Organization of descending neurons in Drosophila melanogaster

Neural processing in the brain controls behavior through descending neurons (DNs) - neurons which carry signals from the brain to the spinal cord (or thoracic ganglia in insects). Because DNs arise from multiple circuits in the brain, the numerical simplicity and availability of genetic tools make Drosophila a tractable model for understanding descending motor control. As a first step towards a comprehensive study of descending motor control, here we estimate the number and distribution of DNs in the Drosophila brain. We labeled DNs by backfilling them with dextran dye applied to the neck connective and estimated that there are ~1100 DNs distributed in 6 clusters in Drosophila. To assess the distribution of DNs by neurotransmitters, we labeled DNs in flies in which neurons expressing the major neurotransmitters were also labeled. We found DNs belonging to every neurotransmitter class we tested: acetylcholine, GABA, glutamate, serotonin, dopamine and octopamine. Both the major excitatory neurotransmitter (acetylcholine) and the major inhibitory neurotransmitter (GABA) are employed equally; this stands in contrast to vertebrate DNs which are predominantly excitatory. By comparing the distribution of DNs in Drosophila to those reported previously in other insects, we conclude that the organization of DNs in insects is highly conserved.

[1]  C. H. Page,et al.  Anatomical organization of neurons descending from the supraesophageal ganglion of the lobster , 1981, Brain Research.

[2]  Vikas Bhandawat,et al.  Activity in descending dopaminergic neurons represents but is not required for leg movements in the fruit fly Drosophila , 2015, Physiological reports.

[3]  Christopher M. Comer,et al.  Cellular Organization of an Antennal Mechanosensory Pathway in the Cockroach, Periplaneta americana , 1996, The Journal of Neuroscience.

[4]  G. Laurent,et al.  Role of GABAergic Inhibition in Shaping Odor-Evoked Spatiotemporal Patterns in the Drosophila Antennal Lobe , 2005, The Journal of Neuroscience.

[5]  Ulrike Träger,et al.  Polarization-Sensitive Descending Neurons in the Locust: Connecting the Brain to Thoracic Ganglia , 2011, The Journal of Neuroscience.

[6]  R. Nudo,et al.  Descending pathways to the spinal cord: A comparative study of 22 mammals , 1988, The Journal of comparative neurology.

[7]  A. Wong,et al.  Two-Photon Calcium Imaging Reveals an Odor-Evoked Map of Activity in the Fly Brain , 2003, Cell.

[8]  Alastair M. Hosie,et al.  Molecular biology of insect neuronal GABA receptors , 1997, Trends in Neurosciences.

[9]  A. Grinnell,et al.  THE PHYSIOLOGY OF EXCITABLE CELLS , 1984 .

[10]  Alexander Borst,et al.  Integration of Lobula Plate Output Signals by DNOVS1, an Identified Premotor Descending Neuron , 2007, The Journal of Neuroscience.

[11]  F. Gabbiani,et al.  Multiplexing of Motor Information in the Discharge of a Collision Detecting Neuron during Escape Behaviors , 2011, Neuron.

[12]  Michael B. Reiser,et al.  Visual Place Learning in Drosophila melanogaster , 2011, Nature.

[13]  Salil S. Bidaye,et al.  Neuronal Control of Drosophila Courtship Song , 2011, Neuron.

[14]  A. Georgopoulos,et al.  Eight pairs of descending visual neurons in the dragonfly give wing motor centers accurate population vector of prey direction , 2012, Proceedings of the National Academy of Sciences.

[15]  Jai Y. Yu,et al.  Cellular Organization of the Neural Circuit that Drives Drosophila Courtship Behavior , 2010, Current Biology.

[16]  N. Strausfeld,et al.  The organization of giant horizontal-motion-sensitive neurons and their synaptic relationships in the lateral deutocerebrum of Calliphora erythrocephala and Musca domestica , 1985, Cell and Tissue Research.

[17]  M. Mizunami Neural organization of ocellar pathways in the cockroach brain , 1995, The Journal of comparative neurology.

