Neural basis of hunger-driven behaviour in Drosophila

Hunger is a motivational state that drives eating and food-seeking behaviour. In a psychological sense, hunger sets the goal that guides an animal in the pursuit of food. The biological basis underlying this purposive, goal-directed nature of hunger has been under intense investigation. With its rich behavioural repertoire and genetically tractable nervous system, the fruit fly Drosophila melanogaster has emerged as an excellent model system for studying the neural basis of hunger and hunger-driven behaviour. Here, we review our current understanding of how hunger is sensed, encoded and translated into foraging and feeding behaviours in the fruit fly.

[1]  T. Wen,et al.  Developmental Control of Foraging and Social Behavior by the Drosophila Neuropeptide Y-like System , 2003, Neuron.

[2]  Michael H. Dickinson,et al.  Idiothetic Path Integration in the Fruit Fly Drosophila melanogaster , 2017, Current Biology.

[3]  Oliver Barnstedt,et al.  Aversive Learning and Appetitive Motivation Toggle Feed-Forward Inhibition in the Drosophila Mushroom Body , 2016, Neuron.

[4]  L. B. Browne,et al.  Locomotor activity of the blowfly as a function of feeding and starvation , 1960 .

[5]  Soohong Min,et al.  Taste-independent detection of the caloric content of sugar in Drosophila , 2011, Proceedings of the National Academy of Sciences.

[6]  Alisson M. Gontijo,et al.  Imaginal Discs Secrete Insulin-Like Peptide 8 to Mediate Plasticity of Growth and Maturation , 2012, Science.

[7]  D. Nässel,et al.  Characterization of a set of abdominal neuroendocrine cells that regulate stress physiology using colocalized diuretic peptides in Drosophila , 2017, Cellular and Molecular Life Sciences.

[8]  H. Kohsaka,et al.  Serotonin and Downstream Leucokinin Neurons Modulate Larval Turning Behavior in Drosophila , 2014, The Journal of Neuroscience.

[9]  A. Fiala,et al.  SIFamide Translates Hunger Signals into Appetitive and Feeding Behavior in Drosophila. , 2017, Cell reports.

[10]  Phuong Chung,et al.  Dissection of the Drosophila neuropeptide F circuit using a high-throughput two-choice assay , 2017, Proceedings of the National Academy of Sciences.

[11]  Xinnian Chen,et al.  Glucose increases activity and Ca2+ in insulin-producing cells of adult Drosophila , 2010, Neuroreport.

[12]  Johannes Felsenberg,et al.  Activity of Defined Mushroom Body Output Neurons Underlies Learned Olfactory Behavior in Drosophila , 2015, Neuron.

[13]  Gyunghee Lee,et al.  Hemolymph Sugar Homeostasis and Starvation-Induced Hyperactivity Affected by Genetic Manipulations of the Adipokinetic Hormone-Encoding Gene in Drosophila melanogaster , 2004, Genetics.

[14]  M. Pankratz,et al.  Neuromedin U and Its Putative Drosophila Homolog hugin , 2006, PLoS biology.

[15]  A Sih,et al.  Optimal behavior: can foragers balance two conflicting demands? , 1980, Science.

[16]  Norbert Perrimon,et al.  Drosophila Cytokine Unpaired 2 Regulates Physiological Homeostasis by Remotely Controlling Insulin Secretion , 2012, Cell.

[17]  J. Pin,et al.  Sensing of Amino Acids in a Dopaminergic Circuitry Promotes Rejection of an Incomplete Diet in Drosophila , 2014, Cell.

[18]  M. Carlsson,et al.  Insulin-Producing Cells in the Drosophila Brain also Express Satiety-Inducing Cholecystokinin-Like Peptide, Drosulfakinin , 2012, Front. Endocrin..

[19]  F. Hauser,et al.  Expression Patterns of the Drosophila Neuropeptide CCHamide-2 and Its Receptor May Suggest Hormonal Signaling from the Gut to the Brain , 2013, PloS one.

