State-dependent representations of mixtures by the olfactory bulb

  1. Aliya Mari Adefuin
  2. Sander Lindeman
  3. Janine K Reinert
  4. Izumi Fukunaga  Is a corresponding author
  1. Okinawa Institute of Science and Technology Graduate University, Japan

Abstract

Sensory systems are often tasked to analyse complex signals from the environment, separating relevant from irrelevant parts. This process of decomposing signals is challenging when a mixture of signals does not equal the sum of its parts, leading to an unpredictable corruption of signal patterns. In olfaction, nonlinear summation is prevalent at various stages of sensory processing. Here, we investigate how the olfactory system deals with binary mixtures of odours under different brain states, using two-photon imaging of olfactory bulb (OB) output neurons. Unlike previous studies using anaesthetised animals, we found that mixture summation is more linear in the early phase of evoked responses in awake, head-fixed mice performing an odour detection task, due to dampened responses. Despite this, and responses being more variable, decoding analyses indicated that the data from behaving mice was well discriminable. Curiously, the time course of decoding accuracy did not correlate strictly with the linearity of summation. Further, a comparison with naïve mice indicated that learning to accurately perform the mixture detection task is not accompanied by more linear mixture summation. Finally, using a simulation, we demonstrate that, while saturating sublinearity tends to degrade the discriminability, the extent of the impairment may depend on other factors, including pattern decorrelation. Altogether, our results demonstrate that the mixture representation in the primary olfactory area is state-dependent, but the analytical perception may not strictly correlate with linearity in summation.

Data availability

The files consist of individual data to compare linear sum vs. observed mixture responses (300 - 1000 ms after odour onset).

The following data sets were generated
    1. Fukunaga I
    (2022) Figure 6C
    Dryad Digital Repository, doi:10.5061/dryad.p2ngf1vrh.

Article and author information

Author details

  1. Aliya Mari Adefuin

    Sensory and Behavioural Neuroscience Unit, Okinawa Institute of Science and Technology Graduate University, Okinawa, Japan
    Competing interests
    The authors declare that no competing interests exist.
  2. Sander Lindeman

    Sensory and Behavioural Neuroscience Unit, Okinawa Institute of Science and Technology Graduate University, Okinawa, Japan
    Competing interests
    The authors declare that no competing interests exist.
  3. Janine K Reinert

    Sensory and Behavioural Neuroscience Unit, Okinawa Institute of Science and Technology Graduate University, Okinawa, Japan
    Competing interests
    The authors declare that no competing interests exist.
  4. Izumi Fukunaga

    Sensory and Behavioural Neuroscience Unit, Okinawa Institute of Science and Technology Graduate University, Okinawa, Japan
    For correspondence
    izumi.fukunaga@oist.jp
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1860-5377

Funding

Okinawa Institute of Science and Technology Graduate University

  • Aliya Mari Adefuin
  • Sander Lindeman
  • Janine K Reinert
  • Izumi Fukunaga

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

Reviewing Editor

  1. Naoshige Uchida, Harvard University, United States

Ethics

Animal experimentation: All procedures described in this study have been approved by the OIST Graduate University's Animal Care and Use Committee (Protocol 2016-151 and 2020-310)

Version history

  1. Preprint posted: September 24, 2021 (view preprint)
  2. Received: January 7, 2022
  3. Accepted: March 5, 2022
  4. Accepted Manuscript published: March 7, 2022 (version 1)
  5. Version of Record published: March 21, 2022 (version 2)

Copyright

© 2022, Adefuin 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. Aliya Mari Adefuin
  2. Sander Lindeman
  3. Janine K Reinert
  4. Izumi Fukunaga
(2022)
State-dependent representations of mixtures by the olfactory bulb
eLife 11:e76882.
https://doi.org/10.7554/eLife.76882

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https://doi.org/10.7554/eLife.76882

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