[18]  Nicholas J. Strausfeld,et al.  Arthropod Brains: Evolution, Functional Elegance, and Historical Significance , 2012 .

[19]  R. Robertson,et al.  A pair of motion-sensitive neurons in the locust encode approaches of a looming object , 2010, Journal of Comparative Physiology A.

[20]  J. Niven,et al.  Are Bigger Brains Better? , 2009, Current Biology.

[21]  T. Kitamoto,et al.  Drosophila cholinergic neurons and processes visualized with Gal4/UAS-GFP. , 2001, Brain research. Gene expression patterns.

[22]  N. J. Strausfeld,et al.  Convergence of visual, haltere, and prosternai inputs at neck motor neurons of Calliphora erythrocephala , 1985, Cell and Tissue Research.

[23]  D. Irving,et al.  The numbers of limb motor neurons in the human lumbosacral cord throughout life , 1977, Journal of the Neurological Sciences.

[24]  M. Mizunami,et al.  Morphology of higher‐order ocellar interneurons in the cockroach brain , 1995, The Journal of comparative neurology.

[25]  Kei Ito,et al.  Responses of Drosophila giant descending neurons to visual and mechanical stimuli , 2014, Journal of Experimental Biology.

[26]  Y. Toh,et al.  Morphological and physiological characterization of small multimodal ocellar interneurons in the American cockroach , 1990, The Journal of comparative neurology.

[27]  Hidehiko K. Inagaki,et al.  The neural basis of Drosophila gravity-sensing and hearing , 2009, Nature.

[28]  R N Singh,et al.  Neuroarchitecture of the tritocerebrum of Drosophila melanogaster , 1994, The Journal of comparative neurology.

[29]  Alexander Borst,et al.  Nonlinear Integration of Binocular Optic Flow by DNOVS2, A Descending Neuron of the Fly , 2008, The Journal of Neuroscience.

[30]  Kei Ito,et al.  A map of octopaminergic neurons in the Drosophila brain , 2009, The Journal of comparative neurology.

[31]  Robert M. Olberg,et al.  Pheromone-triggered flip-flopping interneurons in the ventral nerve cord of the silkworm moth,Bombyx mori , 1983, Journal of comparative physiology.

[32]  E. Staudacher Sensory responses of descending brain neurons in the walking cricket, Gryllus bimaculatus , 2001, Journal of Comparative Physiology A.

[33]  A. Leonardo,et al.  A spike-timing mechanism for action selection , 2014, Nature Neuroscience.

[34]  J. Hildebrand,et al.  Distribution of FMRFamide-like immunoreactivity in the brain and suboesophageal ganglion of the sphinx mothManduca sexta and colocalization with SCPB-, BPP-, and GABA-like immunoreactivity , 1990, Cell and Tissue Research.

[35]  Y. Hamasaka,et al.  γ‐Aminobutyric acid (GABA) signaling components in Drosophila: Immunocytochemical localization of GABAB receptors in relation to the GABAA receptor subunit RDL and a vesicular GABA transporter , 2007, The Journal of comparative neurology.

[36]  M. Changizi Relationship between number of muscles, behavioral repertoire size, and encephalization in mammals. , 2003, Journal of theoretical biology.

[37]  David Bradley,et al.  The Physiology of Excitable Cells, 4th edn. By DAVID J. AIDLEY. (Pp. xii+477; illustrated; £70/$95 hardback, £24.95/$47.95 paperback; ISBN 0 521 57415 3 hardback, 0 521 57421 8 paperback.) Cambridge: Cambridge University Press. 1998. , 1999 .

[38]  Wulfila Gronenberg,et al.  Brain Allometry in Bumblebee and Honey Bee Workers , 2005, Brain, Behavior and Evolution.

[39]  Louis K. Scheffer,et al.  A visual motion detection circuit suggested by Drosophila connectomics , 2013, Nature.

[40]  Rachel I. Wilson,et al.  Thermosensory processing in the Drosophila brain , 2014, Nature.

