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The dilemmas of the gourmet fly: the molecular and neuronal mechanisms of feeding and nutrient decision making in Drosophila.

Itskov PM, Ribeiro C - Front Neurosci (2013)

Bottom Line: To survive and successfully reproduce animals need to maintain a balanced intake of nutrients and energy.This review discusses methodologies developed in order to study insect feeding, the effects of neuropeptides and neuromodulators on feeding behavior, behavioral evidence supporting the existence of internal energy sensors, neuronal and molecular mechanisms controlling protein intake, and finally the regulation of feeding by circadian rhythms and sleep.From the discussed data a conceptual framework starts to emerge which aims to explain the molecular and neuronal processes maintaining the stability of the internal milieu.

View Article: PubMed Central - PubMed

Affiliation: Behaviour and Metabolism Laboratory, Champalimaud Neuroscience Programme, Champalimaud Centre for the Unknown Lisbon, Portugal.

ABSTRACT
To survive and successfully reproduce animals need to maintain a balanced intake of nutrients and energy. The nervous system of insects has evolved multiple mechanisms to regulate feeding behavior. When animals are faced with the choice to feed, several decisions must be made: whether or not to eat, how much to eat, what to eat, and when to eat. Using Drosophila melanogaster substantial progress has been achieved in understanding the neuronal and molecular mechanisms controlling feeding decisions. These feeding decisions are implemented in the nervous system on multiple levels, from alterations in the sensitivity of peripheral sensory organs to the modulation of memory systems. This review discusses methodologies developed in order to study insect feeding, the effects of neuropeptides and neuromodulators on feeding behavior, behavioral evidence supporting the existence of internal energy sensors, neuronal and molecular mechanisms controlling protein intake, and finally the regulation of feeding by circadian rhythms and sleep. From the discussed data a conceptual framework starts to emerge which aims to explain the molecular and neuronal processes maintaining the stability of the internal milieu.

No MeSH data available.


Effects of starvation on olfactory processing in Drosophila. (A) In satiated animals, innate responses to food odors, which are probably mediated by the lateral horn (LH) are weak. A subpopulation of dopaminergic neurons (MB-MP DNs) projecting to the mushroom body (MB) suppresses the output of the mushroom body via tonic release of dopamine. While these neurons are active, retrieval of appetitive conditioned responses to odors does not occur. (B) In starved animals, the inhibition of Insulin-like receptor (InR) signaling in the olfactory receptor neurons (ORNs) stimulates the synthesis and incorporation of Short Neuropeptide F Receptor type 1 (sNPFR1) into the membrane of these neurons. sNPFR1 mediates presynaptic facilitation of the ORN response to odors, increasing the activity of projection neurons (PNs), and enhancing the innate response to attractive food odors, presumably mediated by the lateral horn neurons as well as conditioned responses to odors by the mushroom body neurons. At the same time the decrease in the hemolymph concentration of glucose and trehalose is detected by an internal energy sensor (which may or may not be directly connected to NPF neurons) which in turn activates Neuropeptide F expressing neurons. Activation of the NPF receptor 1 leads to the inhibition of MB-MP dopaminergic neurons and thus the release of the output of the mushroom body from tonic dopaminergic inhibition, allowing the retrieval of conditioned appetitive responses.
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Figure 3: Effects of starvation on olfactory processing in Drosophila. (A) In satiated animals, innate responses to food odors, which are probably mediated by the lateral horn (LH) are weak. A subpopulation of dopaminergic neurons (MB-MP DNs) projecting to the mushroom body (MB) suppresses the output of the mushroom body via tonic release of dopamine. While these neurons are active, retrieval of appetitive conditioned responses to odors does not occur. (B) In starved animals, the inhibition of Insulin-like receptor (InR) signaling in the olfactory receptor neurons (ORNs) stimulates the synthesis and incorporation of Short Neuropeptide F Receptor type 1 (sNPFR1) into the membrane of these neurons. sNPFR1 mediates presynaptic facilitation of the ORN response to odors, increasing the activity of projection neurons (PNs), and enhancing the innate response to attractive food odors, presumably mediated by the lateral horn neurons as well as conditioned responses to odors by the mushroom body neurons. At the same time the decrease in the hemolymph concentration of glucose and trehalose is detected by an internal energy sensor (which may or may not be directly connected to NPF neurons) which in turn activates Neuropeptide F expressing neurons. Activation of the NPF receptor 1 leads to the inhibition of MB-MP dopaminergic neurons and thus the release of the output of the mushroom body from tonic dopaminergic inhibition, allowing the retrieval of conditioned appetitive responses.

