Millisecond Stimulus Onset-Asynchrony Enhances Information about Components in an Odor Mixture

Abstract

Airborne odorants rarely occur as pure, isolated stimuli. In a natural environment, odorants that intermingle from multiple sources create mixtures in which the onset and offset of odor components are asynchronous. Odor mixtures are known to elicit interactions in both behavioral and physiological responses, changing the perceptive quality of mixtures compared with the components. However, relevant odors need to be segregated from a distractive background. Honeybees (Apis mellifera) can use stimulus onset asynchrony of as little as 6 ms to segregate learned odor components within a mixture. Using in vivo calcium imaging of projection neurons in the honeybee, we studied neuronal mechanisms of odor-background segregation based on stimulus onset asynchrony in the antennal lobe. We found that asynchronous mixtures elicit response patterns that are different from their synchronous counterpart: the responses to asynchronous mixtures contain more information about the constituent components. With longer onset shifts, more features of the components were present in the mixture response patterns. Moreover, we found that the processing of asynchronous mixtures activated more inhibitory interactions than the processing of synchronous mixtures. This study provides evidence of neuronal mechanisms that underlie odor-object segregation on a timescale much faster than found for mammals.

Data-driven honeybee antennal lobe model suggests how stimulus-onset asynchrony can aid odour segregation

“…At the end the trajectories then follow the trajectory of the response to the trailing odourant. This corresponds well to similar results reported by Broome et al (2006) in the locust and our observations in experiments (see figure 6 in (Stierle et al, 2013)). …”

“…To further dissect our results and relate them to our concurrent experimental work (Stierle et al, 2013) but also previous work in locust (Broome et al, 2006) we visualised the 30 dimensional response patterns by the first two principle components (Figure 7). The N-6-H response is almost identical to the HN response and its template whereas the H-6-N response is between the N response and the HN response, explaining the comparable correlation values to either of them.…”

“…The complete data that was used to reproduce realistic glomerular activation patterns and the resulting matching model data are shown in the supplementary text. The odourants 1-hexanol (subsequently referred to as H) and 1-nonanol (subsequently referred to as N) have previously been used in behavioural and physiological experiments on asynchronous mixture coding in honeybees (Szyszka et al, 2012;Stierle et al, 2013). The responses to 4 odourant concentrations (see colour code in the caption of figure 2) in 30 glomeruli that are well-accessible to Ca 2+ imaging have been used.…”

“…Two previous studies, in locusts and honeybees, have shown that central olfactory neurons are sensitive to odour-onset asynchrony: their responses to mixtures partly match those evoked by the individual components if the onsets of the stimuli differ (Broome et al, 2006;Stierle et al, 2013). In particular, differences in responses were found in the projection neurons (PNs) of the antennal lobe (AL), the first relay of olfactory information in the insect brain.…”

Understanding smell—The olfactory stimulus problem

“…The importance of time dynamics relative to the spatial dimension is an open question (however, please see Stierle et al, 2013;Fukunaga et al, 2012;Nawrot, 2012;Blumhagen et al, 2011;Verhagen et al, 2007), and physiological studies differ in particular on whether they take time explicitly into account. In the present discussion, we focus on how odors are represented by spatial patterns, because the organization of the spatial domain is a particularly puzzling aspect of olfactory processing.…”