[41]  Christopher M. Comer,et al.  Correspondence of Escape-Turning Behavior with Activity of Descending Mechanosensory Interneurons in the Cockroach,Periplaneta americana , 1996, The Journal of Neuroscience.

[42]  A. Borst,et al.  Robust Coding of Ego-Motion in Descending Neurons of the Fly , 2009, The Journal of Neuroscience.

[43]  M. Burrows The Neurobiology of an Insect Brain , 1996 .

[44]  Julie H. Simpson,et al.  A Systematic Nomenclature for the Insect Brain , 2014, Neuron.

[45]  David K Yeates,et al.  Single-copy nuclear genes resolve the phylogeny of the holometabolous insects , 2009, BMC Biology.

[46]  Ryohei Kanzaki,et al.  Information flow through neural circuits for pheromone orientation , 2014, Nature Communications.

[47]  C. Labandeira,et al.  A Carboniferous insect gall: insight into early ecologic history of the Holometabola. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[48]  Ryuichi Okada,et al.  Distribution of dendrites of descending neurons and its implications for the basic organization of the cockroach brain , 2003, The Journal of comparative neurology.

[49]  Shawn R. Olsen,et al.  Divisive Normalization in Olfactory Population Codes , 2010, Neuron.

[50]  Charles Watson,et al.  Projections from the brain to the spinal cord in the mouse , 2010, Brain Structure and Function.

[51]  A. Büschges,et al.  New Moves in Motor Control , 2011, Current Biology.

[52]  Volker Hartenstein,et al.  Specification and development of the pars intercerebralis and pars lateralis, neuroendocrine command centers in the Drosophila brain. , 2007, Developmental biology.

[53]  N. Strausfeld,et al.  Visual system of calliphorid flies: Organization of optic glomeruli and their lobula complex efferents , 2007, The Journal of comparative neurology.

[54]  Stephan Saalfeld,et al.  Globally optimal stitching of tiled 3D microscopic image acquisitions , 2009, Bioinform..

[55]  Michael B. Reiser,et al.  Corrigendum: Two-photon calcium imaging from head-fixed Drosophila during optomotor walking behavior , 2011, Nature Methods.

[56]  J. Belanger Contrasting Tactics in Motor Control by Vertebrates and Arthropods1 , 2005, Integrative and comparative biology.

[57]  Jamey S. Kain,et al.  Asymmetric neurotransmitter release enables rapid odor lateralization in Drosophila , 2012, Nature.

[58]  Shawn R. Olsen,et al.  Sensory processing in the Drosophila antennal lobe increases reliability and separability of ensemble odor representations , 2007, Nature Neuroscience.

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

[60]  S. Buchner,et al.  Preliminary Investigations on a Pair of Giant Fibers in the Central Nervous System of Dipteran Flies , 1973 .

[61]  Ian A. Meinertzhagen,et al.  Glutamate, GABA and Acetylcholine Signaling Components in the Lamina of the Drosophila Visual System , 2008, PloS one.

[62]  W. Gronenberg,et al.  Oculomotor control in calliphorid flies: Organization of descending neurons to neck motor neurons responding to visual stimuli , 1995, The Journal of comparative neurology.

[63]  C. Goodman,et al.  Genetic analysis of Laminin A in Drosophila: extracellular matrix containing laminin A is required for ocellar axon pathfinding. , 1996, Development.

[64]  J. Storm-Mathisen,et al.  Glutamate-like immunoreactivity in identified neuronal populations of insect nervous systems , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[65]  G. ten Bruggencate Muscles and their neural control. , 1986, Applied neurophysiology.

[66]  W. Gronenberg,et al.  Descending neurons supplying the neck and flight motor of diptera: Organization and neuroanatomical relationships with visual pathways , 1990, The Journal of comparative neurology.

[67]  D. Maxwell,et al.  Neurotransmitter phenotypes of descending systems in the rat lumbar spinal cord , 2012, Neuroscience.

[68]  R. Lemon Descending pathways in motor control. , 2008, Annual review of neuroscience.

[69]  Michael B. Reiser,et al.  Contributions of the 12 Neuron Classes in the Fly Lamina to Motion Vision , 2013, Neuron.

