Organization of antennal lobe‐associated neurons in adult Drosophila melanogaster brain

The primary olfactory centers of both vertebrates and insects are characterized by glomerular structure. Each glomerulus receives sensory input from a specific type of olfactory sensory neurons, creating a topographic map of the odor quality. The primary olfactory center is also innervated by various types of neurons such as local neurons, output projection neurons (PNs), and centrifugal neurons from higher brain regions. Although recent studies have revealed how olfactory sensory input is conveyed to each glomerulus, it still remains unclear how the information is integrated and conveyed to other brain areas. By using the GAL4 enhancer‐trap system, we conducted a systematic mapping of the neurons associated with the primary olfactory center of Drosophila, the antennal lobe (AL). We identified in total 29 types of neurons, among which 13 are newly identified in the present study. Analyses of arborizations of these neurons in the AL revealed how glomeruli are linked with each other, how different PNs link these glomeruli with multiple secondary sites, and how these secondary sites are organized by the projections of the AL‐associated neurons. J. Comp. Neurol. 520:4067–4130, 2012. © 2012 Wiley Periodicals, Inc.

[1]  J. Boeckh,et al.  Connections between the deutocerebrum and the protocerebrum, and neuroanatomy of several classes of deutocerebral projection neurons in the brain of male Periplaneta americana , 1993, The Journal of comparative neurology.

[2]  R. Menzel,et al.  The glomerular code for odor representation is species specific in the honeybee Apis mellifera , 1999, Nature Neuroscience.

[3]  A. Chess,et al.  Identification of candidate Drosophila olfactory receptors from genomic DNA sequence. , 1999, Genomics.

[4]  D. Kvitsiani,et al.  Neural Circuitry that Governs Drosophila Male Courtship Behavior , 2005, Cell.

[5]  N. Strausfeld,et al.  Multimodal efferent and recurrent neurons in the medial lobes of cockroach mushroom bodies , 1999, The Journal of comparative neurology.

[6]  J. Isaacson,et al.  Intraglomerular inhibition: signaling mechanisms of an olfactory microcircuit , 2005, Nature Neuroscience.

[7]  Liqun Luo,et al.  Mosaic Analysis with a Repressible Cell Marker for Studies of Gene Function in Neuronal Morphogenesis , 1999, Neuron.

[8]  C. Löfstedt,et al.  Functional specialization of olfactory glomeruli in a moth. , 1992, Science.

[9]  D. Malun,et al.  Inventory and distribution of synapses of identified uniglomerular projection neurons in the antennal lobe of Periplaneta americana , 1991, The Journal of comparative neurology.

[10]  Gero Miesenböck,et al.  Transmission of Olfactory Information between Three Populations of Neurons in the Antennal Lobe of the Fly , 2002, Neuron.

[11]  Liqun Luo,et al.  Target neuron prespecification in the olfactory map of Drosophila , 2001, Nature.

[12]  M. Heisenberg.  Mushroom body memoir: from maps to models , 2003, Nature Reviews Neuroscience.

[13]  M. Stopfer,et al.  Dye fills reveal additional olfactory tracts in the protocerebrum of wild‐type Drosophila , 2012, The Journal of comparative neurology.

[14]  John R. Carlson,et al.  Coding of Odors by a Receptor Repertoire , 2006, Cell.

[15]  J. Isaacson,et al.  Olfactory Reciprocal Synapses: Dendritic Signaling in the CNS , 1998, Neuron.

[16]  R. Menzel,et al.  Differential parallel processing of olfactory information in the honeybee, Apis mellifera L. , 2002, Journal of Comparative Physiology A.

[17]  Wolfgang Rössler,et al.  Organization of the olfactory pathway and odor processing in the antennal lobe of the ant Camponotus floridanus , 2008, The Journal of comparative neurology.

[18]  L. C. Katz,et al.  Optical Imaging of Odorant Representations in the Mammalian Olfactory Bulb , 1999, Neuron.

[19]  S. Spencer,et al.  Epitope-specific binding of CD8 regulates activation of T cells and induction of cytotoxicity. , 1990, International immunology.

[20]  John R. Carlson,et al.  Receptors and Neurons for Fly Odors in Drosophila , 2007, Current Biology.

[21]  S. Shanbhag,et al.  Fine structure and primary sensory projections of sensilla located in the sacculus of the antenna of Drosophila melanogaster , 1995, Cell and Tissue Research.

[22]  Barry J. Dickson,et al.  The Drosophila pheromone cVA activates a sexually dimorphic neural circuit , 2008, Nature.

[23]  Kei Ito,et al.  Clonal analysis of Drosophila antennal lobe neurons: diverse neuronal architectures in the lateral neuroblast lineage , 2008, Development.

