Layered reward signalling through octopamine and dopamine in Drosophila

Burke, Christopher; Huetteroth, Wolf; Owald, David; Perisse, Emmanuel; Krashes, Michael J.; Das, Gaurav; Gohl, Daryl M.; Silies, Marion; Certel, Sarah J.; Waddell, Scott

doi:10.1038/nature11614

Cited by 523 publications

(753 citation statements)

References 37 publications

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“…Because both olfaction and taste affect oviposition preference for ethanol, integration of multiple sensory inputs likely plays a role. Because innate olfactory preference for ethanol is octopamine-dependent, and a subset of octopaminergic neurons mediates PAM neuron activation required for appetitive memory, octopamine may play a role in the olfactory response (46,47). Neurons expressing neuropeptide F (NPF) or its receptor may also be involved.…”

Section: Discussionmentioning

confidence: 99%

Competing dopamine neurons drive oviposition choice for ethanol in Drosophila

Azanchi

Kaun

Heberlein

2013

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

100

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The neural circuits that mediate behavioral choice evaluate and integrate information from the environment with internal demands and then initiate a behavioral response. Even circuits that support simple decisions remain poorly understood. In Drosophila melanogaster, oviposition on a substrate containing ethanol enhances fitness; however, little is known about the neural mechanisms mediating this important choice behavior. Here, we characterize the neural modulation of this simple choice and show that distinct subsets of dopaminergic neurons compete to either enhance or inhibit egg-laying preference for ethanol-containing food. Moreover, activity in α′β′ neurons of the mushroom body and a subset of ellipsoid body ring neurons (R2) is required for this choice. We propose a model where competing dopaminergic systems modulate oviposition preference to adjust to changes in natural oviposition substrates.I n nature, rotting fruit is the social hub for the fruit fly Drosophila melanogaster. Flies use fermenting fruit as a food source (1) and a site for oviposition (2). The choice of a suitable oviposition substrate is an ecologically important decision with a direct impact on species fitness. However, other than having a clear preference for fermenting fruit, how females choose oviposition sites in nature is largely unknown.One of the main metabolites of fermentation is ethanol, which is present in ripe fleshy fruits (3). Although ethanol concentrations in the fruit are rather low [≤5% (vol/vol)] (4), plumes containing ethanol vapor can act as long-distance signals to attract flies to rotting fruit (3, 5). When given the choice, female flies prefer to lay their eggs on media containing low concentrations of ethanol (up to 5%) (6), which leads to enhanced fitness of the developing larva and the adult fly.D. melanogaster's resistance to ethanol toxicity may have evolved to allow inhabitation of ethanol-containing environments (7). For example, adult flies allowed to mate on ethanolcontaining media improve mating success and fecundity (8). Although rearing larvae on food containing relatively high ethanol concentrations delays development and decreases survival (9-11), larvae reared on low concentrations of ethanol develop into heavier adults (7,12). This weight increase may be a result of D. melanogaster larvae metabolizing ethanol and using it as a food source (12). Ingestion of ethanol during the larval stage has additional benefits, such as protection from natural parasites such as endoparasitoid wasps (13).Studies on the neural circuits underlying the oviposition program and choice of oviposition substrates have been initiated only recently in D. melanogaster (14, 15). Ethanol is a particularly intriguing stimulus for oviposition preference, because it has, depending on concentration, both beneficial and detrimental effects on developing larvae. In flies, the function of dopaminergic neurons has been implicated in responses to both rewarding and aversive stimuli (16-19), making it a candidate neuromodulator to signa...

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Section: Discussionmentioning

confidence: 99%

Competing dopamine neurons drive oviposition choice for ethanol in Drosophila

Azanchi

Kaun

Heberlein

2013

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

100

View full text Add to dashboard Cite

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“…They lack therefore MBs capable of integrating information across sensory modalities and allowing the extraction of sensory-independent regularities as those underlying concepts. Despite their tight association with elemental forms of memory [16,17,73 -75], reinforcement systems [69,71,76] and attention-like processes [63,64], the fly MBs lack the multi-sensoriality that would be required to encode conceptual rules that are valid across distinct sensory modalities. Admittedly, concepts could be established within a single modality.…”

Section: Neurobiological Insights Into Conceptual Learning In Beesmentioning

confidence: 99%

Conceptual learning by miniature brains

2013

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Concepts act as a cornerstone of human cognition. Humans and non-human primates learn conceptual relationships such as 'same', 'different', 'larger than', 'better than', among others. In all cases, the relationships have to be encoded by the brain independently of the physical nature of objects linked by the relation. Consequently, concepts are associated with high levels of cognitive sophistication and are not expected in an insect brain. Yet, various works have shown that the miniature brain of honeybees rapidly learns conceptual relationships involving visual stimuli. Concepts such as 'same', 'different', 'above/below of' or 'left/right are well mastered by bees. We review here evidence about concept learning in honeybees and discuss both its potential adaptive advantage and its possible neural substrates. The results reviewed here challenge the traditional view attributing supremacy to larger brains when it comes to the elaboration of concepts and have wide implications for understanding how brains can form conceptual relations.

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“…Octopamine plays an important role in the regulation of a variety of fly behaviors, such as sleep (38), learning (44), and aggression (45). It is of interest to investigate whether and how different subsets of octopaminergic neurons modulate different behaviors in flies (45,46).…”

Section: Canton-s +Sucrosementioning

confidence: 99%

Octopamine mediates starvation-induced hyperactivity in adult Drosophila

Yang

Zhang

et al. 2015

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

166

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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Layered reward signalling through octopamine and dopamine in Drosophila

Cited by 523 publications

References 37 publications

Competing dopamine neurons drive oviposition choice for ethanol in Drosophila

Competing dopamine neurons drive oviposition choice for ethanol in Drosophila

Conceptual learning by miniature brains

Octopamine mediates starvation-induced hyperactivity in adult Drosophila

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