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      Selection of Motor Programs for Suppressing Food Intake and Inducing Locomotion in the Drosophila Brain

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          There is no author summary for this article yet. Authors can add summaries to their articles on ScienceOpen to make them more accessible to a non-specialist audience.

          Abstract

          This study reveals that a cluster of neurons expressing the neuropeptide hugin transmit inputs from higher brain centers to motor centers, thereby regulating feeding and locomotion in fruit fly larvae.

          Abstract

          Central mechanisms by which specific motor programs are selected to achieve meaningful behaviors are not well understood. Using electrophysiological recordings from pharyngeal nerves upon central activation of neurotransmitter-expressing cells, we show that distinct neuronal ensembles can regulate different feeding motor programs. In behavioral and electrophysiological experiments, activation of 20 neurons in the brain expressing the neuropeptide hugin, a homolog of mammalian neuromedin U, simultaneously suppressed the motor program for food intake while inducing the motor program for locomotion. Decreasing hugin neuropeptide levels in the neurons by RNAi prevented this action. Reducing the level of hugin neuronal activity alone did not have any effect on feeding or locomotion motor programs. Furthermore, use of promoter-specific constructs that labeled subsets of hugin neurons demonstrated that initiation of locomotion can be separated from modulation of its motor pattern. These results provide insights into a neural mechanism of how opposing motor programs can be selected in order to coordinate feeding and locomotive behaviors.

          Author Summary

          In the animal kingdom, two of the most essential behaviors are locomotion and feeding. The motor programs underlying these behaviors are controlled by higher-order circuits in the central nervous system. However, how an organism selects a particular motor program based on inputs from the information-processing higher brain centers to generate an adaptable behavior is not well understood. Here, we analyze the behavior of Drosophila larvae after activating a small cluster of neurons in the brain and show that the animals simultaneously stop eating and start moving. These neurons express the neuropeptide hugin, which is homologous to the mammalian neuromedins. We show that the reduction of food intake depends on hugin and that the cluster of hugin neurons is functionally divided into distinct subgroups that both accelerate the motor program for locomotion and decelerate the motor program for feeding. We propose that hugin neurons represent a control system between the higher brain circuits that process information and those that execute motor programs.

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          Most cited references69

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          Molecular architecture of smell and taste in Drosophila.

          The chemical senses-smell and taste-allow animals to evaluate and distinguish valuable food resources from dangerous substances in the environment. The central mechanisms by which the brain recognizes and discriminates attractive and repulsive odorants and tastants, and makes behavioral decisions accordingly, are not well understood in any organism. Recent molecular and neuroanatomical advances in Drosophila have produced a nearly complete picture of the peripheral neuroanatomy and function of smell and taste in this insect. Neurophysiological experiments have begun to provide insight into the mechanisms by which these animals process chemosensory cues. Given the considerable anatomical and functional homology in smell and taste pathways in all higher animals, experimental approaches in Drosophila will likely provide broad insights into the problem of sensory coding. Here we provide a critical review of the recent literature in this field and comment on likely future directions.
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            An olfactory sensory map in the fly brain.

            We have isolated the "complete" repertoire of genes encoding the odorant receptors in Drosophila and employ these genes to provide a molecular description of the organization of the peripheral olfactory system. The repertoire of Drosophila odorant receptors is encoded by 57 genes. Individual sensory neurons are likely to express only a single receptor gene. Neurons expressing a given gene project axons to one or two spatially invariant glomeruli in the antennal lobe. The insect brain therefore retains a two-dimensional map of receptor activation such that the quality of an odor may be encoded by different spatial patterns of activity in the antennal lobe.
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              Genetic transformation of Drosophila with transposable element vectors.

              Exogenous DNA sequences were introduced into the Drosophila germ line. A rosy transposon (ry1), constructed by inserting a chromosomal DNA fragment containing the wild-type rosy gene into a P transposable element, transformed germ line cells in 20 to 50 percent of the injected rosy mutant embryos. Transformants contained one or two copies of chromosomally integrated, intact ry1 that were stably inherited in subsequent generations. These transformed flies had wild-type eye color indicating that the visible genetic defect in the host strain could be fully and permanently corrected by the transferred gene. To demonstrate the generality of this approach, a DNA segment that does not confer a recognizable phenotype on recipients was also transferred into germ line chromosomes.
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                Author and article information

                Contributors
                Role: Academic Editor
                Journal
                PLoS Biol
                PLoS Biol
                plos
                plosbiol
                PLoS Biology
                Public Library of Science (San Francisco, USA )
                1544-9173
                1545-7885
                June 2014
                24 June 2014
                26 June 2014
                : 12
                : 6
                : e1001893
                Affiliations
                [1 ]Molecular Brain Physiology and Behavior, LIMES-Institute, University of Bonn, Germany
                [2 ]Department of Forensic Entomology, Institute of Legal Medicine, Jena University Hospital, Germany
                [3 ]Brain Research Center, National Tsing Hua University, Taiwan
                Brandeis University, United States of America
                Author notes

                The authors have declared that no competing interests exist.

                The author(s) have made the following declarations about their contributions: Conceived and designed the experiments: AS SH PS AM MP MJP. Performed the experiments: AS SH PS AM MP MZ. Analyzed the data: AS SH PS AM MP MZ MJP. Contributed reagents/materials/analysis tools: RS ASC. Wrote the paper: AS MJP.

                Article
                PBIOLOGY-D-14-00605
                10.1371/journal.pbio.1001893
                4068981
                24960360
                cbbcd539-d3c3-4f80-9241-fe28aebb2587
                Copyright @ 2014

                This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 17 February 2014
                : 15 May 2014
                Page count
                Pages: 17
                Funding
                Financial support from DFG (Deutsche Forschungsgemeinschaft) grant PA787, DFG Sonderforschungsbereich SFB645 and SFB704, LIMES (Life and Medical Sciences) graduate school of Nordrhein-Westfalia (NRW), and DFG Cluster of Excellence ImmunoSensation. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Neuroscience

                Life sciences
                Life sciences

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