Interactions of Carbon Dioxide and Food Odours in Drosophila: Olfactory Hedonics and Sensory Neuron Properties

Abstract

Behavioural responses of animals to volatiles in their environment are generally dependent on context. Most natural odours are mixtures of components that can each induce different behaviours when presented on their own. We have investigated how a complex of two olfactory stimuli is evaluated by Drosophila flies in a free-flying two-trap choice assay and how these stimuli are encoded in olfactory receptor neurons. We first observed that volatiles from apple cider vinegar attracted flies while carbon dioxide (CO2) was avoided, confirming their inherent positive and negative values. In contradiction with previous results obtained from walking flies in a four-field olfactometer, in the present assay the addition of CO2 to vinegar increased rather than decreased the attractiveness of vinegar. This effect was female-specific even though males and females responded similarly to CO2 and vinegar on their own. To test whether the female-specific behavioural response to the mixture correlated with a sexual dimorphism at the peripheral level we recorded from olfactory receptor neurons stimulated with vinegar, CO2 and their combination. Responses to vinegar were obtained from three neuron classes, two of them housed with the CO2-responsive neuron in ab1 sensilla. Sensitivity of these neurons to both CO2 and vinegar per se did not differ between males and females and responses from female neurons did not change when CO2 and vinegar were presented simultaneously. We also found that CO2-sensitive neurons are particularly well adapted to respond rapidly to small concentration changes irrespective of background CO2 levels. The ability to encode temporal properties of stimulations differs considerably between CO2- and vinegar-sensitive neurons. These properties may have important implications for in-flight navigation when rapid responses to fragmented odour plumes are crucial to locate odour sources. However, the flies’ sex-specific response to the CO2-vinegar combination and the context-dependent hedonics most likely originate from central rather than peripheral processing.

Behavioral and Antennal Responses of Drosophila suzukii (Diptera: Drosophilidae) to Volatiles From Fruit Extracts

“…Among vinegar flies, it is known that fruit volatiles are involved in Drosophila spp. orientation (e.g., Lebreton et al 2012, Faucher et al 2013) and oviposition behaviors (e.g., Stensmyr et al 2012, Linz et al 2013. Revadi et al (2012) showed recently that D. suzukii flies are attracted to odors from intact raspberry, blackberry, blueberry, cherry, and strawberry fruit, indicating that fruit volatiles are important in D. suzukii host location.…”

A Higher Brain Circuit for Immediate Integration of Conflicting Sensory Information in Drosophila

“…First of all, not all food odors and thus potential food sources might inhibit CO 2 avoidance by these means. Certainly, vinegar in spite of its behavioral effect does not fall into this category and does not affect sensory neuron responses to CO 2 [13]. Second, it is likely more efficient to block or modulate a neural pathway at multiple levels.…”

“…Despite this positive association, flies innately avoid CO 2 across a large range of concentrations, possibly because it may represent a danger signal released by other flies in stressful situations [9]. How and where flies process CO 2 in these two different contexts to either overcome or submit to their aversion of this odor is not fully understood [10][11][12][13]. Behavioral drive and internal state, however, appear to strongly impact on how CO 2 is perceived [11,13,14].…”

“…How and where flies process CO 2 in these two different contexts to either overcome or submit to their aversion of this odor is not fully understood [10][11][12][13]. Behavioral drive and internal state, however, appear to strongly impact on how CO 2 is perceived [11,13,14]. Given these characteristics, CO 2 represents an excellent model for studying the modulation of innate olfactory behaviors.…”

Intracellular regulation of the insect chemoreceptor complex impacts odor localization in flying insects

“…Responses were calculated as the mean distance flies covered within 4 s after encounter with the odour pulse. In the free-flight trap assay, 30, 4-6 day old female flies, starved for 24 h were released in a 50×50×50 cm mesh cage (Faucher et al, 2013). From preliminary tests, fly catches using either vinegar alone or the single odour were low when tested in the free-flight assay.…”