (Rbp4-Cre), and layer 6 corticothalamic neurons (Ntsr1-Cre). We found distinct axonal projections from the different neuronal classes to many downstream brain areas, which were largely similar for primary and supplementary somatosensory cortices. Functional connectivity maps obtained from optogenetic activation of sensory cortex and wide-field imaging revealed topographically organized evoked activity in frontal cortex with neurons located more laterally in somatosensory cortex signaling to more anteriorly located regions in motor cortex, consistent with the anatomical projections. The current methodology therefore appears to quantify brain-wide axonal innervation patterns supporting brain-wide signaling.

    1. Neuroscience
    Jun Yang, Hanqi Zhang, Sukbin Lim
    Research Article

    Errors in stimulus estimation reveal how stimulus representation changes during cognitive processes. Repulsive bias and minimum variance observed near cardinal axes are well-known error patterns typically associated with visual orientation perception. Recent experiments suggest that these errors continuously evolve during working memory, posing a challenge that neither static sensory models nor traditional memory models can address. Here, we demonstrate that these evolving errors, maintaining characteristic shapes, require network interaction between two distinct modules. Each module fulfills efficient sensory encoding and memory maintenance, which cannot be achieved simultaneously in a single-module network. The sensory module exhibits heterogeneous tuning with strong inhibitory modulation reflecting natural orientation statistics. While the memory module, operating alone, supports homogeneous representation via continuous attractor dynamics, the fully connected network forms discrete attractors with moderate drift speed and nonuniform diffusion processes. Together, our work underscores the significance of sensory-memory interaction in continuously shaping stimulus representation during working memory.