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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.


Related in: MedlinePlus

Regulation of amino acid preference. (A) When locusts are kept on a balanced diet the sensitivity of amino acid responsive GRNs in the maxillary palps is moderate. (B) Upon amino acid deprivation hemolymph amino acid concentration and osmolality are decreased. This leads to an increase in the sensitivity of amino acid responsive GRNs followed by an increase in food consumption. (C) In Drosophila kept on a balanced diet ppk+ neurons are active, causing flies to prefer sucrose. (D) When flies are deprived of amino acids, it is conceivable that, TOR/S6K signaling in neurons is altered presumably indicating an internal amino acid deficiency and serotonin levels in the brain are thought to increase. Furthermore, upon mating Sex Peptide, as well as other ligands of the Sex Peptide receptor, are transferred to the uterus causing the inhibition of the ppk+ neurons which project to the Ventral Nerve Cord (VNC) and the brain. These changes lead to an increase in yeast (amino acid rich food) preference.
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Figure 4: Regulation of amino acid preference. (A) When locusts are kept on a balanced diet the sensitivity of amino acid responsive GRNs in the maxillary palps is moderate. (B) Upon amino acid deprivation hemolymph amino acid concentration and osmolality are decreased. This leads to an increase in the sensitivity of amino acid responsive GRNs followed by an increase in food consumption. (C) In Drosophila kept on a balanced diet ppk+ neurons are active, causing flies to prefer sucrose. (D) When flies are deprived of amino acids, it is conceivable that, TOR/S6K signaling in neurons is altered presumably indicating an internal amino acid deficiency and serotonin levels in the brain are thought to increase. Furthermore, upon mating Sex Peptide, as well as other ligands of the Sex Peptide receptor, are transferred to the uterus causing the inhibition of the ppk+ neurons which project to the Ventral Nerve Cord (VNC) and the brain. These changes lead to an increase in yeast (amino acid rich food) preference.

Mentions: Interestingly, in locusts the sensitivity of maxillary palp GRNs (Figures 4A,B) is correlated with the increase in food intake seen in response to the low protein diet: the sensitivity of the GRNs to leucine and a mixture of 10 amino acids increased, with no apparent change in the sensitivity to sucrose (Abisgold and Simpson, 1988). Importantly, injection of amino acids into the hemolymph reversed the change in receptor sensitivity to pre-deprivation levels (Abisgold and Simpson, 1988). The effects on the sensitivity of GRNs were not mediated by a top-down effect from the central nervous system, since transection of the maxillary nerve did not affect the changes in sensitivity, which could be reversed by injection of amino acids directly in to the isolated maxillary palp (Simpson and Simpson, 1992). In locusts the current hypothesis is that the amino acid sensor is likely to be located in the GRNs themselves, and that the increased consumption of proteins is largely determined by elevated sensitivity of GRNs to amino acids. This stands in contrast to vertebrates, where protein homeostasis is thought to rely on amino acid sensing in the brain (Hao et al., 2005; Maurin et al., 2005; Gietzen et al., 2007). Following these discoveries, further research suggested that protein intake is tightly regulated on a behavioral level in many different species (Raubenheimer and Simpson, 1997), leading to the development of a unifying methodological and theoretical framework which was termed “nutritional geometry” (Raubenheimer and Simpson, 1993; Lee, 2006).


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)

Regulation of amino acid preference. (A) When locusts are kept on a balanced diet the sensitivity of amino acid responsive GRNs in the maxillary palps is moderate. (B) Upon amino acid deprivation hemolymph amino acid concentration and osmolality are decreased. This leads to an increase in the sensitivity of amino acid responsive GRNs followed by an increase in food consumption. (C) In Drosophila kept on a balanced diet ppk+ neurons are active, causing flies to prefer sucrose. (D) When flies are deprived of amino acids, it is conceivable that, TOR/S6K signaling in neurons is altered presumably indicating an internal amino acid deficiency and serotonin levels in the brain are thought to increase. Furthermore, upon mating Sex Peptide, as well as other ligands of the Sex Peptide receptor, are transferred to the uterus causing the inhibition of the ppk+ neurons which project to the Ventral Nerve Cord (VNC) and the brain. These changes lead to an increase in yeast (amino acid rich food) preference.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 4: Regulation of amino acid preference. (A) When locusts are kept on a balanced diet the sensitivity of amino acid responsive GRNs in the maxillary palps is moderate. (B) Upon amino acid deprivation hemolymph amino acid concentration and osmolality are decreased. This leads to an increase in the sensitivity of amino acid responsive GRNs followed by an increase in food consumption. (C) In Drosophila kept on a balanced diet ppk+ neurons are active, causing flies to prefer sucrose. (D) When flies are deprived of amino acids, it is conceivable that, TOR/S6K signaling in neurons is altered presumably indicating an internal amino acid deficiency and serotonin levels in the brain are thought to increase. Furthermore, upon mating Sex Peptide, as well as other ligands of the Sex Peptide receptor, are transferred to the uterus causing the inhibition of the ppk+ neurons which project to the Ventral Nerve Cord (VNC) and the brain. These changes lead to an increase in yeast (amino acid rich food) preference.
Mentions: Interestingly, in locusts the sensitivity of maxillary palp GRNs (Figures 4A,B) is correlated with the increase in food intake seen in response to the low protein diet: the sensitivity of the GRNs to leucine and a mixture of 10 amino acids increased, with no apparent change in the sensitivity to sucrose (Abisgold and Simpson, 1988). Importantly, injection of amino acids into the hemolymph reversed the change in receptor sensitivity to pre-deprivation levels (Abisgold and Simpson, 1988). The effects on the sensitivity of GRNs were not mediated by a top-down effect from the central nervous system, since transection of the maxillary nerve did not affect the changes in sensitivity, which could be reversed by injection of amino acids directly in to the isolated maxillary palp (Simpson and Simpson, 1992). In locusts the current hypothesis is that the amino acid sensor is likely to be located in the GRNs themselves, and that the increased consumption of proteins is largely determined by elevated sensitivity of GRNs to amino acids. This stands in contrast to vertebrates, where protein homeostasis is thought to rely on amino acid sensing in the brain (Hao et al., 2005; Maurin et al., 2005; Gietzen et al., 2007). Following these discoveries, further research suggested that protein intake is tightly regulated on a behavioral level in many different species (Raubenheimer and Simpson, 1997), leading to the development of a unifying methodological and theoretical framework which was termed “nutritional geometry” (Raubenheimer and Simpson, 1993; Lee, 2006).

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.


Related in: MedlinePlus