Tests of the chromatographic theory of olfaction with highly soluble odors: a combined electro-olfactogram and computational fluid dynamics study in the mouse.

David M Coppola,Alex D Rygg,Brent A Craven,Emily Fitzwater

doi:10.1242/bio.047217

Abstract

ABSTRACTThe idea that the vertebrate nasal cavity operates like a gas chromatograph to separate and discriminate odors, referred to herein as the ‘chromatographic theory’ (CT), has a long and interesting history. Though the last decade has seen renewed interest in the notion, its validity remains in question. Here we examine a necessary condition of the theory: a correlation between nasal odor deposition patterns based on mucus solubility and the distribution of olfactory sensory neuron odotypes. Our recent work in the mouse failed to find such a relationship even across large sorption gradients within the olfactory epithelium (OE). However, these studies did not test extremely soluble odorants or low odor concentrations, factors that could explain our inability to find supporting evidence for the CT. The current study combined computational fluid dynamics (CFD) simulations of odor sorption patterns and electro-olfactogram (EOG) measurements of olfactory sensory neuron responses. The odorants tested were at the extremes of mucus solubility and at a range of concentrations. Results showed no relationship between local odor sorption patterns and EOG response maps. Together, results again failed to support a necessary condition of the CT casting further doubt on the viability of this classical odor coding mechanism.

Highlights

More than a half century ago, Maxwell Mozell (1964, 1966, 1970) made a series of observations in the frog that prompted him to liken the workings of the vertebrate nasal mucosa to a gas chromatograph, an analogy that crystalized ideas about a mechanism of odor discrimination based on receptor spatial layout suggested earlier by his mentor, the Nobel laureate, Lord Adrian (1942, 1950, 1954)
It is clear that the chromatographic theory (CT) predicts a relationship between odor sorption patterns, which are dictated by odor mucus solubility and nasal airflow, and the distribution of olfactory sensory neuron receptive-field types
Our sampling of six whole-mount and five cryostat-sectioned mice suggest that the NQO1 pattern, and by inference the boundaries of the dorsal olfactory receptor zone, is quite similar across animals

Summary

Introduction

More than a half century ago, Maxwell Mozell (1964, 1966, 1970) made a series of observations in the frog that prompted him to liken the workings of the vertebrate nasal mucosa to a gas chromatograph, an analogy that crystalized ideas about a mechanism of odor discrimination based on receptor spatial layout suggested earlier by his mentor, the Nobel laureate, Lord Adrian (1942, 1950, 1954). For Adrian, his proposed mechanism rendered olfaction consistent with the other exteroceptive sensory epithelia like the retina, cochlea and somatosensory components of the skin, in having a spatial logic. It is clear that the chromatographic theory (CT) predicts a relationship between odor sorption patterns, which are dictated by odor mucus solubility and nasal airflow, and the distribution of olfactory sensory neuron receptive-field types

Methods

Results

Conclusion