Processing of Odor Mixtures in the Zebrafish Olfactory Bulb

Abstract

Components of odor mixtures often are not perceived individually, suggesting that neural representations of mixtures are not simple combinations of the representations of the components. We studied odor responses to binary mixtures of amino acids and food extracts at different processing stages in the olfactory bulb (OB) of zebrafish. Odor-evoked input to the OB was measured by imaging Ca 2ϩ signals in afferents to olfactory glomeruli. Activity patterns evoked by mixtures were predictable within narrow limits from the component patterns, indicating that mixture interactions in the peripheral olfactory system are weak. OB output neurons, the mitral cells (MCs), were recorded extra-and intracellularly and responded to odors with stimulus-dependent temporal firing rate modulations. Responses to mixtures of amino acids often were dominated by one of the component responses. Responses to mixtures of food extracts, in contrast, were more distinct from both component responses. These results show that mixture interactions can result from processing in the OB. Moreover, our data indicate that mixture interactions in the OB become more pronounced with increasing overlap of input activity patterns evoked by the components. Emerging from these results are rules of mixture interactions that may explain behavioral data and provide a basis for understanding the processing of natural odor stimuli in the OB.

Antennal Lobe Processing Increases Separability of Odor Mixture Representations in the Honeybee

“…We show that a rather fine rearrangement occurs from AL input to output and that such a rearrangement results in a higher separation power between complex odors. Several studies suggested that mixture representation is rather elemental at the input level (zebra fish: Tabor et al 2004;bees: Deisig et al 2006;moths: Carlsson et al 2007; fruit flies : Silbering et al 2007), even though within individual ORNs nonlinear responses to mixtures can be observed (Akers and Getz 1993;Cromarty and Derby 1998;Duchamp-Viret et al 2003). At the output level, studies in the zebrafish (Tabor et al 2004) and in Drosophila (Silbering et al 2007) showed an increased proportion of cases of nonlinear summation between component signals within individual neurons or glomeruli.…”

“…Because natural odors are complex blends including many different components, studying how the neural code for olfactory mixtures is reshaped by AL processing is imperative to understand odor processing in a natural framework. At the OB/AL input level, mixture representation follows essentially elemental rules because it can be predicted from the responses to the components (Carlsson et al 2007; Deisig et al 2006;Silbering and Galizia 2007;Tabor et al 2004). By contrast, at the AL output level, strong interactions between component signals within the AL networks were found in the zebrafish (Tabor et al 2004) and Drosophila (Silbering and Galizia 2007), assigning unique properties to each mixture's representation and making it different from the sum of its components.…”

Synaptic Integration of Olfactory Information in Mouse Anterior Olfactory Nucleus

“…1, available at www.jneurosci.org as supplemental material), three (30%) were to two components, and one (10%) was to three components. Finally, to exclude the possibility that the lack of responses to certain mixtures was attributable to cancellation of responses between mutually inhibitory components (Oka et al, 2004;Tabor et al, 2004), the responses of all (n ϭ 44) cells to individual components of a randomly chosen noneffective mixture were also examined. No responses to individual components in noneffective mixtures were found, reinforcing the idea that mitral cells only respond to a very small fraction of odorants in our panel.…”

Spatial and Temporal Distribution of Odorant-Evoked Activity in the Piriform Cortex

“…Glomeruli serve as the site of synaptic contact between olfactory receptor neurons and second-order neurons, mitral/tufted cells. Most naturally occurring odors are complex mixtures, and the spatial pattern of glomerular activity reflects both individual components (Lin et al, 2006) and early intercomponent interactions (Joerges et al, 1997;Vickers et al, 1998;Tabor et al, 2004). In addition to spatial patterns, both glomerular (Spors et al, 2006) and mitral/ tufted cell activity (Meredith, 1986;Cang and Isaacson, 2003) demonstrate stimulus-specific temporal structure.…”