1. Neuroscience
Download icon

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
Research Article
  • Cited 8
  • Views 2,959
  • Annotations
Cite this article as: eLife 2018;7:e34831 doi: 10.7554/eLife.34831

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

  • 2,959
    Page views
  • 460
    Downloads
  • 8
    Citations

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

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)

Download citations (links to download the citations from this article in formats compatible with various reference manager tools)

Open citations (links to open the citations from this article in various online reference manager services)

Categories and tags

Further reading

    1. Neuroscience

    The connectome of the adult Drosophila mushroom body provides insights into function

    Feng Li et al.
    Research Article Updated

    Making inferences about the computations performed by neuronal circuits from synapse-level connectivity maps is an emerging opportunity in neuroscience. The mushroom body (MB) is well positioned for developing and testing such an approach due to its conserved neuronal architecture, recently completed dense connectome, and extensive prior experimental studies of its roles in learning, memory, and activity regulation. Here, we identify new components of the MB circuit in Drosophila, including extensive visual input and MB output neurons (MBONs) with direct connections to descending neurons. We find unexpected structure in sensory inputs, in the transfer of information about different sensory modalities to MBONs, and in the modulation of that transfer by dopaminergic neurons (DANs). We provide insights into the circuitry used to integrate MB outputs, connectivity between the MB and the central complex and inputs to DANs, including feedback from MBONs. Our results provide a foundation for further theoretical and experimental work.

    1. Neuroscience

    Dissociation of task engagement and arousal effects in auditory cortex and midbrain

    Daniela Saderi et al.
    Research Article Updated

    Both generalized arousal and engagement in a specific task influence sensory neural processing. To isolate effects of these state variables in the auditory system, we recorded single-unit activity from primary auditory cortex (A1) and inferior colliculus (IC) of ferrets during a tone detection task, while monitoring arousal via changes in pupil size. We used a generalized linear model to assess the influence of task engagement and pupil size on sound-evoked activity. In both areas, these two variables affected independent neural populations. Pupil size effects were more prominent in IC, while pupil and task engagement effects were equally likely in A1. Task engagement was correlated with larger pupil; thus, some apparent effects of task engagement should in fact be attributed to fluctuations in pupil size. These results indicate a hierarchy of auditory processing, where generalized arousal enhances activity in midbrain, and effects specific to task engagement become more prominent in cortex.

    1. Neuroscience

    Brain endothelial cell TRPA1 channels initiate neurovascular coupling

    Pratish Thakore et al.
    Research Article

    Cerebral blood flow is dynamically regulated by neurovascular coupling to meet the dynamic metabolic demands of the brain. We hypothesized that TRPA1 channels in capillary endothelial cells are stimulated by neuronal activity and instigate a propagating retrograde signal that dilates upstream parenchymal arterioles to initiate functional hyperemia. We find that activation of TRPA1 in capillary beds and post-arteriole transitional segments with mural cell coverage initiates retrograde signals that dilate upstream arterioles. These signals exhibit a unique mode of biphasic propagation. Slow, short-range intercellular Ca2+ signals in the capillary network are converted to rapid electrical signals in transitional segments that propagate to and dilate upstream arterioles. We further demonstrate that TRPA1 is necessary for functional hyperemia and neurovascular coupling within the somatosensory cortex of mice in vivo. These data establish endothelial cell TRPA1 channels as neuronal activity sensors that initiate microvascular vasodilatory responses to redirect blood to regions of metabolic demand.