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Octopamine Mediates Starvation-Induced Hyperactivity in Adult Drosophila

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Octopamine Mediates Starvation-Induced Hyperactivity in Adult Drosophila Octopamine mediates starvation-induced hyperactivity in adult Drosophila Zhe Yang (杨哲)a,1,YueYu(于悦)a,1, Vivian Zhang (张维嘉)b,1, Yinjun Tian (田引军)a,WeiQi(祁伟)a,c, and Liming Wang (王立铭)a,2 aLife Sciences Institute, Zhejiang University, Hangzhou, Zhejiang 310058, China; bDepartment of Molecular and Cell Biology, University of California, Berkeley, CA 94720-3200; and cCollege of Life Sciences, Sichuan University, Chengdu, Sichuan 610064, China Edited* by David J. Anderson, California Institute of Technology, Pasadena, CA, and approved March 10, 2015 (received for review September 16, 2014) Starved animals often exhibit elevated locomotion, which has and if so whether npr-1 and foraging are involved (4). It is worth been speculated to partly resemble foraging behavior and facili- noting that both the roundworm and fruit fly larvae are continuous tate food acquisition and energy intake. Despite its importance, feeders. It is therefore difficult to disassociate the effect of the in- the neural mechanism underlying this behavior remains unknown ternal energy state on foraging behavior from that of acute change in any species. In this study we confirmed and extended previous in food availability. findings that starvation induced locomotor activity in adult fruit In this present study, we sought to characterize foraging be- flies Drosophila melanogaster. We also showed that starvation- havior in an intermittent feeder, the adult fruit fly. We confirmed induced hyperactivity was directed toward the localization and that starved flies exhibited robust and sustained increase in their acquisition of food sources, because it could be suppressed upon locomotor activity and provided evidence that it partly resembled the detection of food cues via both central nutrient-sensing and foraging behavior. Furthermore, we found octopamine, a bio- peripheral sweet-sensing mechanisms, via induction of food inges- logical amine structurally related to vertebrate norepinephrine tion. We further found that octopamine, the insect counterpart with similar physiological roles, both necessary and sufficient for of vertebrate norepinephrine, as well as the neurons expressing starvation-induced hyperactivity. To summarize, our results re- octopamine, were both necessary and sufficient for starvation- veal a highly conserved neural mechanism that promotes loco- induced hyperactivity. Octopamine was not required for starva- motion upon starvation, shedding important light on the regu- tion-induced changes in feeding behaviors, suggesting indepen- lation of foraging behavior by the CNS. dent regulations of energy intake behaviors upon starvation. NEUROSCIENCE Taken together, our results establish a quantitative behavioral Results paradigm to investigate the regulation of energy homeostasis by Starvation Induces Hyperactivity of Adult Flies. We first examined the CNS and identify a conserved neural substrate that links or- the locomotor effect of food deprivation in adult flies. To do so, ganismal metabolic state to a specific behavioral output. we adapted an assay in which fly locomotion was indirectly measured by the flies’ frequency to cross the midline of tubes Drosophila | starvation | foraging | octopamine (Fig. 1A) (12). In the presence of sucrose, wild-type Canton-S flies exhibited a characteristic and relatively stable locomotor he CNS plays an essential role in energy homeostasis (1). It profile (Fig. 1B, dark blue). In contrast, flies showed incremental Tactively monitors changes in the internal energy state and increase in locomotor activity following food deprivation (Fig. modulates an array of physiological and behavioral responses to 1B, light blue and SI Appendix, Fig. S1). For a more quantitative enable energy homeostasis. Foraging behavior is critical for the localization and acquisition of food supply and hence energy Significance homeostasis. It has been extensively documented both in etho- logical settings (2, 3) and under well-controlled laboratory con- The central nervous system monitors reduction in metabolic ditions (4). Laboratory rodents with limited food access exhibit state and promotes feeding and foraging in response. While stereotypic food anticipatory activity (FAA) several hours before feeding behavior has been extensively studied, the regulation the mealtime, which is characterized by a steady increase in lo- of foraging behavior remains largely unknown. In this study, comotion and other appetitive behaviors (5). The neural substrate we show that starvation-induced hyperactivity in adult fruit that drives FAA still remains elusive (5, 6). Notably, the regulation flies resembled foraging activity. We also