Mechanisms and functions of respiration-driven gamma oscillations in the primary olfactory cortex

  1. Joaquin Gonzalez  Is a corresponding author
  2. Pablo Torterolo
  3. Adriano BL Tort  Is a corresponding author
  1. Universidad de la Republica, Uruguay
  2. Federal University of Rio Grande do Norte, Brazil

Abstract

Gamma oscillations are believed to underlie cognitive processes by shaping the formation of transient neuronal partnerships on a millisecond scale. These oscillations are coupled to the phase of breathing cycles in several brain areas, possibly reflecting local computations driven by sensory inputs sampled at each breath. Here, we investigated the mechanisms and functions of gamma oscillations in the piriform (olfactory) cortex of awake mice to understand their dependence on breathing and how they relate to local spiking activity. Mechanistically, we find that respiration drives gamma oscillations in the piriform cortex, which correlate with local feedback inhibition and result from recurrent connections between local excitatory and inhibitory neuronal populations. Moreover, respiration-driven gamma oscillations are triggered by the activation of mitral/tufted cells in the olfactory bulb and are abolished during ketamine/xylazine anesthesia. Functionally, we demonstrate that they locally segregate neuronal assemblies through a winner-take-all computation leading to sparse odor coding during each breathing cycle. Our results shed new light on the mechanisms of gamma oscillations, bridging computation, cognition and physiology.

Data availability

All the data employed is freely available at: http://crcns.org, pcx-1 dataset. http://dx.doi.org/10.6080/K00C4SZB

The following previously published data sets were used

Article and author information

Author details

  1. Joaquin Gonzalez

    Departamento de Fisiología, Universidad de la Republica, Montevideo, Uruguay
    For correspondence
    joaqgonzar@gmail.com
    Competing interests
    The authors declare that no competing interests exist.
  2. Pablo Torterolo

    Departamento de Fisiología, Universidad de la Republica, Montevideo, Uruguay
    Competing interests
    The authors declare that no competing interests exist.
  3. Adriano BL Tort

    Brain Institute, Federal University of Rio Grande do Norte, Natal, Brazil
    For correspondence
    tort@neuro.ufrn.br
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9877-7816

Funding

Conselho Nacional de Desenvolvimento Científico e Tecnológico

  • Adriano BL Tort

Coordenação de Aperfeiçoamento de Pessoal de Nível Superior

  • Adriano BL Tort

Comisión Sectorial de Investigación Científica

  • Joaquin Gonzalez
  • Pablo Torterolo

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

Ethics

Animal experimentation: The present study used a third-party dataset and required no ethical permit for the performed computational analyses. The experimental protocols of the original data source (Bolding and Franks, 2018) were approved by Duke University Institutional Animal Care and Use Committee (protocol A220-15-08).

Reviewing Editor

  1. Laura L Colgin, University of Texas at Austin, United States

Publication history

  1. Received: August 28, 2022
  2. Accepted: February 17, 2023
  3. Accepted Manuscript published: February 20, 2023 (version 1)

Copyright

© 2023, Gonzalez 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.

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  1. Joaquin Gonzalez
  2. Pablo Torterolo
  3. Adriano BL Tort
(2023)
Mechanisms and functions of respiration-driven gamma oscillations in the primary olfactory cortex
eLife 12:e83044.
https://doi.org/10.7554/eLife.83044

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