Postprandial sleep mechanics in Drosophila

Food consumption is thought to induce sleepiness. However, little is known about how postprandial sleep is regulated. Here, we simultaneously measured sleep and food intake of individual flies and found a transient rise in sleep following meals. Depending on the amount consumed, the effect ranged from slightly arousing to strongly sleep inducing. Postprandial sleep was positively correlated with ingested volume, protein, and salt—but not sucrose—revealing meal property-specific regulation. Silencing of leucokinin receptor (Lkr) neurons specifically reduced sleep induced by protein consumption. Thermogenetic stimulation of leucokinin (Lk) neurons decreased whereas Lk downregulation by RNAi increased postprandial sleep, suggestive of an inhibitory connection in the Lk-Lkr circuit. We further identified a subset of non-leucokininergic cells proximal to Lkr neurons that rhythmically increased postprandial sleep when silenced, suggesting that these cells are cyclically gated inhibitory inputs to Lkr neurons. Together, these findings reveal the dynamic nature of postprandial sleep. DOI: http://dx.doi.org/10.7554/eLife.19334.001

[1]  Giulio Tononi,et al.  Sleep homeostasis in Drosophila melanogaster. , 2004, Sleep.

[2]  G. Goodhill,et al.  How deeply does your mutant sleep? Probing arousal to better understand sleep defects in Drosophila , 2015, Scientific Reports.

[3]  Julie H. Simpson,et al.  A GAL4-driver line resource for Drosophila neurobiology. , 2012, Cell reports.

[4]  Ronald L. Davis,et al.  Spatiotemporal Gene Expression Targeting with the TARGET and Gene-Switch Systems in Drosophila , 2004, Science's STKE.

[5]  R. Mains,et al.  Inducible Genetic Suppression of Neuronal Excitability , 1999, The Journal of Neuroscience.

[6]  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.

[7]  Gil B. Carvalho,et al.  Quantifying Drosophila food intake: comparative analysis of current methodology , 2014, Nature Methods.

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

[9]  B. van Swinderen,et al.  A Dynamic Deep Sleep Stage in Drosophila , 2013, The Journal of Neuroscience.

[10]  C. Maggi,et al.  The tachykinin NH2-senktide, a selective neurokinin B receptor agonist, is a very potent inhibitor of salt appetite in the rat , 1988, Neuroscience Letters.

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

[12]  J. Dow,et al.  Isolation and characterization of a leucokinin-like peptide of Drosophila melanogaster. , 1999, The Journal of experimental biology.

[13]  Scott Waddell,et al.  Clock and cycle Limit Starvation-Induced Sleep Loss in Drosophila , 2010, Current Biology.

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

[15]  A. Knutsson,et al.  Onset of Drowsiness and Satiation After Meals with Different Energy Contents , 2001, Nutrition and health.

[16]  A. Harmar,et al.  Dietary Modulation of Drosophila Sleep-Wake Behaviour , 2010, PloS one.

[17]  S. Tomchik,et al.  Neurofibromin Loss of Function Drives Excessive Grooming in Drosophila , 2016, G3: Genes, Genomes, Genetics.

[18]  Johannes D. Seelig,et al.  Feature detection and orientation tuning in the Drosophila central complex , 2013, Nature.

[19]  Matthew S. Thimgan,et al.  Inducing Sleep by Remote Control Facilitates Memory Consolidation in Drosophila , 2011, Science.

[20]  D. Gerashchenko,et al.  Substance P and the neurokinin-1 receptor regulate electroencephalogram non-rapid eye movement sleep slow-wave activity locally , 2015, Neuroscience.

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

[22]  G. Tononi,et al.  Correlates of sleep and waking in Drosophila melanogaster. , 2000, Science.

[23]  L. A. Reyner,et al.  ‘Post-lunch’ sleepiness during prolonged, monotonous driving — Effects of meal size , 2012, Physiology & Behavior.

[24]  P. Shaw,et al.  The Perilipin Homologue, Lipid Storage Droplet 2, Regulates Sleep Homeostasis and Prevents Learning Impairments Following Sleep Loss , 2010, PLoS biology.

[25]  S. Benzer,et al.  Prandiology of Drosophila and the CAFE assay , 2007, Proceedings of the National Academy of Sciences.

[26]  Gero Miesenböck,et al.  Neuronal Machinery of Sleep Homeostasis in Drosophila , 2014, Neuron.

[27]  C. Winrow,et al.  Orexin receptors: pharmacology and therapeutic opportunities. , 2011, Annual review of pharmacology and toxicology.

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

[29]  J. Blau,et al.  Circadian rhythms in neuronal activity propagate through output circuits , 2016, Nature Neuroscience.

[30]  S. Elsenbruch,et al.  Meal Composition and Its Effect on Postprandial Sleepiness , 1997, Physiology & Behavior.

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

[32]  S. Pletcher,et al.  Re-Patterning Sleep Architecture in Drosophila through Gustatory Perception and Nutritional Quality , 2012, PLoS genetics.

[33]  S. Woods,et al.  Hydration state controls stress responsiveness and social behavior , 2011, Appetite.

[34]  M. Rosbash,et al.  Short Neuropeptide F Is a Sleep-Promoting Inhibitory Modulator , 2013, Neuron.

[35]  D. Kripke,et al.  Relationships among dietary nutrients and subjective sleep, objective sleep, and napping in women. , 2010, Sleep medicine.

[36]  N. Read,et al.  Effects of meals on objective and subjective measures of daytime sleepiness. , 1998, Journal of applied physiology.

[37]  Pavel Masek,et al.  translin Is Required for Metabolic Regulation of Sleep , 2016, Current Biology.

[38]  Allan I Pack,et al.  Rest in Drosophila Is a Sleep-like State , 2000, Neuron.

[39]  G K Zammit,et al.  Postprandial sleep in healthy men. , 1995, Sleep.

[40]  K. Seipel,et al.  Filling the gut activates paradoxical sleep in suckling rats. , 1998, Developmental psychobiology.

[41]  A. Sehgal,et al.  Identification of Redeye, a new sleep-regulating protein whose expression is modulated by sleep amount , 2014, eLife.

[42]  E. Z. Kim,et al.  High-Resolution Positional Tracking for Long-Term Analysis of Drosophila Sleep and Locomotion Using the “Tracker” Program , 2012, PloS one.

[43]  Michael Bate,et al.  Altered Electrical Properties in DrosophilaNeurons Developing without Synaptic Transmission , 2001, The Journal of Neuroscience.

[44]  W. Orr,et al.  Postprandial sleepiness: objective documentation via polysomnography. , 1983, Sleep.

[45]  M. Lancel,et al.  Intracerebral oxytocin modulates sleep–wake behaviour in male rats , 2003, Regulatory Peptides.

[46]  Kevin W Eliceiri,et al.  NIH Image to ImageJ: 25 years of image analysis , 2012, Nature Methods.

[47]  W. Orr,et al.  A Comparison of Feeding to Cephalic Stimulation on Postprandial Sleepiness , 1998, Physiology & Behavior.