A Trophic Role for Serotonin in the Development of a Simple Feeding Circuit

Neckameyer, Wendi S.

doi:10.1159/000304888

Cited by 58 publications

(88 citation statements)

References 135 publications

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“…Similarly, it has been proposed that 5-HT has a critical role in fly development (Colas et al 1999;Sykes and Condron 2005;Willard et al 2006;Schaerlinger et al 2007). In contrast to these results, it has been shown that mutants of aromatic L-amino acid decarboxylase/Dopa decarboxylase (AADC/DDC)-which converts 5-hydroxy-Ltryptophan (5-HTP) to 5-HT (Hodgetts and O'Keefe 2006)-and flies with increased or decreased 5-HT survive beyond third-instar larval stages (Budnik et al 1986;Sykes and Condron 2005;Neckameyer 2010). Moreover, a recent study showed that pale mutants lacking DA synthesis in the nervous system (but not cuticle-forming tissue) survived to adulthood, despite observed deficits in phototaxis, arousal, and avoidance of shock-associated odor (Riemensperger et al 2011).…”

Section: Discussionmentioning

confidence: 99%

Dispensable, Redundant, Complementary, and Cooperative Roles of Dopamine, Octopamine, and Serotonin inDrosophila melanogaster

Chen

Lebestky

et al. 2013

Genetics

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To investigate the regulation of Drosophila melanogaster behavior by biogenic amines, we have exploited the broad requirement of the vesicular monoamine transporter (VMAT) for the vesicular storage and exocytotic release of all monoamine neurotransmitters. We used the Drosophila VMAT (dVMAT) null mutant to globally ablate exocytotic amine release and then restored DVMAT activity in either individual or multiple aminergic systems, using transgenic rescue techniques. We find that larval survival, larval locomotion, and female fertility rely predominantly on octopaminergic circuits with little apparent input from the vesicular release of serotonin or dopamine. In contrast, male courtship and fertility can be rescued by expressing DVMAT in octopaminergic or dopaminergic neurons, suggesting potentially redundant circuits. Rescue of major aspects of adult locomotion and startle behavior required octopamine, but a complementary role was observed for serotonin. Interestingly, adult circadian behavior could not be rescued by expression of DVMAT in a single subtype of aminergic neurons, but required at least two systems, suggesting the possibility of unexpected cooperative interactions. Further experiments using this model will help determine how multiple aminergic systems may contribute to the regulation of other behaviors. Our data also highlight potential differences between behaviors regulated by standard exocytotic release and those regulated by other mechanisms. BOTH invertebrate and mammalian behaviors undergo extensive regulation by monoamine neurotransmitters (reviewed in Joshua et al.

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Section: Discussionmentioning

confidence: 99%

Dispensable, Redundant, Complementary, and Cooperative Roles of Dopamine, Octopamine, and Serotonin inDrosophila melanogaster

Chen

Lebestky

et al. 2013

Genetics

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“…The activity of NE in PVN has been shown to antagonize that of 5-HT, which suppresses intake of carbohydraterich food (44). In Drosophila, 5-HT is also known to suppress feeding response (45). These findings suggest that the homeostatic control of intake of preferred food is likely mediated by a conserved neural network in flies and mammals.…”

Section: Mb01242mentioning

confidence: 99%

Octopamine-mediated circuit mechanism underlying controlled appetite for palatable food in Drosophila

Zhang

Branch

Shen

2013

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

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The easy accessibility of energy-rich palatable food makes it difficult to resist food temptation. Drosophila larvae are surrounded by sugar-rich food most of their lives, raising the question of how these animals modulate food-seeking behaviors in tune with physiological needs. Here we describe a circuit mechanism defined by neurons expressing tdc2-Gal4 (a tyrosine decarboxylase 2 promoter-directed driver) that selectively drives a distinct foraging strategy in food-deprived larvae. Stimulation of this otherwise functionally latent circuit in tdc2-Gal4 neurons was sufficient to induce exuberant feeding of liquid food in fed animals, whereas targeted lesions in a small subset of tdc2-Gal4 neurons in the subesophageal ganglion blocked hunger-driven increases in the feeding response. Furthermore, regulation of feeding rate enhancement by tdc2-Gal4 neurons requires a novel signaling mechanism involving the VEGF2-like receptor, octopamine, and its receptor. Our findings provide fresh insight for the neurobiology and evolution of appetitive motivation. T he adaptive control of foraging decisions is crucial to survival and reproduction and is mediated by complex brain mechanisms. For example, in hungry animals, feeding behaviors can be modulated by diverse neural systems including those responsible for receiving and processing sensory properties and assigning reward and motivational significance of food stimuli (1-3). At present, elucidation of molecular and circuit mechanisms underlying the adaptive control of feeding behavior remains highly challenging.Our previous studies have shown that Drosophila larvae, like mammals, display diverse adaptive foraging strategies in response to appetizing odors or satiety state and food quality (4-6). For example, larvae fed for ad libitum intake tend to prefer soft, liquid sugar media that contain readily ingestible sugar solution but decline solid media in which sugar solution is embedded in gelled agar and is less accessible (5). However, as food deprivation is prolonged, larvae will become increasingly persistent in extracting the sugar solution from solid media (7). We have also shown that an evolutionarily conserved signaling cascade, involving neuropeptide F (NPF, the fly homolog of neuropeptide Y, or NPY) and insulin-like peptides (dILPs), selectively integrates motivational state (hunger) with persistence to pulverize solid food (5, 7).The observation that the conserved NPY-like system selectively promotes food acquisition behaviors that require high energetic cost has led us to postulate that fly larvae may use other conserved neural mechanisms to regulate acquisition of readily accessible palatable food. In this work, we provide evidence which supports this hypothesis. We show that an octopamine (OA)/β-adrenergic-like receptor (Octß3R)-dependent circuit mechanism selectively regulates appetite for soft sugar media. This circuit mechanism seems to involve two subsets of tdc2-Gal4 neurons in the subesophogeal ganglia (SOG). One of them mediates the hunger-driven increase ...

