A transformation from temporal to ensemble coding in a model of piriform cortex

  1. Merav Stern
  2. Kevin A Bolding
  3. Larry F Abbott
  4. Kevin M Franks  Is a corresponding author
  1. Hebrew University, Israel
  2. Duke University Medical School, United States
  3. Columbia University, United States
  4. Duke University School of Medicine, United States

Abstract

Different coding strategies are used to represent odor information at various stages of the mammalian olfactory system. A temporal latency code represents odor identity in olfactory bulb (OB), but this temporal information is discarded in piriform cortex (PCx) where odor identity is instead encoded through ensemble membership. We developed a spiking PCx network model to understand how this transformation is implemented. In the model, the impact of OB inputs activated earliest after inhalation is amplified within PCx by diffuse recurrent collateral excitation, which then recruits strong, sustained feedback inhibition that suppresses the impact of later-responding glomeruli. We model increasing odor concentrations by decreasing glomerulus onset latencies while preserving their activation sequences. This produces a multiplexed cortical odor code in which activated ensembles are robust to concentration changes while concentration information is encoded through population synchrony. Our model demonstrates how PCx circuitry can implement multiplexed ensemble-identity/temporal-concentration odor coding.

Article and author information

Author details

  1. Merav Stern

    Edmond and Lily Safra Center for Brain Sciences, Hebrew University, Jerusalem, Israel
    Competing interests
    The authors declare that no competing interests exist.
  2. Kevin A Bolding

    Department of Neurobiology, Duke University Medical School, Durham, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2271-5280
  3. Larry F Abbott

    Department of Neuroscience, Columbia University, New York, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Kevin M Franks

    Department of Neurobiology, Duke University School of Medicine, Durham, United States
    For correspondence
    franks@neuro.duke.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6386-9518

Funding

National Institute on Deafness and Other Communication Disorders (DC015525)

  • Kevin M Franks

National Institute on Deafness and Other Communication Disorders (DC016782)

  • Kevin M Franks

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 experimental protocols were approved by Duke University Institutional Animal Care and Use Committee (protocol # A220-15-08), which was approved on 08-27-2015.

Copyright

© 2018, Stern 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

  • 3,846
    views
  • 582
    downloads
  • 49
    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. Merav Stern
  2. Kevin A Bolding
  3. Larry F Abbott
  4. Kevin M Franks
(2018)
A transformation from temporal to ensemble coding in a model of piriform cortex
eLife 7:e34831.
https://doi.org/10.7554/eLife.34831

Share this article

https://doi.org/10.7554/eLife.34831

Further reading

    1. Neuroscience
    Friedrich Schuessler, Francesca Mastrogiuseppe ... Omri Barak
    Research Article

    The relation between neural activity and behaviorally relevant variables is at the heart of neuroscience research. When strong, this relation is termed a neural representation. There is increasing evidence, however, for partial dissociations between activity in an area and relevant external variables. While many explanations have been proposed, a theoretical framework for the relationship between external and internal variables is lacking. Here, we utilize recurrent neural networks (RNNs) to explore the question of when and how neural dynamics and the network’s output are related from a geometrical point of view. We find that training RNNs can lead to two dynamical regimes: dynamics can either be aligned with the directions that generate output variables, or oblique to them. We show that the choice of readout weight magnitude before training can serve as a control knob between the regimes, similar to recent findings in feedforward networks. These regimes are functionally distinct. Oblique networks are more heterogeneous and suppress noise in their output directions. They are furthermore more robust to perturbations along the output directions. Crucially, the oblique regime is specific to recurrent (but not feedforward) networks, arising from dynamical stability considerations. Finally, we show that tendencies toward the aligned or the oblique regime can be dissociated in neural recordings. Altogether, our results open a new perspective for interpreting neural activity by relating network dynamics and their output.

    1. Neuroscience
    Sudhanvan Iyer, Kathryn Maxson Jones ... Mary A Majumder
    Review Article

    In this paper, we provide an overview and analysis of the BRAIN Initiative data-sharing ecosystem. First, we compare and contrast the characteristics of the seven BRAIN Initiative data archives germane to data sharing and reuse, namely data submission and access procedures and aspects of interoperability. Second, we discuss challenges, benefits, and future opportunities, focusing on issues largely specific to sharing human data and drawing on N = 34 interviews with diverse stakeholders. The BRAIN Initiative-funded archive ecosystem faces interoperability and data stewardship challenges, such as achieving and maintaining interoperability of data and archives and harmonizing research participants’ informed consents for tiers of access for human data across multiple archives. Yet, a benefit of this distributed archive ecosystem is the ability of more specialized archives to adapt to the needs of particular research communities. Finally, the multiple archives offer ample raw material for network evolution in response to the needs of neuroscientists over time. Our first objective in this paper is to provide a guide to the BRAIN Initiative data-sharing ecosystem for readers interested in sharing and reusing neuroscience data. Second, our analysis supports the development of empirically informed policy and practice aimed at making neuroscience data more findable, accessible, interoperable, and reusable.