Cell and circuit origins of fast network oscillations in the mammalian main olfactory bulb

  1. Shawn D Burton  Is a corresponding author
  2. Nathan N Urban  Is a corresponding author
  1. Lehigh University, United States

Abstract

Neural synchrony generates fast network oscillations throughout the brain, including the main olfactory bulb (MOB), the first processing station of the olfactory system. Identifying the mechanisms synchronizing neurons in the MOB will be key to understanding how network oscillations support the coding of a high-dimensional sensory space. Here, using paired recordings and optogenetic activation of glomerular sensory inputs in MOB slices, we uncovered profound differences in principal mitral cell (MC) vs. tufted cell (TC) spike-time synchrony: TCs robustly synchronized across fast- and slow-gamma frequencies, while MC synchrony was weaker and concentrated in slow-gamma frequencies. Synchrony among both cell types was enhanced by shared glomerular input but was independent of intraglomerular lateral excitation. Cell-type differences in synchrony could also not be traced to any difference in the synchronization of synaptic inhibition. Instead, greater TC than MC synchrony paralleled the more periodic firing among resonant TCs than MCs and emerged in patterns consistent with densely synchronous network oscillations. Collectively, our results thus reveal a mechanism for parallel processing of sensory information in the MOB via differential TC vs. MC synchrony, and further contrast mechanisms driving fast network oscillations in the MOB from those driving the sparse synchronization of irregularly-firing principal cells throughout cortex.

Data availability

All data generated or analyzed during this study are included in the manuscript and supporting files. Source data files have been provided for all figures.

Article and author information

Author details

  1. Shawn D Burton

    Biological Sciences, Lehigh University, Bethlehem, United States
    For correspondence
    shb420@lehigh.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8907-6487
  2. Nathan N Urban

    Biological Sciences, Lehigh University, Bethlehem, United States
    For correspondence
    nnu220@lehigh.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0365-9068

Funding

National Institue on Deafness and Other Communication Disorders (R01DC016560)

  • Nathan N Urban

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

Reviewing Editor

  1. Gary L Westbrook, Oregon Health and Science University, United States

Ethics

Animal experimentation: All experiments were completed in compliance with the guidelines established by the Institutional Animal Care and Use Committee of the University of Pittsburgh (protocol #18103723).

Version history

  1. Received: September 25, 2021
  2. Accepted: October 9, 2021
  3. Accepted Manuscript published: October 18, 2021 (version 1)
  4. Version of Record published: October 28, 2021 (version 2)

Copyright

© 2021, Burton & Urban

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. Shawn D Burton
  2. Nathan N Urban
(2021)
Cell and circuit origins of fast network oscillations in the mammalian main olfactory bulb
eLife 10:e74213.
https://doi.org/10.7554/eLife.74213

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https://doi.org/10.7554/eLife.74213

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