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“…Serotonin also modulates insect feeding behavior. Serotonergic systems inhibit feeding in the locust, the ant, adults of two species of fly, an aphid, a cockroach and larval Drosophila (Dacks et al, 2003;Kaufmann et al, 2004;Falibene et al, 2012;Neckameyer, 2010), although serotonin appears to stimulate feeding by the adult mosquito Aedes triseriatus (Novak and Rowley, 1994). As in vertebrates, serotonergic pathways inhibit appetite and feeding behavior in insects (Gillette, 2006;Halford et al, 2007).…”

Section: Serotonin and Behaviormentioning

confidence: 99%

“…The response of fed larvae to paroxetine resembles that of mammals, and most insects investigated to date, including a locust, an ant, adults of two species of flies, larval Drosophila, an aphid, and a cockroach, in all of which serotonin acts to inhibit appetite and/or feeding (Dacks et al, 2003;Kaufmann et al, 2004;Falibene et al, 2012;Neckameyer, 2010). For example, serotonin triggers a decrease in sucrose consumption by the blowfly Phormia regina, whereas the flesh fly Neobelliera bullata shows reduced feeding, and reduced electrophysiological responses to sensory input from sucrose receptors, following serotonin injection (Dacks et al, 2003;Long and Murdock, 1983).…”

Section: Effects Of Paroxetine On Behaviormentioning

confidence: 99%

“…For example, serotonin triggers a decrease in sucrose consumption by the blowfly Phormia regina, whereas the flesh fly Neobelliera bullata shows reduced feeding, and reduced electrophysiological responses to sensory input from sucrose receptors, following serotonin injection (Dacks et al, 2003;Long and Murdock, 1983). Serotonin depresses feeding, whereas low neuronal serotonin levels increase appetite of Drosophila larvae (Neckameyer, 2010). In contrast, adults of the mosquito Aedes triseriatus respond to depletion of serotonin levels with a decrease in the amount of blood taken during feeding and in numbers of feeding episodes, but with no change in host-seeking behavior, suggesting that serotonin stimulates feeding (Novak and Rowley, 1994).…”

Section: Effects Of Paroxetine On Behaviormentioning

confidence: 99%

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Modulation of appetite and feeding behavior of the larval mosquito Aedes aegypti (L.) by the serotonin-selective reuptake inhibitor paroxetine: shifts between distinct feeding modes and the influence of feeding status.

Kinney

Panting

Clark

2013

Journal of Experimental Biology

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The effects of the serotonin-selective reuptake inhibitor paroxetine (2×10 -5 mol l -1) on behavior of the larval mosquito Aedes aegypti are described. Four discrete behavioral states dominate larval behavior: wriggling, two distinct types of feeding, and quiescence. Feeding behaviors consist of foraging along the bottom of the container (substrate browsing), and stationary filter feeding while suspended from the surface film. Fed larvae respond to paroxetine with increased wriggling, and reductions in both feeding behaviors. In contrast, food-deprived larvae treated with paroxetine show no change in the proportion of time spent wriggling or feeding, but shift from stationary filter feeding to substrate browsing. Thus, actions of paroxetine in fed larvae are consistent with suppression of appetite and stimulation of wriggling, whereas paroxetine causes fooddeprived larvae to switch from one feeding behavior to another. Further analysis of unfed larvae revealed that paroxetine decreased the power stroke frequency during wriggling locomotion, but had no effect on the swimming velocity during either wriggling or substrate browsing. These data suggest that: (1) serotonergic pathways may trigger shifts between distinct behaviors by actions on higher level (brain) integrating centers where behaviors such as feeding and locomotion are coordinated; (2) these centers in fed and fooddeprived larvae respond differently to serotonergic stimulation suggesting sensory feedback from feeding status; and (3) serotonergic pathways also modulate central pattern generators of the nerve cord where the bursts of action potentials originate that drive the rhythmic muscle contractions of wriggling.

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A Trophic Role for Serotonin in the Development of a Simple Feeding Circuit

Cited by 58 publications

References 135 publications

Dispensable, Redundant, Complementary, and Cooperative Roles of Dopamine, Octopamine, and Serotonin inDrosophila melanogaster

Dispensable, Redundant, Complementary, and Cooperative Roles of Dopamine, Octopamine, and Serotonin inDrosophila melanogaster

Octopamine-mediated circuit mechanism underlying controlled appetite for palatable food in Drosophila

Modulation of appetite and feeding behavior of the larval mosquito Aedes aegypti (L.) by the serotonin-selective reuptake inhibitor paroxetine: shifts between distinct feeding modes and the influence of feeding status.

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