Integration of Taste and Calorie Sensing in<i>Drosophila</i>

Stafford, Jeffrey W; Lynd, Kaylea M; Jung, Aera Y; Gordon, Michael D.

doi:10.1523/jneurosci.1887-12.2012

Cited by 92 publications

(108 citation statements)

References 62 publications

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“…4B). The data confirm that starvation induces a feeding preference toward a nutritious food source (19). TβH M18 mutant flies exhibited comparable responses as Canton-S flies under both fed and starved conditions (Fig.…”

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

confidence: 74%

“…Animals are able to evaluate food quality based on both the nutrient content and the palatability (e.g., sweetness) (19). We first asked whether starvation-induced hyperactivity could be suppressed by nutrient supply in the absence of sweet taste.…”

Section: Significancementioning

confidence: 99%

“…S3 and S4), suggesting that nutrient supply alone is sufficient to suppress starvation-induced hyperactivity. Taste-independent nutrientsensing mechanisms have been reported in fruit flies (19,22). Specifically, a recent report has shown that SLC5A11, a brainspecific sodium/solute cotransporter, mediates the evaluation of nutrient content by the CNS (23).…”

Section: Significancementioning

confidence: 99%

“…Fruit flies use both nutrient-and taste-sensing mechanisms to evaluate and choose among potential food sources (19,22); and whereas fed flies mostly choose food sources based on sweetness, the preference of starved flies shifts toward nutritious food (19). We developed a simple and quantitative feeding preference assay, in which a group of flies was allowed to choose between two food sources containing either D-glucose or L-glucose (Fig.…”

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

confidence: 99%

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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 Insupporting

confidence: 74%

Section: Significancementioning

confidence: 99%

Section: Significancementioning

confidence: 99%

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

confidence: 99%

See 2 more Smart Citations

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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“…Similar temporal transitions have been found in feeding choice (58), where flies initially choose sugars according to sweet taste, but later prioritize caloric contents. Similarly, ethanol exposure initially acts as an aversive reinforcer, but eventually turns into reward and induces LTM (51).…”

Section: Discussionsupporting

confidence: 60%

Distinct dopamine neurons mediate reward signals for short- and long-term memories

Yamagata

Ichinose

Aso

et al. 2014

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

238

287

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Drosophila melanogaster can acquire a stable appetitive olfactory memory when the presentation of a sugar reward and an odor are paired. However, the neuronal mechanisms by which a single training induces long-term memory are poorly understood. Here we show that two distinct subsets of dopamine neurons in the fly brain signal reward for short-term (STM) and long-term memories (LTM). One subset induces memory that decays within several hours, whereas the other induces memory that gradually develops after training. They convey reward signals to spatially segregated synaptic domains of the mushroom body (MB), a potential site for convergence. Furthermore, we identified a single type of dopamine neuron that conveys the reward signal to restricted subdomains of the mushroom body lobes and induces long-term memory. Constant appetitive memory retention after a single training session thus comprises two memory components triggered by distinct dopamine neurons.dopamine | learning and memory | Drosophila | mushroom body M emory of a momentous event persists for a long time.Whereas some forms of long-term memory (LTM) require repetitive training (1-3), a highly relevant stimulus such as food or poison is sufficient to induce LTM in a single training session (4-7). Recent studies have revealed aspects of the molecular and cellular mechanisms of LTM formation induced by repetitive training (8-11), but how a single training induces a stable LTM is poorly understood (12).Appetitive olfactory learning in fruit flies is suited to address the question, as a presentation of a sugar reward paired with odor induces robust short-term memory (STM) and LTM (6, 7). Odor is represented by a sparse ensemble of the 2,000 intrinsic neurons, the Kenyon cells (13). A current working model suggests that concomitant reward signals from sugar ingestion cause associative plasticity in Kenyon cells that might underlie memory formation (14-20). A single activation session of a specific cluster of dopamine neurons (PAM neurons) by sugar ingestion can induce appetitive memory that is stable over 24 h (19), underscoring the importance of sugar reward to the fly.The mushroom body (MB) is composed of the three different cell types, α/β, α′/β′, and γ, which have distinct roles in different phases of appetitive memories (11,(21)(22)(23)(24)(25). Similar to midbrain dopamine neurons in mammals (26,27), the structure and function of PAM cluster neurons are heterogeneous, and distinct dopamine neurons intersect unique segments of the MB lobes (19,(28)(29)(30)(31)(32)(33)(34). Further circuit dissection is thus crucial to identify candidate synapses that undergo associative modulation.By activating distinct subsets of PAM neurons for reward signaling, we found that short-and long-term memories are independently formed by two complementary subsets of PAM cluster dopamine neurons. Conditioning flies with nutritious and nonnutritious sugars revealed that the two subsets could represent different reinforcing properties: sweet taste and nutritional value of sugar....

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Food selection in larval fruit flies: dynamics and effects on larval development

Schwarz

Durisko

Dukas

2013

Naturwissenschaften

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Selecting food items and attaining a nutritionally balanced diet is an important challenge for all animals including humans. We aimed to establish fruit fly larvae (Drosophila melanogaster) as a simple yet powerful model system for examining the mechanisms of specific hunger and diet selection. In two lab experiments with artificial diets, we found that larvae deprived of either sucrose or protein later selectively fed on a diet providing the missing nutrient. When allowed to freely move between two adjacent food patches, larvae surprisingly preferred to settle on one patch containing yeast and ignored the patch providing sucrose. Moreover, when allowed to move freely between three patches, which provided either yeast only, sucrose only or a balanced mixture of yeast and sucrose, the majority of larvae settled on the yeast-plus-sucrose patch and about one third chose to feed on the yeast only food. While protein (yeast) is essential for development, we also quantified larval success on diets with or without sucrose and show that larvae develop faster on diets containing sucrose. Our data suggest that fruit fly larvae can quickly assess major nutrients in food and seek a diet providing a missing nutrient. The larvae, however, probably prefer to quickly dig into a single food substrate for enhanced protection over achieving an optimal diet.

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Integration of Taste and Calorie Sensing inDrosophila

Cited by 92 publications

References 62 publications

Octopamine mediates starvation-induced hyperactivity in adult Drosophila

Octopamine mediates starvation-induced hyperactivity in adult Drosophila

Distinct dopamine neurons mediate reward signals for short- and long-term memories

Food selection in larval fruit flies: dynamics and effects on larval development

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