Abstract

Natural environments feature mixtures of odorants of diverse quantities, qualities and complexities. Olfactory receptor neurons (ORNs) are the first layer in the sensory pathway and transmit the olfactory signal to higher regions of the brain. Yet, the response of ORNs to mixtures is strongly non-additive, and exhibits antagonistic interactions among odorants. Here, we model the processing of mixtures by mammalian ORNs, focusing on the role of inhibitory mechanisms. We show how antagonism leads to an effective 'normalization' of the ensemble ORN response, that is, the distribution of responses of the ORN population induced by any mixture is largely independent of the number of components in the mixture. This property arises from a novel mechanism involving the distinct statistical properties of receptor binding and activation, without any recurrent neuronal circuitry. Normalization allows our encoding model to outperform non-interacting models in odor discrimination tasks, leads to experimentally testable predictions and explains several psychophysical experiments in humans.

Highlights

  • The olfactory system, like other sensory modalities, is entrusted to perform certain basic computational tasks

  • Inhibitory interactions in the form of receptor antagonism have been observed in experiments with olfactory receptor neurons (ORNs) (Oka et al, 2004; Takeuchi et al, 2009; Kurahashi et al, 1994), it has not been quantified systematically

  • Odorants in the nasal cavity are captured by G-protein-coupled-receptors located on the cilia of ORNs

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Summary

Introduction

The olfactory system, like other sensory modalities, is entrusted to perform certain basic computational tasks. Of primary importance is the specific identification of odors and the recognition of isolated sources or objects in an olfactory scene. A typical scene in a natural environment is complex: the olfactory landscape is determined by the chemical composition of odorants released by the objects, the stoichiometry of the mixture and the physical location of the objects relative to the observer. The importance of filtering a complex background is shared by the olfactory and the adaptive immune systems. In the latter, lymphocytes must quickly and accurately identify a small fraction of foreign ligands in a sea of native ligands (Abbas et al, 2014). The response of cells expressing the mOR-EG receptor is strongly suppressed when methyl isoeugenol is

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