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      The Dilemmas of the Gourmet Fly: The Molecular and Neuronal Mechanisms of Feeding and Nutrient Decision Making in Drosophila

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          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.

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          Most cited references108

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          Orexins and orexin receptors: a family of hypothalamic neuropeptides and G protein-coupled receptors that regulate feeding behavior.

          The hypothalamus plays a central role in the integrated control of feeding and energy homeostasis. We have identified two novel neuropeptides, both derived from the same precursor by proteolytic processing, that bind and activate two closely related (previously) orphan G protein-coupled receptors. These peptides, termed orexin-A and -B, have no significant structural similarities to known families of regulatory peptides. prepro-orexin mRNA and immunoreactive orexin-A are localized in neurons within and around the lateral and posterior hypothalamus in the adult rat brain. When administered centrally to rats, these peptides stimulate food consumption. prepro-orexin mRNA level is up-regulated upon fasting, suggesting a physiological role for the peptides as mediators in the central feedback mechanism that regulates feeding behavior.
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            The hypocretins: hypothalamus-specific peptides with neuroexcitatory activity.

            We describe a hypothalamus-specific mRNA that encodes preprohypocretin, the putative precursor of a pair of peptides that share substantial amino acid identities with the gut hormone secretin. The hypocretin (Hcrt) protein products are restricted to neuronal cell bodies of the dorsal and lateral hypothalamic areas. The fibers of these neurons are widespread throughout the posterior hypothalamus and project to multiple targets in other areas, including brainstem and thalamus. Hcrt immunoreactivity is associated with large granular vesicles at synapses. One of the Hcrt peptides was excitatory when applied to cultured, synaptically coupled hypothalamic neurons, but not hippocampal neurons. These observations suggest that the hypocretins function within the CNS as neurotransmitters.
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              A spatial map of olfactory receptor expression in the Drosophila antenna.

              Insects provide an attractive system for the study of olfactory sensory perception. We have identified a novel family of seven transmembrane domain proteins, encoded by 100 to 200 genes, that is likely to represent the family of Drosophila odorant receptors. Members of this gene family are expressed in topographically defined subpopulations of olfactory sensory neurons in either the antenna or the maxillary palp. Sensory neurons express different complements of receptor genes, such that individual neurons are functionally distinct. The isolation of candidate odorant receptor genes along with a genetic analysis of olfactory-driven behavior in insects may ultimately afford a system to understand the mechanistic link between odor recognition and behavior.
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                Author and article information

                Journal
                Front Neurosci
                Front. Neurosci.
                Frontiers in Neuroscience
                Frontiers Media S.A.
                1662-4548
                1662-453X
                01 May 2012
                12 February 2013
                2013
                : 7
                : 12
                Affiliations
                [1] 1Behaviour and Metabolism Laboratory, Champalimaud Neuroscience Programme, Champalimaud Centre for the Unknown Lisbon, Portugal
                Author notes

                Edited by: Björn Brembs, Freie Universität Berlin, Germany

                Reviewed by: Frédéric Marion-Poll, AgroParisTech, France; Greg Suh, NYU School of Medicine, USA

                *Correspondence: Carlos Ribeiro, Behaviour and Metabolism Laboratory, Champalimaud Neuroscience Programme, Champalimaud Centre for the Unknown, Avenida Brasília s/n, 1400-038 Lisboa, Portugal. e-mail: carlos.ribeiro@ 123456neuro.fchampalimaud.org

                This article was submitted to Frontiers in Decision Neuroscience, a specialty of Frontiers in Neuroscience.

                Article
                10.3389/fnins.2013.00012
                3569668
                23407678
                37b7322c-4678-4811-811d-afbe6cfac8f7
                Copyright © 2013 Itskov and Ribeiro.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in other forums, provided the original authors and source are credited and subject to any copyright notices concerning any third-party graphics etc.

                History
                : 06 March 2012
                : 21 January 2013
                Page count
                Figures: 5, Tables: 0, Equations: 0, References: 131, Pages: 13, Words: 11478
                Categories
                Neuroscience
                Review Article

                Neurosciences
                behavior,sensory systems,feeding,olfaction,taste,neuromodulators,neuropeptides,internal state
                Neurosciences
                behavior, sensory systems, feeding, olfaction, taste, neuromodulators, neuropeptides, internal state

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