[20]  P. Shen,et al.  Genetic and Neurobiological Analyses of the Noradrenergic-like System in Vulnerability to Sugar Overconsumption Using a Drosophila Model , 2017, Scientific Reports.

[21]  K. Nairz,et al.  Nutrient-Dependent Expression of Insulin-like Peptides from Neuroendocrine Cells in the CNS Contributes to Growth Regulation in Drosophila , 2002, Current Biology.

[22]  M. Tatar,et al.  Drosophila short neuropeptide F signalling regulates growth by ERK-mediated insulin signalling , 2008, Nature Cell Biology.

[23]  E. Rulifson,et al.  Conserved mechanisms of glucose sensing and regulation by Drosophila corpora cardiaca cells , 2004, Nature.

[24]  M. Texada,et al.  Modulation of Drosophila post-feeding physiology and behavior by the neuropeptide leucokinin , 2018, PLoS genetics.

[25]  P. Shen,et al.  Regulation of aversion to noxious food by Drosophila neuropeptide Y– and insulin-like systems , 2005, Nature Neuroscience.

[26]  Paul T. Tarr,et al.  A glucagon-like endocrine pathway in Drosophila modulates both lipid and carbohydrate homeostasis , 2008, Journal of Experimental Biology.

[27]  Young-Joon Kim,et al.  A fat-derived metabolite regulates a peptidergic feeding circuit in Drosophila , 2017, PLoS biology.

[28]  Soohong Min,et al.  Identification of a Peptidergic Pathway Critical to Satiety Responses in Drosophila , 2016, Current Biology.

[29]  J. Beshel,et al.  Graded Encoding of Food Odor Value in the Drosophila Brain , 2013, The Journal of Neuroscience.

[30]  S. Kondo,et al.  CCHamide-2 Is an Orexigenic Brain-Gut Peptide in Drosophila , 2015, PloS one.

[31]  Kyeong-Man Kim,et al.  Developmental regulation and functions of the expression of the neuropeptide corazonin in Drosophila melanogaster , 2008, Cell and Tissue Research.

[32]  Yong-Mahn Han,et al.  Drosophila Short Neuropeptide F Regulates Food Intake and Body Size* , 2004, Journal of Biological Chemistry.

[33]  M. Pankratz,et al.  Selection of Motor Programs for Suppressing Food Intake and Inducing Locomotion in the Drosophila Brain , 2014, PLoS biology.

[34]  R. Stocker,et al.  Drosophila P[Gal4] lines reveal that motor neurons involved in feeding persist through metamorphosis. , 1998, Journal of neurobiology.

[35]  G. Rubin,et al.  The neuronal architecture of the mushroom body provides a logic for associative learning , 2014, eLife.

[36]  Shamik Dasgupta,et al.  A Neural Circuit Mechanism Integrating Motivational State with Memory Expression in Drosophila , 2009, Cell.

[37]  Visualizing neuromodulation in vivo: TANGO-mapping of dopamine signaling reveals appetite control of sugar sensing. , 2012, Cell.

[38]  E. Rulifson,et al.  Remote control of insulin secretion by fat cells in Drosophila. , 2009, Cell metabolism.

[39]  Seth M Tomchik,et al.  Postprandial sleep mechanics in Drosophila , 2016, eLife.

[40]  G. Rubin,et al.  Mushroom body output neurons encode valence and guide memory-based action selection in Drosophila , 2014, eLife.

[41]  Pavel M Itskov,et al.  Internal amino acid state modulates yeast taste neurons to support protein homeostasis in Drosophila , 2017, bioRxiv.

[42]  M. Pankratz,et al.  Central relay of bitter taste to the protocerebrum by peptidergic interneurons in the Drosophila brain , 2016, Nature Communications.

[43]  Daryl M. Gohl,et al.  Motor neurons controlling fluid ingestion in Drosophila , 2012, Proceedings of the National Academy of Sciences.

[44]  Identification and characterization of mushroom body neurons that regulate fat storage in Drosophila , 2018, Neural Development.

