Neuronal Basis of Innate Olfactory Attraction to Ethanol in Drosophila

Schneider, Andreá; Ruppert, Manuela; Hendrich, Oliver; Giang, Thomas; Ogueta, Maite; Hampel, Stefanie; Vollbach, Marvin; Büschges, Ansgar; Scholz, Henrike

doi:10.1371/journal.pone.0052007

Cited by 51 publications

(113 citation statements)

References 43 publications

(57 reference statements)

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“…The light activation setup is described in [8]. Briefly one odor trap was illuminated with a blue light with a blue LED (465–485 nm; Cree, Germany); a second trap was illuminated with yellow light which was generated by a warm-white LED (Cree, XLAMP, XR_E LED with 2,600 k-3,700K CCT) and a 510-nm blue light filter (HEBO, Aalen, Germany), that takes out all visible wavelengths up to 510-nm.…”

Section: Methodsmentioning

confidence: 99%

“…Immunostaining was performed as described previously [8]. The following antibodies were used: rabbit anti-GFP (1:1000, Life Technologies), chicken anti-GFP (1:1000, Life Technologies), rat anti-5HT (1:100, Millipore), mouse anti-nc82 (1:20, DSHB), Alexa Fluor 488 goat anti-chicken IgG (1:1000, Life Technologies), Alexa Fluor 488 goat anti-rabbit IgG (1:1000, Life Technologies), Cy3 goat anti-rat IgG (1:200, Jackson Immunoresearch), and Alexa Fluor 546 goat anti-mouse IgG (1:500, Life Technologies).…”

Section: Methodsmentioning

confidence: 99%

“…The approach to the ethanol containing food odors requires a reinforcing mechanism that involves the octopaminergic neurotransmitter system [8]. Other factors that might influence the attraction to ethanol are inhibitory mechanisms that alter the execution of the approach and therefore allowing the animal to dynamically adjust their goal oriented behaviors [9].…”

Section: Introductionmentioning

confidence: 99%

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A Single Pair of Serotonergic Neurons Counteracts Serotonergic Inhibition of Ethanol Attraction in Drosophila

Xu¹,

He²,

Kaiser³

et al. 2016

PLoS ONE

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Attraction to ethanol is common in both flies and humans, but the neuromodulatory mechanisms underlying this innate attraction are not well understood. Here, we dissect the function of the key regulator of serotonin signaling—the serotonin transporter–in innate olfactory attraction to ethanol in Drosophila melanogaster. We generated a mutated version of the serotonin transporter that prolongs serotonin signaling in the synaptic cleft and is targeted via the Gal4 system to different sets of serotonergic neurons. We identified four serotonergic neurons that inhibit the olfactory attraction to ethanol and two additional neurons that counteract this inhibition by strengthening olfactory information. Our results reveal that compensation can occur on the circuit level and that serotonin has a bidirectional function in modulating the innate attraction to ethanol. Given the evolutionarily conserved nature of the serotonin transporter and serotonin, the bidirectional serotonergic mechanisms delineate a basic principle for how random behavior is switched into targeted approach behavior.

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Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

A Single Pair of Serotonergic Neurons Counteracts Serotonergic Inhibition of Ethanol Attraction in Drosophila

Xu¹,

He²,

Kaiser³

et al. 2016

PLoS ONE

Self Cite

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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.

101

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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“…It is perhaps not surprising that there is a difference between Drosophila and honey bees in ethanol preference, given their different ecologies. Flies seek out rotting fruit, the presence of which can be detected by ethanol odours, for egg laying [Schneider et al, 2012]. Honey bees may encounter nectars containing alcohol while foraging, but these would be indicative of decomposition.…”

Section: Drug Reward In Invertebrate Animalsmentioning

confidence: 99%

Invertebrate Models in Addiction Research

Søvik

Barron²

2013

Brain Behav Evol

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While drug addiction is a uniquely human problem, most research examining the biological mechanisms of the transition from substance use to addiction is conducted with vertebrate animal models. Many other fields of neuroscience have greatly benefitted from contributions from simple and manipulable invertebrate model systems. However, the potential of invertebrate research has yet to be fully capitalised on in the field of addiction neuroscience. This may be because of the complexity of addiction and the clinical imperative of addiction research. We argue that the homocentric diagnostic criteria of addiction are no more a hindrance to the use of invertebrate models than they are to vertebrate models. We highlight the strengths of the diversity of different invertebrate model systems in terms of neuroanatomy and molecular machinery, and stress that working with a range of different models will aid in understanding addiction and not be a disadvantage. Finally, we discuss the specific advantages of utilising invertebrate animals for addiction research and highlight key areas in which invertebrates are suited for making unique and meaningful contributions to this field.

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Neuronal Basis of Innate Olfactory Attraction to Ethanol in Drosophila

Cited by 51 publications

References 43 publications

A Single Pair of Serotonergic Neurons Counteracts Serotonergic Inhibition of Ethanol Attraction in Drosophila

A Single Pair of Serotonergic Neurons Counteracts Serotonergic Inhibition of Ethanol Attraction in Drosophila

Competing dopamine neurons drive oviposition choice for ethanol in Drosophila

Invertebrate Models in Addiction Research

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