A resource for the Drosophila antennal lobe provided by the connectome of glomerulus VA1v

Using FIB-SEM we report the entire synaptic connectome of glomerulus VA1v of the right antennal lobe in Drosophila melanogaster. Within the glomerulus we densely reconstructed all neurons, including hitherto elusive local interneurons. The fruitless-positive, sexually dimorphic VA1v included >11,140 presynaptic sites with ~38,050 postsynaptic dendrites. These connected input olfactory receptor neurons (ORNs, 51 ipsilateral, 56 contralateral), output projection neurons (18 PNs), and local interneurons (56 of >150 previously reported LNs). ORNs are predominantly presynaptic and PNs predominantly postsynaptic; newly reported LN circuits are largely an equal mixture and confer extensive synaptic reciprocity, except the newly reported LN2V with input from ORNs and outputs mostly to monoglomerular PNs, however. PNs were more numerous than previously reported from genetic screens, suggesting that the latter failed to reach saturation. We report a matrix of 192 bodies each having >50 connections; these form 88% of the glomerulus’ pre/postsynaptic sites.

[1]  L. Luo,et al.  Synaptic organization of the Drosophila antennal lobe and its regulation by the Teneurins , 2014, eLife.

[2]  Bill S Hansson,et al.  Digital in vivo 3D atlas of the antennal lobe of Drosophila melanogaster , 2015, The Journal of comparative neurology.

[3]  Daryl M. Gohl,et al.  Diverse populations of local interneurons integrate into the Drosophila adult olfactory circuit , 2018, Nature Communications.

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

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

[6]  I. Meinertzhagen,et al.  Immunocytochemical localization of synaptic proteins to photoreceptor synapses of Drosophila melanogaster , 2010, The Journal of comparative neurology.

[7]  S. Sachse,et al.  Physiological and morphological characterization of local interneurons in the Drosophila antennal lobe. , 2010, Journal of neurophysiology.

[8]  I. Meinertzhagen,et al.  Synaptic connections of cholinergic antennal lobe relay neurons innervating the lateral horn neuropile in the brain of Drosophila melanogaster , 2003, The Journal of comparative neurology.

[9]  Rachel I. Wilson,et al.  Origins of correlated activity in an olfactory circuit , 2009, Nature Neuroscience.

[10]  Louis K. Scheffer,et al.  Minimizing Manual Image Segmentation Turn-Around Time for Neuronal Reconstruction by Embracing Uncertainty , 2012, PloS one.

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

[12]  Louis K. Scheffer,et al.  Semi-automated reconstruction of neural circuits using electron microscopy , 2010, Current Opinion in Neurobiology.

[13]  P. Shannon,et al.  Cytoscape: a software environment for integrated models of biomolecular interaction networks. , 2003, Genome research.

[14]  Gaia Tavosanis,et al.  Synaptic organization in the adult Drosophila mushroom body calyx , 2009, The Journal of comparative neurology.

[15]  Jing W. Wang,et al.  Presynaptic peptidergic modulation of olfactory receptor neurons in Drosophila , 2009, Proceedings of the National Academy of Sciences.

[16]  Zhiyuan Lu,et al.  Different classes of input and output neurons reveal new features in microglomeruli of the adult Drosophila mushroom body calyx , 2012, The Journal of comparative neurology.

[17]  Rachel I. Wilson,et al.  Glutamate is an inhibitory neurotransmitter in the Drosophila olfactory system , 2013, Proceedings of the National Academy of Sciences.

[18]  Louis K. Scheffer,et al.  Large-scale EM Analysis of the Drosophila Antennal Lobe with Automatically Computed Synapse Point Clouds , 2015, 1508.06232.

[19]  Rafael Cantera,et al.  Synaptic circuitry of identified neurons in the antennal lobe of Drosophila melanogaster , 2016, The Journal of comparative neurology.

[20]  B. Boycott,et al.  Organization of the primate retina: electron microscopy , 1966, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[21]  Anirban Chakraborty,et al.  A Context-aware Delayed Agglomeration Framework for EM Segmentation , 2014, ArXiv.

[22]  L. Luo,et al.  Lineage-specific effects of Notch/Numb signaling in post-embryonic development of the Drosophila brain , 2010, Development.

[23]  A Fröhlich,et al.  Freeze‐fracture study of an invertebrate multiple‐contact synapse: The fly photoreceptor tetrad , 1985, The Journal of comparative neurology.