[24]  S. Benzer,et al.  Behavioral genetics of thermosensation and hygrosensation in Drosophila. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[25]  Pavan Ramdya,et al.  Complementary Function and Integrated Wiring of the Evolutionarily Distinct Drosophila Olfactory Subsystems , 2011, The Journal of Neuroscience.

[26]  J. Hildebrand,et al.  Anatomy of antenno-cerebral pathways in the brain of the sphinx moth Manduca sexta , 1988, Cell and Tissue Research.

[27]  Matthias Landgraf,et al.  Metamorphosis of an identified serotonergic neuron in the Drosophila olfactory system , 2007, Neural Development.

[28]  N. Perrimon,et al.  A genetic screen for mutations that disrupt an auditory response in Drosophila melanogaster. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[29]  D. Müller,et al.  Anatomical organization of antennal lobe projection neurons in the moth Heliothis virescens , 2007, The Journal of comparative neurology.

[30]  David J. Anderson,et al.  A single population of olfactory sensory neurons mediates an innate avoidance behaviour in Drosophila , 2004, Nature.

[31]  Kei Ito,et al.  Integration of Chemosensory Pathways in the Drosophila Second-Order Olfactory Centers , 2004, Current Biology.

[32]  Leslie B. Vosshall,et al.  Or83b Encodes a Broadly Expressed Odorant Receptor Essential for Drosophila Olfaction , 2004, Neuron.

[33]  K. Fischbach,et al.  The optic lobe of Drosophila melanogaster. I. A Golgi analysis of wild-type structure , 1989, Cell and Tissue Research.

[34]  Andrey Rzhetsky,et al.  A Chemosensory Gene Family Encoding Candidate Gustatory and Olfactory Receptors in Drosophila , 2001, Cell.

[35]  K. Störtkuhl,et al.  Functional analysis of an olfactory receptor in Drosophila melanogaster , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[36]  P. Kloppenburg,et al.  Serotonin modulation of moth central olfactory neurons. , 2008, Annual review of entomology.

[37]  John R Carlson,et al.  The Molecular Basis of Odor Coding in the Drosophila Antenna , 2004, Cell.

[38]  G. Gisselmann,et al.  Functional expression and characterization of a Drosophila odorant receptor in a heterologous cell system , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[39]  R. Stocker,et al.  Cobalt filling of sensory projections from internal and external mouthparts in Drosophila , 2004, Cell and Tissue Research.

[40]  G. Miesenböck,et al.  Excitatory Local Circuits and Their Implications for Olfactory Processing in the Fly Antennal Lobe , 2007, Cell.

[41]  L. Luo,et al.  Representation of the Glomerular Olfactory Map in the Drosophila Brain , 2002, Cell.

[42]  Erich Buchner,et al.  [3H]2-Deoxyglucose mapping of odor-induced neuronal activity in the antennal lobes of Drosophila melanogaster , 1984, Brain Research.

[43]  R. Greenspan,et al.  Courtship in Drosophila. , 2003, Annual review of genetics.

[44]  Veronica Rodrigues.  Spatial coding of olfactory information in the antennal lobe of Drosophila melanogaster , 1988, Brain Research.

[45]  Kei Ito,et al.  Distribution, classification, and development ofDrosophila glial cells in the late embryonic and early larval ventral nerve cord , 1995, Roux's archives of developmental biology.

[46]  F. Schürmann,et al.  Separate Distribution of Deutocerebral Projection Neurons in the Mushroom Bodies of the Cricket Brain , 2004, Acta biologica Hungarica.

[47]  P. Salvaterra,et al.  Analysis of choline acetyltransferase protein in temperature sensitive mutant flies using newly generated monoclonal antibody , 1996, Neuroscience Research.

[48]  D. Yamamoto,et al.  Evolution of sexual dimorphism in the olfactory brain of Hawaiian Drosophila , 2003, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[49]  Ronald L. Davis,et al.  Olfactory Learning , 2004, Neuron.

[50]  Richard Axel,et al.  Spatial Representation of the Glomerular Map in the Drosophila Protocerebrum , 2002, Cell.

[51]  L. Luo,et al.  Comprehensive Maps of Drosophila Higher Olfactory Centers: Spatially Segregated Fruit and Pheromone Representation , 2007, Cell.

[52]  Kei Ito,et al.  Comprehensive classification of the auditory sensory projections in the brain of the fruit fly Drosophila melanogaster , 2006, The Journal of comparative neurology.

[53]  T. Tanimura,et al.  External morphology of sensilla in the sacculus of an antennal flagellum of the fruit fly Drosophila melanogaster Meigen (Diptera : Drosophilidae) , 1991 .

[54]  Leslie B. Vosshall,et al.  Variant Ionotropic Glutamate Receptors as Chemosensory Receptors in Drosophila , 2009, Cell.