[70]  J. Hildebrand,et al.  Serotonin-immunoreactive neurons in the median protocerebrum and suboesophageal ganglion of the sphinx moth Manduca sexta , 1989, Cell and Tissue Research.

[71]  R. Kanzaki,et al.  Morphological and physiological properties of pheromone-triggered flipflopping descending interneurons of the male silkworm moth, Bombyx mori , 1994, Journal of Comparative Physiology A.

[72]  Stefan Schöneich,et al.  Neuronal organization of a fast‐mediating cephalothoracic pathway for antennal‐tactile information in the cricket (Gryllus bimaculatus DeGeer) , 2011, The Journal of comparative neurology.

[73]  H. Numata,et al.  Neurons projecting to the retrocerebral complex of the adult blow fly, Protophormia terraenovae , 2000, Cell and Tissue Research.

[74]  E. Staudacher,et al.  Gating of sensory responses of descending brain neurones during walking in crickets , 1998 .

[75]  J. Hounsgaard,et al.  Stereological Estimate of the Total Number of Neurons in Spinal Segment D9 of the Red-Eared Turtle , 2011, The Journal of Neuroscience.

[76]  J Kien,et al.  Preparation and execution of movement: parallels between insect and mammalian motor systems. , 1992, Comparative biochemistry and physiology. Comparative physiology.

[77]  R. Mann,et al.  Lineage and Birth Date Specify Motor Neuron Targeting and Dendritic Architecture in Adult Drosophila , 2009, The Journal of Neuroscience.

[78]  Nicholas J. Strausfeld,et al.  Descending pathways connecting the male-specific visual system of flies to the neck and flight motor , 1991, Journal of Comparative Physiology A.

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

[80]  Barry J. Dickson,et al.  Neuronal Control of Drosophila Walking Direction , 2014, Science.

[81]  Organisation of intersegmental interneurons in the suboesophageal ganglion of Schistocerca gregaria (Forksal) and Locusta migratoria migratorioides (Reiche & Fairmaire) (Acrididae, Orthoptera , 1990 .

[82]  D. Nässel Serotonin and serotonin-immunoreactive neurons in the nervous system of insects , 1988, Progress in Neurobiology.

[83]  Kei Ito,et al.  Systematic analysis of the visual projection neurons of Drosophila melanogaster. I. Lobula‐specific pathways , 2006, The Journal of comparative neurology.

[84]  Ryohei Kanzaki,et al.  Neural control mechanisms of the pheromone‐triggered programmed behavior in male silkmoths revealed by double‐labeling of descending interneurons and a motor neuron , 2005, The Journal of comparative neurology.

[85]  D. Nässel,et al.  Factors that regulate insulin producing cells and their output in Drosophila , 2013, Front. Physiol..

[86]  Gilles Laurent,et al.  Evaluating a Genetically Encoded Optical Sensor of Neural Activity Using Electrophysiology in Intact Adult Fruit Flies , 2007, Frontiers in neural circuits.

[87]  E. Marder Neuromodulation of Neuronal Circuits: Back to the Future , 2012, Neuron.

[88]  S. Blackband,et al.  Visualization of synaptic domains in the Drosophila brain by magnetic resonance microscopy at 10 micron isotropic resolution , 2015, Scientific Reports.

[89]  Michael O'Shea,et al.  The Anatomy of a Locust Visual Interneurone; the Descending Contralateral Movement Detector , 1974 .

[90]  P. Salvaterra,et al.  Localization of choline acetyltransferase‐expressing neurons in Drosophila nervous system , 1999, Microscopy research and technique.

[91]  Gilles Laurent,et al.  Transformation of Olfactory Representations in the Drosophila Antennal Lobe , 2004, Science.

[92]  E. Staudacher Distribution and morphology of descending brain neurons in the cricket Gryllus bimaculatus , 1998, Cell and Tissue Research.

[93]  D. Sattelle,et al.  Pharmacology of insect GABA receptors , 1991, Neurochemical Research.