Mentions: Neuropeptide F, is an ortholog of mammalian Neuropeptide Y and shares its involvement in the regulation of food intake (Tatemoto et al., 1982; Wu et al., 2005a,b; Krashes et al., 2009; Nässel and Wegener, 2011). NPF should not be confused with short Neuropeptide F, which performs different functions and which we will discuss separately (Nässel and Wegener, 2011). In Drosophila larvae, NPF receptor 1 (NPFR1) activation promotes feeding on noxious food as well as solid (unattractive) food, mimicking the effect of starvation (Wu et al., 2005a,b). These effects are partially mediated by the suppression of the RPS6-p70-protein kinase (S6K) and by Insulin-like receptor (InR) signaling in NPFR1 neurons. In the neurosecretory neurons that produce ILP (Insulin-like peptide), the same S6K cascade affects the intake of both liquid and solid food and is mediated by changes in the release of ILP2 and ILP4 (Wu et al., 2005a). NPF has also been shown to be necessary for the recall of olfactory appetitive memory in adult flies through action on so called MB-MP dopaminergic neurons, which send their efferents to the mushroom body (Krashes et al., 2009). In satiated animals, the NPF neurons are silent and the output of the mushroom body is inhibited by the MB-MP neurons (Figure 3A). In starved animals NPF neurons are activated, leading to inhibition of the dopaminergic MB-MP neurons. The opening of the inhibitory gate from the MBs allows for the recall of the appetitive conditioned responses to odors and subsequent attraction toward presumptive appetitive food sources (Figure 3B).


The dilemmas of the gourmet fly: the molecular and neuronal mechanisms of feeding and nutrient decision making in Drosophila.

Itskov PM, Ribeiro C - Front Neurosci (2013)

Effects of starvation on olfactory processing in Drosophila. (A) In satiated animals, innate responses to food odors, which are probably mediated by the lateral horn (LH) are weak. A subpopulation of dopaminergic neurons (MB-MP DNs) projecting to the mushroom body (MB) suppresses the output of the mushroom body via tonic release of dopamine. While these neurons are active, retrieval of appetitive conditioned responses to odors does not occur. (B) In starved animals, the inhibition of Insulin-like receptor (InR) signaling in the olfactory receptor neurons (ORNs) stimulates the synthesis and incorporation of Short Neuropeptide F Receptor type 1 (sNPFR1) into the membrane of these neurons. sNPFR1 mediates presynaptic facilitation of the ORN response to odors, increasing the activity of projection neurons (PNs), and enhancing the innate response to attractive food odors, presumably mediated by the lateral horn neurons as well as conditioned responses to odors by the mushroom body neurons. At the same time the decrease in the hemolymph concentration of glucose and trehalose is detected by an internal energy sensor (which may or may not be directly connected to NPF neurons) which in turn activates Neuropeptide F expressing neurons. Activation of the NPF receptor 1 leads to the inhibition of MB-MP dopaminergic neurons and thus the release of the output of the mushroom body from tonic dopaminergic inhibition, allowing the retrieval of conditioned appetitive responses.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3569668&req=5