[45]  S. Sternson Hypothalamic Survival Circuits: Blueprints for Purposive Behaviors , 2013, Neuron.

[46]  A. Kamikouchi,et al.  The Nutrient-Responsive Hormone CCHamide-2 Controls Growth by Regulating Insulin-like Peptides in the Brain of Drosophila melanogaster , 2015, PLoS genetics.

[47]  Jing W. Wang,et al.  Presynaptic Facilitation by Neuropeptide Signaling Mediates Odor-Driven Food Search , 2011, Cell.

[48]  C. Grimmelikhuijzen,et al.  Molecular cloning and genomic organization of a novel receptor from Drosophila melanogaster structurally related to mammalian galanin receptors. , 2000, Biochemical and biophysical research communications.

[49]  Yan Zhu,et al.  Taotie neurons regulate appetite in Drosophila , 2016, Nature Communications.

[50]  Kristin Scott,et al.  Motor Control in a Drosophila Taste Circuit , 2009, Neuron.

[51]  D. Nässel,et al.  Systemic corazonin signalling modulates stress responses and metabolism in Drosophila , 2016, Open Biology.

[52]  Kei Ito,et al.  A single pair of interneurons commands the Drosophila feeding motor program , 2013, Nature.

[53]  Kevin J Mann,et al.  Starvation-Induced Depotentiation of Bitter Taste in Drosophila , 2016, Current Biology.

[54]  D. Nässel,et al.  A comparative review of short and long neuropeptide F signaling in invertebrates: Any similarities to vertebrate neuropeptide Y signaling? , 2011, Peptides.

[55]  F. Hauser,et al.  Molecular identification of the first SIFamide receptor. , 2006, Biochemical and biophysical research communications.

[56]  Ting Zhang,et al.  Octopamine-mediated circuit mechanism underlying controlled appetite for palatable food in Drosophila , 2013, Proceedings of the National Academy of Sciences.

[57]  Wei L. Shen,et al.  A post-ingestive amino acid sensor promotes food consumption in Drosophila , 2018, Cell Research.

[58]  S. Waddell,et al.  Rapid Consolidation to a radish and Protein Synthesis-Dependent Long-Term Memory after Single-Session Appetitive Olfactory Conditioning in Drosophila , 2008, The Journal of Neuroscience.

[59]  S. Waddell,et al.  Sequential Use of Mushroom Body Neuron Subsets during Drosophila Odor Memory Processing , 2007, Neuron.

[60]  M. Miura,et al.  A Drosophila orphan G protein-coupled receptor BOSS functions as a glucose-responding receptor: Loss of boss causes abnormal energy metabolism , 2008, Proceedings of the National Academy of Sciences.

[61]  M. Pankratz,et al.  Opposing effects of dietary protein and sugar regulate a transcriptional target of Drosophila insulin-like peptide signaling. , 2008, Cell metabolism.

[62]  P. Kapahi,et al.  A Role for S6 Kinase and Serotonin in Postmating Dietary Switch and Balance of Nutrients in D. melanogaster , 2010, Current Biology.

[63]  P. Shen,et al.  Regulation of hunger-driven behaviors by neural ribosomal S6 kinase in Drosophila. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[64]  R. Birse,et al.  Regulation of insulin-producing cells in the adult Drosophila brain via the tachykinin peptide receptor DTKR , 2011, Journal of Experimental Biology.

[65]  F. Díaz-Benjumea,et al.  Variability in the number of abdominal leucokinergic neurons in adult Drosophila melanogaster , 2017, The Journal of comparative neurology.

[66]  Julie H. Simpson,et al.  A Subset of Serotonergic Neurons Evokes Hunger in Adult Drosophila , 2015, Current Biology.

[67]  T. Tanimura,et al.  Drosophila Evaluates and Learns the Nutritional Value of Sugars , 2011, Current Biology.

[68]  J. Veenstra Isolation and structure of the Drosophila corazonin gene. , 1994, Biochemical and biophysical research communications.