found that octop- of FAA seems to be dissociable from that of feeding behavior (7, 8). amine, the insect counterpart of vertebrate norepinephrine, These results hint at the presence of an independent and somewhat was crucial for starvation-induced foraging. We further discrete regulatory mechanism of foraging behavior. showed that octopamine was not required for starvation- Foraging behavior has also been extensively studied in in- induced changes in feeding, suggesting independent regula- vertebrate species such as the roundworm Caenorhabditis elegans tions of energy intake behaviors upon starvation. Taken to- (9) and fruit flies Drosophila melanogaster (10). Roundworm gether, our results establish a quantitative foraging assay and populations exhibit two naturally emerged foraging patterns: “ ” “ ” a highly conserved neural substrate that regulates foraging, solitary worms disperse across the bacterial lawn, and social offering an entry point to further dissect the neural circuitry of worms aggregate along the food edge and form clumps (9). This this important behavior. behavioral dimorphism is controlled by natural variations of the npr-1 (neuropeptide receptor resemblance) gene that encodes a Author contributions: Z.Y., Y.Y., V.Z., and L.W. designed research; Z.Y., Y.Y., V.Z., Y.T., receptor homologous to the receptor family of orexigenic neuro- W.Q., and L.W. performed research; Z.Y., Y.Y., V.Z., Y.T., W.Q., and L.W. analyzed data; peptide Y in mammals (9). A comparable scenario has also been and L.W. wrote the paper. identified in larval fruit flies (10), with two distinct forms of for- The authors declare no conflict of interest. aging present in nature: “rover” and “sitter.” On food sources, *This Direct Submission article had a prearranged editor. sitter but not rover reduces moving speed for feeding (11). Natural Freely available online through the PNAS open access option. variations of a single gene named foraging that encodes a cGMP- 1Z.Y., Y.Y., and V.Z. contributed equally to this work. dependent protein kinase are responsible for this behavioral di- 2To whom correspondence should be addressed. Email: [email protected]. morphism (10). It remains unclear, however, whether the foraging This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. strategies outlined above are driven by animals’ metabolic state, 1073/pnas.1417838112/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1417838112 PNAS | April 21, 2015 | vol. 112 | no. 16 | 5219–5224 Downloaded by guest on September 29, 2021 latter seemed unlikely because food deprivation did not induce AB Night 0 Day 1 Night 1 Day 2 Night 2 Day 3 Night 3 120 Light cycle hyperactivity immediately (Fig. 1B, night 0 and SI Appendix, Fig. +Sucrose 100 -Sucrose S1). To further distinguish between these two alternatives, we Stopper Fly Medium 80 assayed flies on different sucrose concentrations (Fig. 1 G and 60 H). We found that flies showed comparable locomotor activity 2.5 C **** 40 on sucrose mediums that could support their survival, but hy- 2.0 Crossings per 30 min 20 peractivity on media that could not support survival (Fig. 1 G 1.5 0 and H, 5.0, 1.0, and 0.5% sucrose vs. 0.1 and 0% sucrose). No- 1.0 B’ 100 0.5 tably, all these sucrose concentrations fall within the dynamic (%) Daily crossings (x1,000) 0.0 Survival range of the sweet-sensing gustatory neurons of fruit flies (18), +Sucrose -Sucrose 0 and hence can likely be discriminated by flies. Taken together, DE F these results suggest that hyperactivity induced by food depri- 2 *** * ** *** * NS * ** ** ** * NS +Sucrose -Sucrose vation is more likely a starvation response than a gustatory re- 1 sponse (see next section). +Sucrose -Sucrose Velocity (mm/s) Velocity 0 1 2 3 4 5 6 0 Food Cues Suppress Starvation-Induced Hyperactivity. Starvation- Cumulative time (min) 10 20 30 40 50 60 70 80 90 100 110 120 Recording time (min) induced hyperactivity of adult flies has been thought to resemble 120 Light cycle G 5.0% Sucrose foraging behavior in laboratory conditions (13–16). However, it 100 1.0% Sucrose 0.5% Sucrose 0.1% Sucrose can also be a nonforaging response, e.g., a stressful response to 80 0% Sucrose H **** 2.5 starvation. We therefore asked whether starvation-induced hy- 60 2.0 peractivity could be suppressed and even reversed upon the de- 40 1.5 tection of food cues, which distinguished these two possibilities. Crossings per 30 min 20 1.0 Animals are able to evaluate food quality based on both the 0 0.5 100 Daily crossings (x1,000) nutrient content and the palatability (e.g., sweetness) (19). We G’ 0.0 5.0% 1.0% 0.5% 0.1% 0% (%) Sucrose concentration first asked whether starvation-induced hyperactivity could be Survival 0 suppressed by nutrient supply in the absence of sweet taste. Fig. 1. Starvation induces hyperactivity of adult flies. (A) Locomotion assay. Sorbitol is a nutritious
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