State-dependent representations of mixtures by the olfactory bulb

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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.

https://dx.doi.org/10.5061/dryad.p2ngf1vrh

Article and author information

Author details

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.
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.
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.
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.

"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.

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)

Copyright

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.