Single olfactory sensory neurons simultaneously integrate the components of an odour mixture

Abstract

Most odours are complex mixtures. However, the capacities of olfactory sensory neurons (OSNs) to process complex odour stimuli have never been explored in air-breathing vertebrates. To face this issue, the present study compares the electrical responses of single OSNs to two odour molecules, delivered singly and mixed together, in rats in vivo. This work is the first aimed at demonstrating that single OSNs simultaneously integrate several chemical signals and which, furthermore, attempts to describe such processes for the whole concentration range over which single OSNs can work. The results stress that complex interactions occur between components in odour mixtures and that OSN responses to such mixtures are not simply predictable from the responses to their components. Three types of interactions are described. They are termed suppression, hypoadditivity and synergy, in accord with psychophysical terminology. This allows us to draw links between peripheral odour reception and central odour coding. Indeed, events occurring in single OSNs may account for the dominating or even the masking effects of odour molecules in complex mixtures, i.e. for the prevailing action of a minor component in the final qualitative perception of a mixture. We conclude that our observations with binary mixtures anticipate the complexity of processes which may rise at the level of a single OSN in physiological conditions. Following this hypothesis, a natural odour would induce a multi-chemical integration at the level of single OSNs which may result in refining their individual odour-coding properties, leading them to play a crucial role in the final performance of the olfactory system.

Odor detection of single chemicals and binary mixtures

“…psychophysically at high detectability has a further neurophysiological correlate, measured as spike frequency of single olfactory neurons [23]. The responses of receptor cells to binary mixtures shifted towards decreasing additivity as the concentration of the mixed chemicals increased.…”

Plant odour stimuli reshape pheromonal representation in neurons of the antennal lobe macroglomerular complex of a male moth

“…According to the definition of interactions described by Duchamp-Viret et al (Duchamp-Viret et al, 2003), A1 and A2 neurons showed a 'suppression' type of mixture interaction. Purely excitatory or purely inhibitory responses of B and C neurons to the pheromone were not affected when heptanal was added, thus these neurons exhibited a 'hypoadditivity' type of interaction.…”

“…A widely used definition of interaction types arises from frog ORN recordings Odour interactions in the moth MGC (Duchamp-Viret et al, 2003;Rospars et al, 2008): hypoaddivity is described as a response to the mixture, which is equal to or a little lower than the response to the strongest component; a response to the mixture lower than the strongest component is defined as suppression, and synergism is defined as a response to the mixture that is stronger than the response to the strongest component (Duchamp-Viret et al, 2003). All three interaction types have been found in insects at different neuronal levels from the analysis of responses to mixtures of general odorants and mixtures of pheromone components [honeybee (Deisig et al, 2006); moths (Martin and Hildebrand, 2010;Kuebler et al, 2011;Hillier and Vickers, 2011); Drosophila (Silbering and Galizia, 2007)].…”

Antennal Lobe Processing Correlates to Moth Olfactory Behavior

“…We differentiated between two main network interaction types, synergism and suppression (Duchamp-Viret et al, 2003;Silbering and Galizia, 2007;Kuebler et al, 2011b). Our criteria were highly restrictive: to be considered as a suppressive interaction, at least one of the activity regions in the mixture pattern (black bars) had to completely disappear compared with the projected mixture (white bars).…”