We present a complete hardware and software system for collecting and quantifying continuous measures of feeding behaviors in the fruit fly, Drosophila melanogaster. The FLIC (Fly Liquid-Food Interaction Counter) detects analog electronic signals as brief as 50 µs that occur when a fly makes physical contact with liquid food. Signal characteristics effectively distinguish between different types of behaviors, such as feeding and tasting events. The FLIC system performs as well or better than popular methods for simple assays, and it provides an unprecedented opportunity to study novel components of feeding behavior, such as time-dependent changes in food preference and individual levels of motivation and hunger. Furthermore, FLIC experiments can persist indefinitely without disturbance, and we highlight this ability by establishing a detailed picture of circadian feeding behaviors in the fly. We believe that the FLIC system will work hand-in-hand with modern molecular techniques to facilitate mechanistic studies of feeding behaviors in Drosophila using modern, high-throughput technologies.
Sensory perception modulates aging and physiology across taxa. We found that perception of female sexual pheromones through a specific gustatory receptor expressed in a subset of foreleg neurons in male fruit flies, Drosophila melanogaster, rapidly and reversibly decreases fat stores, reduces resistance to starvation, and limits lifespan together with neurons that express the reward-mediating neuropeptide F. High-throughput RNA-seq experiments revealed a set of molecular processes that were impacted by the activity of the longevity circuit, thereby identifying new candidate cell non-autonomous aging mechanisms. Mating reversed the effects of pheromone perception, suggesting a model where lifespan is modulated through integration of sensory and reward circuits and where healthy aging may be compromised when the expectations defined by sensory perception are discordant with ensuing experience.
Sensory perception modulates lifespan across taxa, presumably due to alterations in physiological homeostasis after central nervous system integration. The coordinating circuitry of this control, however, remains unknown. Here, we used the Drosophila melanogaster gustatory system to dissect one component of sensory regulation of aging. We found that loss of the critical water sensor, pickpocket 28 (ppk28), altered metabolic homeostasis to promote internal lipid and water stores and extended healthy lifespan. Additionally, loss of ppk28 increased neuronal glucagon-like adipokinetic hormone (AKH) signaling, and the AKH receptor was necessary for ppk28 mutant effects. Furthermore, activation of AKH-producing cells alone was sufficient to enhance longevity, suggesting that a perceived lack of water availability triggers a metabolic shift that promotes the production of metabolic water and increases lifespan via AKH signaling. This work provides an example of how discrete gustatory signals recruit nutrient-dependent endocrine systems to coordinate metabolic homeostasis, thereby influencing long-term health and aging.taste | adipokinetic hormone signaling S ensory signaling systems are potent modulators of organismal metabolism and lifespan (1-6) but the mechanisms by which sensory inputs are transduced into relevant physiological outputs remain poorly understood. For even the simplest organisms, an extensive array of sensory stimuli-including chemical, mechanical, thermal, and visual cues-must be properly transduced and integrated to ensure a reliable response to environmental quality. In the nematode Caenorhabditis elegans, sensory neurons alone may accomplish these tasks. They express multiple sensory receptors, which provide simple integrative capabilities to the cell, and they secrete neuropeptides, which can direct cell-nonautonomous responses in peripheral tissues (7). The fruit fly, Drosophila melanogaster, however, is similar to mammals in that sensory neurons are often highly specialized, and elaborate mechanisms of sensory integration and interpretation are performed by specialized processing centers in the central brain (8). Once decoded, sensory signals are presumably relayed to neuroendocrine centers to stimulate appropriate actions in peripheral tissues. Whereas the release of endocrine molecules, including insulinlike peptides, via central nervous system (CNS) control has emerged as a critical regulator of aging across model organisms, the extent to which sensory signals impact such systems, and the underlying neurocircuitry involved, are unknown (9-11).The Drosophila system is a powerful tool for elucidating evolutionarily conserved aspects of neural circuitry that link sensory information to a variety of behavioral and metabolic responses. Although comprised of only ∼100,000 neurons, the fly brain is sufficiently complex to share many aspects of structure and function with humans and mice. This, along with the ability to manipulate neuronal activity in a temporally and spatially controlled manner, ha...
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