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.

Reviewing Editor

  1. Naoshige Uchida, Harvard University, United States

Publication history

  1. Received: January 5, 2018
  2. Accepted: March 20, 2018
  3. Accepted Manuscript published: March 29, 2018 (version 1)
  4. Version of Record published: April 16, 2018 (version 2)

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

  • 3,298
    Page views
  • 506
    Downloads
  • 21
    Citations

Article citation count generated by polling the highest count across the following sources: Crossref, Scopus, PubMed Central.

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

Further reading

    1. Developmental Biology
    2. Neuroscience
    Ashtyn T Wiltbank et al.
    Research Article

    Efficient neurotransmission is essential for organism survival and is enhanced by myelination. However, the genes that regulate myelin and myelinating glial cell development have not been fully characterized. Data from our lab and others demonstrates that cd59, which encodes for a small GPI-anchored glycoprotein, is highly expressed in developing zebrafish, rodent, and human oligodendrocytes (OLs) and Schwann cells (SCs), and that patients with CD59 dysfunction develop neurological dysfunction during early childhood. Yet, the function of Cd59 in the developing nervous system is currently undefined. In this study, we demonstrate that cd59 is expressed in a subset of developing SCs. Using cd59 mutant zebrafish, we show that developing SCs proliferate excessively and nerves may have reduced myelin volume, altered myelin ultrastructure, and perturbed node of Ranvier assembly. Finally, we demonstrate that complement activity is elevated in cd59 mutants and that inhibiting inflammation restores SC proliferation, myelin volume, and nodes of Ranvier to wildtype levels. Together, this work identifies Cd59 and developmental inflammation as key players in myelinating glial cell development, highlighting the collaboration between glia and the innate immune system to ensure normal neural development.

    1. Neuroscience
    Arefeh Sherafati et al.
    Research Article Updated

    Cochlear implants are neuroprosthetic devices that can restore hearing in people with severe to profound hearing loss by electrically stimulating the auditory nerve. Because of physical limitations on the precision of this stimulation, the acoustic information delivered by a cochlear implant does not convey the same level of acoustic detail as that conveyed by normal hearing. As a result, speech understanding in listeners with cochlear implants is typically poorer and more effortful than in listeners with normal hearing. The brain networks supporting speech understanding in listeners with cochlear implants are not well understood, partly due to difficulties obtaining functional neuroimaging data in this population. In the current study, we assessed the brain regions supporting spoken word understanding in adult listeners with right unilateral cochlear implants (n=20) and matched controls (n=18) using high-density diffuse optical tomography (HD-DOT), a quiet and non-invasive imaging modality with spatial resolution comparable to that of functional MRI. We found that while listening to spoken words in quiet, listeners with cochlear implants showed greater activity in the left prefrontal cortex than listeners with normal hearing, specifically in a region engaged in a separate spatial working memory task. These results suggest that listeners with cochlear implants require greater cognitive processing during speech understanding than listeners with normal hearing, supported by compensatory recruitment of the left prefrontal cortex.