[69]  David J. Anderson,et al.  Independent, Reciprocal Neuromodulatory Control of Sweet and Bitter Taste Sensitivity during Starvation in Drosophila , 2014, Neuron.

[70]  B. Dickson,et al.  Sex Peptide Receptor and Neuronal TOR/S6K Signaling Modulate Nutrient Balancing in Drosophila , 2010, Current Biology.

[71]  S. Kondo,et al.  The Neuropeptide Allatostatin A Regulates Metabolism and Feeding Decisions in Drosophila , 2015, Scientific Reports.

[72]  V. G. Dethier,et al.  Chemoreception in insects. , 1948, Physiological reviews.

[73]  J. Lichtenberg On motivational systems. , 1990, Journal of the American Psychoanalytic Association.

[74]  Michael H. Dickinson,et al.  Automated monitoring and quantitative analysis of feeding behaviour in Drosophila , 2014, Nature Communications.

[75]  C. Helfrich-Förster,et al.  Allatostatin A Signalling in Drosophila Regulates Feeding and Sleep and Is Modulated by PDF , 2016, PLoS genetics.

[76]  David J. Anderson,et al.  Allatostatin-A neurons inhibit feeding behavior in adult Drosophila , 2012, Proceedings of the National Academy of Sciences.

[77]  G. Cooney,et al.  Insulin controls food intake and energy balance via NPY neurons , 2017, Molecular metabolism.

[78]  J. Montagne,et al.  A Nutrient Sensor Mechanism Controls Drosophila Growth , 2003, Cell.

[79]  Qili Liu,et al.  Branch-specific plasticity of a bifunctional dopamine circuit encodes protein hunger , 2017, Science.

[80]  S. Waddell,et al.  Remembering Nutrient Quality of Sugar in Drosophila , 2011, Current Biology.

[81]  D. Nässel,et al.  Identified peptidergic neurons in the Drosophila brain regulate insulin-producing cells, stress responses and metabolism by coexpressed short neuropeptide F and corazonin , 2012, Cellular and Molecular Life Sciences.

[82]  Yan Li,et al.  Drosophila FIT is a protein-specific satiety hormone essential for feeding control , 2017, Nature Communications.

[83]  M. Blackburn,et al.  The identification of two myoinhibitory peptides, with sequence similarities to the galanins, isolated from the ventral nerve cord of Manduca sexta , 1995, Regulatory Peptides.

[84]  M. Tatar,et al.  Minibrain/Dyrk1a Regulates Food Intake through the Sir2-FOXO-sNPF/NPY Pathway in Drosophila and Mammals , 2012, PLoS genetics.

[85]  D. Nässel,et al.  Insulin-producing cells in the brain of adult Drosophila are regulated by the serotonin 5-HT1A receptor , 2011, Cellular and Molecular Life Sciences.

[86]  Aldo A. Faisal,et al.  Internal states drive nutrient homeostasis by modulating exploration-exploitation trade-off , 2016, bioRxiv.

[87]  Zhe Yang,et al.  Octopamine mediates starvation-induced hyperactivity in adult Drosophila , 2015, Proceedings of the National Academy of Sciences.

[88]  M. Pankratz,et al.  Candidate Gustatory Interneurons Modulating Feeding Behavior in the Drosophila Brain , 2005, PLoS biology.

[89]  Minrong Ai,et al.  Taste-independent nutrient selection is mediated by a brain-specific Na+/solute cotransporter in Drosophila , 2013, Nature Neuroscience.

[90]  Casey M. Schneider-Mizell,et al.  Synaptic transmission parallels neuromodulation in a central food-intake circuit , 2016, bioRxiv.

[91]  Kevin J Mann,et al.  Dopaminergic Modulation of Sucrose Acceptance Behavior in Drosophila , 2012, Neuron.

[92]  Guo Cheng,et al.  Regulation of starvation-induced hyperactivity by insulin and glucagon signaling in adult Drosophila , 2016, eLife.

[93]  J. Veenstra,et al.  Detailed analysis of leucokinin-expressing neurons and their candidate functions in the Drosophila nervous system , 2010, Cell and Tissue Research.