[55]  J. Hildebrand,et al.  Ramification pattern and ultrastructural characteristics of the serotonin‐immunoreactive neuron in the antennal lobe of the moth Manduca sexta: A laser scanning confocal and electron microscopic study , 1993, The Journal of comparative neurology.

[56]  John R Carlson,et al.  Chemosensory Coding by Neurons in the Coeloconic Sensilla of the Drosophila Antenna , 2005, The Journal of Neuroscience.

[57]  Kei Ito,et al.  Flybrain neuron database: A comprehensive database system of the Drosophila brain neurons , 2011, The Journal of comparative neurology.

[58]  N. Strausfeld,et al.  Comparison of octopamine‐like immunoreactivity in the brains of the fruit fly and blow fly , 2006, The Journal of comparative neurology.

[59]  R. Stocker,et al.  Neuroblast ablation in Drosophila P[GAL4] lines reveals origins of olfactory interneurons. , 1997, Journal of neurobiology.

[60]  Keita Endo,et al.  Notch signal organizes the Drosophila olfactory circuitry by diversifying the sensory neuronal lineages , 2007, Nature Neuroscience.

[61]  Leslie B. Vosshall,et al.  Genetic and Functional Subdivision of the Drosophila Antennal Lobe , 2005, Current Biology.

[62]  M. E. Power.  The antennal centers and their connections within the brain of Drosophila melanogaster , 1946, The Journal of comparative neurology.

[63]  S. Nakanishi,et al.  Refinement of odor molecule tuning by dendrodendritic synaptic inhibition in the olfactory bulb. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[64]  Mosaic Analysis with a Repressible Neurotechnique Cell Marker for Studies of Gene Function in Neuronal Morphogenesis , 1999 .

[65]  S. Zipursky,et al.  Afferent Induction of Olfactory Glomeruli Requires N-Cadherin , 2004, Neuron.

[66]  Kei Ito,et al.  Gamma‐aminobutyric acid (GABA)‐mediated neural connections in the Drosophila antennal lobe , 2009, The Journal of comparative neurology.

[67]  W. Gronenberg.  Subdivisions of hymenopteran mushroom body calyces by their afferent supply , 2001, The Journal of comparative neurology.

[68]  Kei Ito,et al.  Neural architecture of the primary gustatory center of Drosophila melanogaster visualized with GAL4 and LexA enhancer‐trap systems , 2010, The Journal of comparative neurology.

[69]  Kei Ito,et al.  Activity-Dependent Plasticity in an Olfactory Circuit , 2007, Neuron.

[70]  Richard Axel,et al.  Visualizing an Olfactory Sensory Map , 1996, Cell.

[71]  Kei Ito,et al.  Mushroom bodies are not required for courtship behavior by normal and sexually mosaic Drosophila. , 2002, Journal of neurobiology.

[72]  L. Luo,et al.  Diversity and Wiring Variability of Olfactory Local Interneurons in the Drosophila Antennal Lobe , 2010, Nature Neuroscience.

[73]  N. Strausfeld,et al.  The organization of extrinsic neurons and their implications in the functional roles of the mushroom bodies in Drosophila melanogaster Meigen. , 1998, Learning & memory.

[74]  John R. Carlson,et al.  A Novel Family of Divergent Seven-Transmembrane Proteins Candidate Odorant Receptors in Drosophila , 1999, Neuron.

[75]  M. Heisenberg,et al.  Dopamine and Octopamine Differentiate between Aversive and Appetitive Olfactory Memories in Drosophila , 2003, The Journal of Neuroscience.

[76]  N. Strausfeld,et al.  Organization of olfactory and multimodal afferent neurons supplying the calyx and pedunculus of the cockroach mushroom bodies , 1999, The Journal of comparative neurology.

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

[78]  P. Hiesinger,et al.  Three‐dimensional reconstruction of the antennal lobe in Drosophila melanogaster , 1999, The Journal of comparative neurology.

[79]  D. Nässel,et al.  Pigment-dispersing hormone-immunoreactive neurons and their relation to serotonergic neurons in the blowfly and cockroach visual system , 1991, Cell and Tissue Research.

[80]  John R. Carlson,et al.  Odor Coding in the Drosophila Antenna , 2001, Neuron.

[81]  Kei Ito,et al.  Odor-Evoked Neural Oscillations in Drosophila Are Mediated by Widely Branching Interneurons , 2009, The Journal of Neuroscience.

[82]  Kei Ito,et al.  Neuronal assemblies of the Drosophila mushroom body , 2008, The Journal of comparative neurology.

[83]  A. Borst,et al.  Neuronal architecture of the antennal lobe in Drosophila melanogaster , 1990, Cell and Tissue Research.

[84]  Richard Axel,et al.  An Olfactory Sensory Map in the Fly Brain , 2000, Cell.

