The internal state of an organism influences its perception of attractive or aversive stimuli and thus promotes adaptive behaviors that increase its likelihood of survival. The mechanisms underlying these perceptual shifts are critical to our understanding of how neural circuits support animal cognition and behavior. Starved flies exhibit enhanced sensitivity to attractive odors and reduced sensitivity to aversive odors. Here, we show that a functional remodeling of the olfactory map is mediated by two parallel neuromodulatory systems that act in opposing directions on olfactory attraction and aversion at the level of the first synapse. Short neuropeptide F sensitizes an antennal lobe glomerulus wired for attraction, while tachykinin (DTK) suppresses activity of a glomerulus wired for aversion. Thus we show parallel neuromodulatory systems functionally reconfigure early olfactory processing to optimize detection of nutrients at the risk of ignoring potentially toxic food resources.DOI: http://dx.doi.org/10.7554/eLife.08298.001

SUMMARY During the lifespans of most animals, reproductive maturity and mating activity are highly coordinated. In Drosophila melanogaster, for instance, male fertility increases with age and older males are known to have a copulation advantage over young ones. The molecular and neural basis of this age-related disparity in mating behavior is unknown. Here we show that the Or47b odorant receptor is required for the copulation advantage of older males. Notably, the sensitivity of Or47b neurons to a stimulatory pheromone, palmitoleic acid, is low in young males but high in older ones, which accounts for older males’ higher courtship intensity. Mechanistically, this age-related sensitization of Or47b neurons requires a reproductive hormone, juvenile hormone, as well as its binding protein Methoprene-tolerant in Or47b neurons. Together, our study identifies a direct neural substrate for juvenile hormone that permits coordination of courtship activity with reproductive maturity to maximize male reproductive fitness.

Highlights d Group housing enhances courtship motivation in mature but not immature males d Group housing elevates the pheromone response of Or47b ORNs only in mature males d CaMKI/CBP pathway synergizes with juvenile hormone in sensitizing Or47b ORNs d Fru M levels fine-tune pheromone sensitivity according to both fly density and age

Highlights d Ionotropic signal amplification occurs in select olfactory receptor neurons (ORNs) d Amplification is mediated by Pickpocket 25 (PPK25), a DEG/ENaC member d Receptor-mediated influx of Ca 2+ , serving as a second messenger, activates PPK25 d A reproductive hormone dynamically regulates PPK25 expression to impact courtship Authors

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