[94]  K. Kaiser,et al.  Hormonally controlled chloride movement across Drosophila tubules is via ion channels in stellate cells. , 1998, American journal of physiology. Regulatory, integrative and comparative physiology.

[95]  Jing W Wang,et al.  Starvation promotes concerted modulation of appetitive olfactory behavior via parallel neuromodulatory circuits , 2015, eLife.

[96]  J. Dubnau,et al.  A Leptin Analog Locally Produced in the Brain Acts via a Conserved Neural Circuit to Modulate Obesity-Linked Behaviors in Drosophila. , 2017, Cell metabolism.

[97]  B. Rudy,et al.  Drosophila SLC5A11 Mediates Hunger by Regulating K+ Channel Activity , 2016, Current Biology.

[98]  Shireen A. Davies,et al.  Systematic G-protein-coupled Receptor Analysis inDrosophila melanogaster Identifies a Leucokinin Receptor with Novel Roles* , 2002, The Journal of Biological Chemistry.

[99]  K. Tsutsui,et al.  Evolution of gonadotropin-inhibitory hormone receptor and its ligand. , 2014, General and comparative endocrinology.

[100]  M. Williamson,et al.  Molecular cloning, genomic organization, and expression of a B-type (cricket-type) allatostatin preprohormone from Drosophila melanogaster. , 2001, Biochemical and biophysical research communications.

[101]  Tetsuya Miyamoto,et al.  A Fructose Receptor Functions as a Nutrient Sensor in the Drosophila Brain , 2012, Cell.

[102]  Tamas L. Horvath,et al.  Hypothalamic Agrp Neurons Drive Stereotypic Behaviors beyond Feeding , 2017, Cell.

[103]  M. Carlsson,et al.  Serotonin and insulin‐like peptides modulate leucokinin‐producing neurons that affect feeding and water homeostasis in Drosophila , 2015, The Journal of comparative neurology.

[104]  E. Hafen,et al.  An evolutionarily conserved function of the Drosophila insulin receptor and insulin-like peptides in growth control , 2001, Current Biology.

[105]  Christian Schusterreiter,et al.  A Taste Circuit that Regulates Ingestion by Integrating Food and Hunger Signals , 2016, Cell.

[106]  S. Benzer,et al.  The Leucokinin Pathway and Its Neurons Regulate Meal Size in Drosophila , 2010, Current Biology.

[107]  Suewei Lin,et al.  Drosophila mushroom bodies integrate hunger and satiety signals to control innate food-seeking behavior , 2018, eLife.

[108]  J. C. Hall,et al.  Comparative analysis of Corazonin‐encoding genes (Crz's) in Drosophila species and functional insights into Crz‐expressing neurons , 2005, The Journal of comparative neurology.

[109]  Differential Effects of Tissue-Specific Deletion of BOSS on Feeding Behaviors and Energy Metabolism , 2015, PloS one.

[110]  D. Andersen,et al.  Secreted Peptide Dilp8 Coordinates Drosophila Tissue Growth with Developmental Timing , 2012, Science.

[111]  Mark R. Brown,et al.  Identification of a Drosophila brain-gut peptide related to the neuropeptide Y family , 1999, Peptides.

[112]  D. Richter,et al.  Reverse physiology in Drosophila: identification of a novel allatostatin‐like neuropeptide and its cognate receptor structurally related to the mammalian somatostatin/galanin/opioid receptor family , 1999, The EMBO journal.

[113]  D. Nässel,et al.  Drosophila Insulin-Producing Cells Are Differentially Modulated by Serotonin and Octopamine Receptors and Affect Social Behavior , 2014, PloS one.

[114]  Jason Sih-Yu Lai,et al.  Nutrient Sensor in the Brain Directs the Action of the Brain-Gut Axis in Drosophila , 2015, Neuron.

[115]  Kevin J Mann,et al.  Coupled Sensing of Hunger and Thirst Signals Balances Sugar and Water Consumption , 2016, Cell.