Visualizing Neuromodulation In Vivo: TANGO-Mapping of Dopamine Signaling Reveals Appetite Control of Sugar Sensing

Inagaki, Hidehiko K.; De-Leon, Shlomo Ben-Tabou; Wong, Allan; Jagadish, S.; Ishimoto, Hiroshi; Barnea, Gilad; Kitamoto, Toshihiro; Anderson, David J.

doi:10.1016/j.cell.2012.02.027

Cited by 52 publications

(93 citation statements)

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“…In fruit flies, it has been shown that starvation increases the likelihood of proboscis extension reflex (PER) to sucrose, a behavioral component of feeding initiation (39). We found that TβH M18 mutant flies showed comparable PER responses to Canton-S controls under both fed and starved conditions (Fig.…”

Section: Octopamine Is Not Required For Starvation-induced Changes Inmentioning

confidence: 55%

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Octopamine mediates starvation-induced hyperactivity in adult Drosophila

Yang

Zhang

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

171

180

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Starved animals often exhibit elevated locomotion, which has been speculated to partly resemble foraging behavior and facilitate food acquisition and energy intake. Despite its importance, the neural mechanism underlying this behavior remains unknown in any species. In this study we confirmed and extended previous findings that starvation induced locomotor activity in adult fruit flies Drosophila melanogaster. We also showed that starvationinduced hyperactivity was directed toward the localization and acquisition of food sources, because it could be suppressed upon the detection of food cues via both central nutrient-sensing and peripheral sweet-sensing mechanisms, via induction of food ingestion. We further found that octopamine, the insect counterpart of vertebrate norepinephrine, as well as the neurons expressing octopamine, were both necessary and sufficient for starvationinduced hyperactivity. Octopamine was not required for starvation-induced changes in feeding behaviors, suggesting independent regulations of energy intake behaviors upon starvation. Taken together, our results establish a quantitative behavioral paradigm to investigate the regulation of energy homeostasis by the CNS and identify a conserved neural substrate that links organismal metabolic state to a specific behavioral output.T he CNS plays an essential role in energy homeostasis (1). It actively monitors changes in the internal energy state and modulates an array of physiological and behavioral responses to enable energy homeostasis. Foraging behavior is critical for the localization and acquisition of food supply and hence energy homeostasis. It has been extensively documented both in ethological settings (2, 3) and under well-controlled laboratory conditions (4). Laboratory rodents with limited food access exhibit stereotypic food anticipatory activity (FAA) several hours before the mealtime, which is characterized by a steady increase in locomotion and other appetitive behaviors (5). The neural substrate that drives FAA still remains elusive (5, 6). Notably, the regulation of FAA seems to be dissociable from that of feeding behavior (7,8). These results hint at the presence of an independent and somewhat discrete regulatory mechanism of foraging behavior.Foraging behavior has also been extensively studied in invertebrate species such as the roundworm Caenorhabditis elegans (9) and fruit flies Drosophila melanogaster (10). Roundworm populations exhibit two naturally emerged foraging patterns: "solitary" worms disperse across the bacterial lawn, and "social" worms aggregate along the food edge and form clumps (9). This behavioral dimorphism is controlled by natural variations of the npr-1 (neuropeptide receptor resemblance) gene that encodes a receptor homologous to the receptor family of orexigenic neuropeptide Y in mammals (9). A comparable scenario has also been identified in larval fruit flies (10), with two distinct forms of foraging present in nature: "rover" and "sitter." On food sources, sitter but not rover reduces moving speed ...

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Section: Octopamine Is Not Required For Starvation-induced Changes Inmentioning

confidence: 55%

“…PER. PER was assayed as described previously (39). Briefly, sucrose-fed and starved flies were gently aspirated and mounted into Pipetman tips (200 μL).…”

Section: Methodsmentioning

confidence: 99%

Octopamine mediates starvation-induced hyperactivity in adult Drosophila

Yang

Zhang

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

171

180

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“…The neural transmission of the gustatory receptor neurons that sense amino acids might be enhanced (Inagaki et al, 2012). Because the taste sensitivity to amino acids specifically increases, an alternative possibility is that deprivation induces expression of a gene or genes encoding a putative taste receptor for amino acids.…”

Section: Discussionmentioning

confidence: 99%

Taste preference for amino acids is dependent on internal nutritional state inDrosophila melanogaster

Toshima

Tanimura

2012

Journal of Experimental Biology

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SUMMARYLike mammals, insects need to ingest proteins from foods because they cannot synthesise several amino acids. Amino acids are also essential nutrients for Drosophila melanogaster, especially for female egg production, but how flies detect amino acids and how the feeding response to amino acids is regulated are unknown. In this study, the two-choice preference test, the proboscis extension reflex test and a CAFE assay were performed to explore the ability of D. melanogaster to detect and discriminate amino acids. To determine whether D. melanogaster change their feeding preference to amino acids after being deprived of them, as previously reported in the locust, two groups of flies raised on the usual medium or on glucose medium were compared. Aminoacid-deprived flies demonstrated enhanced preference to an amino acid mixture and to several amino acids. These flies ingested amino acids even when they were replete with glucose. The proboscis extension reflex to particular amino acids was induced only in amino-acid-deprived flies. Our findings indicate that the sensitivity of labellar taste cells to amino acids may change when flies are deficient in amino acid supply, and also reveal that the detection pathways for individual amino acids may differ. We suggest the existence of an amino acid receptor and a monitoring system regulating the feeding responses to amino acids. Supplementary material available online at

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“…Preference for caloric sugars is potentiated by starvation Starvation is known to enhance feeding behaviors and taste sensitivity in flies (Barton Browne, 1975;Scheiner et al, 2004;Farhadian et al, 2012;Hergarden et al, 2012;Inagaki et al, 2012). To test the effects of starvation on preference for caloric sugars, we fooddeprived flies for 8 or 24 h and measured their preference for the mixture of 20% sucrose and 80% mannose versus L-fucose.…”

Section: Flies Shift Feeding Preference Toward Caloric Sugarsmentioning

confidence: 99%

Integration of Taste and Calorie Sensing inDrosophila

et al. 2012

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Animals use gustatory information to assess the suitability of potential food sources and make critical decisions on what to consume. For example, the taste of sugar generally signals a potent dietary source of carbohydrates. However, the intensity of the sensory response to a particular sugar, or "sweetness," is not always a faithful reporter of its nutritional value, and recent evidence suggests that animals can sense the caloric content of food independently of taste. Here, we demonstrate that the vinegar fly Drosophila melanogaster uses both taste and calorie sensing to determine feeding choices, and that the relative contribution of each changes over time. Using the capillary feeder assay, we allowed flies to choose between sources of sugars that varied in their ratio of sweetness to caloric value. We found that flies initially consume sugars according to taste. However, over several hours their preference shifts toward the food source with higher caloric content. This behavioral shift occurs more rapidly following food deprivation and is modulated by cAMP and insulin signaling within neurons. Our results are consistent with the existence of a taste-independent calorie sensor in flies, and suggest that calorie-based reward modifies long-term feeding preferences.

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Visualizing Neuromodulation In Vivo: TANGO-Mapping of Dopamine Signaling Reveals Appetite Control of Sugar Sensing

Cited by 52 publications

References 0 publications

Octopamine mediates starvation-induced hyperactivity in adult Drosophila

Octopamine mediates starvation-induced hyperactivity in adult Drosophila

Taste preference for amino acids is dependent on internal nutritional state inDrosophila melanogaster

Integration of Taste and Calorie Sensing inDrosophila

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