Neural mechanism for food search behavior in Drosophila melanogaster

Early sensory processing plays a critical role in detecting environmental cues. We used genetic tools to investigate the contribution of odor map in the antennal lobe to behavior in Drosophila. Apple cider vinegar triggers robust innate attraction at a relatively low concentration, which activates six glomeruli. By silencing individual glomeruli, we found that the absence of activity in two glomeruli, DM1 and VA2, markedly reduced attraction. Conversely, when each of these two glomeruli was selectively activated, flies exhibited as robust an attraction to vinegar as wild type flies. Notably, a higher concentration of vinegar excites an additional glomerulus and is less attractive to flies. We show that the activation of the additional glomerulus is necessary and sufficient to mediate the behavioral switch. Together, these results indicate that individual glomeruli, rather than the entire pattern of active glomeruli, mediate innate behavioral output.

Hunger has a profound impact on olfactory behavior. We therefore investigated the neural mechanism for hunger modulation of the antennal lobe odor map and food search behavior. We found that sensory neurons express short neuropeptide F (sNPF) and its receptor (sNPFR1). We established an assay to measure appetitive behavior and found that expression of the neuropeptide and its receptor in odorant receptor neurons (ORNs) is necessary for starvation-induced food search behavior. Using two-photon calcium imaging technique, we found that starvation increases presynaptic activity in select ORNs via sNPF signaling. Furthermore, presynaptic facilitation specifically in Or42b (DM2) neurons is necessary for food finding. Quantitative RT-PCR experiments demonstrated that starvation increases the transcription level of the receptor but not that of the neuropeptide. Thus, starvation increases expression of sNPFR1 to change the odor map in the antennal lobe, resulting in more robust food search behavior.