[85]  P. Mobbs.  The Brain of the Honeybee Apis Mellifera. I. The Connections and Spatial Organization of the Mushroom Bodies , 1982 .

[86]  Stefan R. Pulver,et al.  An internal thermal sensor controlling temperature preference in Drosophila , 2008, Nature.

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

[88]  Stephan J. Sigrist,et al.  Bruchpilot, a Protein with Homology to ELKS/CAST, Is Required for Structural Integrity and Function of Synaptic Active Zones in Drosophila , 2006, Neuron.

[89]  Dual-labeling method for electron microscopy to characterize synaptic connectivity using genetically encoded fluorescent reporters in Drosophila , 2011, Journal of Neuroscience Methods.

[90]  Barry J. Dickson,et al.  Molecular, Anatomical, and Functional Organization of the Drosophila Olfactory System , 2005, Current Biology.

[91]  Shubha V. Nayak,et al.  Primary sensory projections from the labella to the brain of Drosophila melanogaster Meigen (Diptera : Drosophilidae) , 1985 .

[92]  Sebastian Kirschner,et al.  Dual olfactory pathway in the honeybee, Apis mellifera , 2006, The Journal of comparative neurology.

[93]  J. Hildebrand,et al.  Synaptic organization of the uniglomerular projection neurons of the antennal lobe of the moth Manduca sexta: A laser scanning confocal and electron microscopic study , 1997, The Journal of comparative neurology.

[94]  C Giovanni Galizia,et al.  Parallel olfactory systems in insects: anatomy and function. , 2010, Annual review of entomology.

[95]  R. Menzel,et al.  Structure and response patterns of olfactory interneurons in the honeybee, Apis mellifera , 2001, The Journal of comparative neurology.

[96]  Kouji Yasuyama,et al.  Localization of choline acetyltransferase-expressing neurons in the larval visual system of Drosophila melanogaster. , 1995 .

[97]  G. Laurent.  A systems perspective on early olfactory coding. , 1999, Science.

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

[99]  Kristin Scott,et al.  Taste Representations in the Drosophila Brain , 2004, Cell.

[100]  G. Shepherd,et al.  Mechanisms of olfactory discrimination: converging evidence for common principles across phyla. , 1997, Annual review of neuroscience.

[101]  Charles S. Zuker,et al.  The Coding of Temperature in the Drosophila Brain , 2011, Cell.

[102]  Guan-Yu Chen,et al.  Three-Dimensional Reconstruction of Brain-wide Wiring Networks in Drosophila at Single-Cell Resolution , 2011, Current Biology.

[103]  Shigeo Hayashi,et al.  GETDB, a database compiling expression patterns and molecular locations of a collection of gal4 enhancer traps , 2002, Genesis.

[104]  N. Perrimon,et al.  Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. , 1993, Development.

[105]  R. Ignell.  Monoamines and neuropeptides in antennal lobe interneurons of the desert locust, Schistocerca gregaria: an immunocytochemical study , 2001, Cell and Tissue Research.

[106]  N. Schoppa,et al.  Synchronization of Olfactory Bulb Mitral Cells by Precisely Timed Inhibitory Inputs , 2006, Neuron.

[107]  M. Hammer,et al.  Multiple sites of associative odor learning as revealed by local brain microinjections of octopamine in honeybees. , 1998, Learning & memory.

[108]  Glenn C. Turner,et al.  Oscillations and Sparsening of Odor Representations in the Mushroom Body , 2002, Science.

[109]  V. Jayaraman,et al.  Intensity versus Identity Coding in an Olfactory System , 2003, Neuron.

[110]  Uwe Homberg,et al.  Antennal Lobe Structure , 1999 .

[111]  Gordon M. Shepherd,et al.  The Olfactory Bulb , 1988 .

[112]  M. Kasei.  Distribution, classification, and development of Drosophila glial cells in the late embryonic and early larval ventral nerve cord , 1995 .

[113]  S. Sachse,et al.  The spatial representation of chemical structures in the antennal lobe of honeybees: steps towards the olfactory code , 1999, The European journal of neuroscience.

[114]  H. Amrein,et al.  Taste Perception and Coding in Drosophila , 2004, Current Biology.

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

[116]  Naoshige Uchida,et al.  Odor maps in the mammalian olfactory bulb: domain organization and odorant structural features , 2000, Nature Neuroscience.

[117]  Reinhard F. Stocker,et al.  The organization of the chemosensory system in Drosophila melanogaster: a rewiew , 2004, Cell and Tissue Research.

[118]  L C Katz,et al.  Symmetry, Stereotypy, and Topography of Odorant Representations in Mouse Olfactory Bulbs , 2001, The Journal of Neuroscience.

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

[120]  Linda B. Buck,et al.  Information coding in the olfactory system: Evidence for a stereotyped and highly organized epitope map in the olfactory bulb , 1994, Cell.