Gustatory and metabolic perception of nutrient stress in Drosophila

Sleep loss is an adaptive response to nutrient deprivation that alters behavior to maximize the chances of feeding before imminent death. Organisms must maintain systems for detecting the quality of the food source to resume healthy levels of sleep when the stress is alleviated. We determined that gustatory perception of sweetness is both necessary and sufficient to suppress starvation-induced sleep loss when animals encounter nutrient-poor food sources. We further find that blocking specific dopaminergic neurons phenocopies the absence of gustatory stimulation, suggesting a specific role for these neurons in transducing taste information to sleep centers in the brain. Finally, we show that gustatory perception is required for survival, specifically in a low nutrient environment. Overall, these results demonstrate an important role for gustatory perception when environmental food availability approaches zero and illustrate the interplay between sensory and metabolic perception of nutrient availability in regulating behavioral state.Starvation is a condition of extreme nutrient stress that leads to rapid death. On detecting the absence of environmental nutrient sources, organisms use multiple strategies to adjust resource allocation to maximize the chances of finding a food source, including inducing longer foraging searches (1) and limiting sleep behavior (2, 3). Sleep loss in Drosophila melanogaster is a characteristic response to nutrient deprivation that appears ∼12 h after the removal of a food source; in males, it is followed by death in another 12 h (2). Sleep loss is thought to represent a cost to the organism (4–6), and mechanisms for evaluating the environment and terminating this behavioral response when food is available would likely confer an adaptive benefit. A deeper understanding of how organisms perceive and respond to environmental stress could offer substantial benefit to humans attempting to maintain maximal health in the face of food shortages and unstable environmental conditions. The strategies used by organisms to evaluate the sufficiency of a food source and to initiate or suppress sleep loss under very low nutrient conditions remain largely unknown and represent one path toward understanding global stress response.