Figure 3: Effects of starvation on olfactory processing in Drosophila. (A) In satiated animals, innate responses to food odors, which are probably mediated by the lateral horn (LH) are weak. A subpopulation of dopaminergic neurons (MB-MP DNs) projecting to the mushroom body (MB) suppresses the output of the mushroom body via tonic release of dopamine. While these neurons are active, retrieval of appetitive conditioned responses to odors does not occur. (B) In starved animals, the inhibition of Insulin-like receptor (InR) signaling in the olfactory receptor neurons (ORNs) stimulates the synthesis and incorporation of Short Neuropeptide F Receptor type 1 (sNPFR1) into the membrane of these neurons. sNPFR1 mediates presynaptic facilitation of the ORN response to odors, increasing the activity of projection neurons (PNs), and enhancing the innate response to attractive food odors, presumably mediated by the lateral horn neurons as well as conditioned responses to odors by the mushroom body neurons. At the same time the decrease in the hemolymph concentration of glucose and trehalose is detected by an internal energy sensor (which may or may not be directly connected to NPF neurons) which in turn activates Neuropeptide F expressing neurons. Activation of the NPF receptor 1 leads to the inhibition of MB-MP dopaminergic neurons and thus the release of the output of the mushroom body from tonic dopaminergic inhibition, allowing the retrieval of conditioned appetitive responses.
Mentions: Neuropeptide F, is an ortholog of mammalian Neuropeptide Y and shares its involvement in the regulation of food intake (Tatemoto et al., 1982; Wu et al., 2005a,b; Krashes et al., 2009; Nässel and Wegener, 2011). NPF should not be confused with short Neuropeptide F, which performs different functions and which we will discuss separately (Nässel and Wegener, 2011). In Drosophila larvae, NPF receptor 1 (NPFR1) activation promotes feeding on noxious food as well as solid (unattractive) food, mimicking the effect of starvation (Wu et al., 2005a,b). These effects are partially mediated by the suppression of the RPS6-p70-protein kinase (S6K) and by Insulin-like receptor (InR) signaling in NPFR1 neurons. In the neurosecretory neurons that produce ILP (Insulin-like peptide), the same S6K cascade affects the intake of both liquid and solid food and is mediated by changes in the release of ILP2 and ILP4 (Wu et al., 2005a). NPF has also been shown to be necessary for the recall of olfactory appetitive memory in adult flies through action on so called MB-MP dopaminergic neurons, which send their efferents to the mushroom body (Krashes et al., 2009). In satiated animals, the NPF neurons are silent and the output of the mushroom body is inhibited by the MB-MP neurons (Figure 3A). In starved animals NPF neurons are activated, leading to inhibition of the dopaminergic MB-MP neurons. The opening of the inhibitory gate from the MBs allows for the recall of the appetitive conditioned responses to odors and subsequent attraction toward presumptive appetitive food sources (Figure 3B).

Bottom Line: To survive and successfully reproduce animals need to maintain a balanced intake of nutrients and energy.This review discusses methodologies developed in order to study insect feeding, the effects of neuropeptides and neuromodulators on feeding behavior, behavioral evidence supporting the existence of internal energy sensors, neuronal and molecular mechanisms controlling protein intake, and finally the regulation of feeding by circadian rhythms and sleep.From the discussed data a conceptual framework starts to emerge which aims to explain the molecular and neuronal processes maintaining the stability of the internal milieu.

View Article: PubMed Central - PubMed

Affiliation: Behaviour and Metabolism Laboratory, Champalimaud Neuroscience Programme, Champalimaud Centre for the Unknown Lisbon, Portugal.

ABSTRACT
To survive and successfully reproduce animals need to maintain a balanced intake of nutrients and energy. The nervous system of insects has evolved multiple mechanisms to regulate feeding behavior. When animals are faced with the choice to feed, several decisions must be made: whether or not to eat, how much to eat, what to eat, and when to eat. Using Drosophila melanogaster substantial progress has been achieved in understanding the neuronal and molecular mechanisms controlling feeding decisions. These feeding decisions are implemented in the nervous system on multiple levels, from alterations in the sensitivity of peripheral sensory organs to the modulation of memory systems. This review discusses methodologies developed in order to study insect feeding, the effects of neuropeptides and neuromodulators on feeding behavior, behavioral evidence supporting the existence of internal energy sensors, neuronal and molecular mechanisms controlling protein intake, and finally the regulation of feeding by circadian rhythms and sleep. From the discussed data a conceptual framework starts to emerge which aims to explain the molecular and neuronal processes maintaining the stability of the internal milieu.

No MeSH data available.