[24]  C Giovanni Galizia,et al.  Processing of Odor Mixtures in the Drosophila Antennal Lobe Reveals both Global Inhibition and Glomerulus-Specific Interactions , 2007, The Journal of Neuroscience.

[25]  Louis K. Scheffer,et al.  Toward large-scale connectome reconstructions , 2014, Current Opinion in Neurobiology.

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

[27]  M. V. Bennett,et al.  Gap junctions, electrotonic coupling, and intercellular communication. , 1978, Neurosciences Research Program bulletin.

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

[29]  G. Knott,et al.  Serial Section Scanning Electron Microscopy of Adult Brain Tissue Using Focused Ion Beam Milling , 2008, The Journal of Neuroscience.

[30]  Anirban Chakraborty,et al.  A Context-Aware Delayed Agglomeration Framework for Electron Microscopy Segmentation , 2014, PloS one.

[31]  I. Meinertzhagen,et al.  The genetic analysis of functional connectomics in Drosophila. , 2012, Advances in genetics.

[32]  A. Chess,et al.  Convergent projections of Drosophila olfactory neurons to specific glomeruli in the antennal lobe , 2000, Nature Neuroscience.

[33]  I. Meinertzhagen,et al.  Synaptic organization of the mushroom body calyx in Drosophila melanogaster , 2002, The Journal of comparative neurology.

[34]  Shin-ya Takemura,et al.  Synaptic circuits of the Drosophila optic lobe: The input terminals to the medulla , 2008, The Journal of comparative neurology.

[35]  Bill S Hansson,et al.  Elucidating the Neuronal Architecture of Olfactory Glomeruli in the Drosophila Antennal Lobe. , 2016, Cell reports.

[36]  S. Sachse,et al.  Calcium imaging revealed no modulatory effect on odor-evoked responses of the Drosophila antennal lobe by two populations of inhibitory local interneurons , 2017, Scientific Reports.

[37]  M. Heisenberg,et al.  Isolation of Anatomical Brain Mutants of Drosophila by Histological Means , 1979 .

[38]  Shin-ya Takemura,et al.  From Form to Function: the Ways to Know a Neuron , 2009, Journal of neurogenetics.

[39]  Gary B. Huang,et al.  Identifying Synapses Using Deep and Wide Multiscale Recursive Networks , 2014, ArXiv.

[40]  Fred A. Hamprecht,et al.  Automated Detection and Segmentation of Synaptic Contacts in Nearly Isotropic Serial Electron Microscopy Images , 2011, PloS one.

[41]  Julie H. Simpson,et al.  Genetic Manipulation of Genes and Cells in the Nervous System of the Fruit Fly , 2011, Neuron.

[42]  Yisheng He,et al.  A Complete Developmental Sequence of a Drosophila Neuronal Lineage as Revealed by Twin-Spot MARCM , 2010, PLoS biology.

[43]  R. Stocker,et al.  Projection patterns of different types of antennal sensilla in the antennal glomeruli of Drosophila melanogaster , 2004, Cell and Tissue Research.

[44]  Louis K. Scheffer,et al.  Synaptic circuits and their variations within different columns in the visual system of Drosophila , 2015, Proceedings of the National Academy of Sciences.

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

[46]  William F Tobin,et al.  Wiring variations that enable and constrain neural computation in a sensory microcircuit , 2017, bioRxiv.

[47]  G M Shepherd,et al.  Dendrodendritic synaptic pathway for inhibition in the olfactory bulb. , 1966, Experimental neurology.

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

[49]  I. Meinertzhagen,et al.  Synaptic organization of columnar elements in the lamina of the wild type in Drosophila melanogaster , 1991, The Journal of comparative neurology.

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

[51]  Srdjan D Antic,et al.  Voltage imaging to understand connections and functions of neuronal circuits. , 2016, Journal of neurophysiology.

[52]  I. Meinertzhagen,et al.  Synaptic organization in the fly's optic lamina: few cells, many synapses and divergent microcircuits. , 2001, Progress in brain research.

[53]  Kei Ito,et al.  Organization of antennal lobe‐associated neurons in adult Drosophila melanogaster brain , 2012, The Journal of comparative neurology.

[54]  J. Rybak,et al.  Synaptic Spinules in the Olfactory Circuit of Drosophila melanogaster , 2018, Front. Cell. Neurosci..

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

[56]  G. Shepherd The Synaptic Organization of the Brain , 1979 .

[57]  M. Koganezawa,et al.  Select interneuron clusters determine female sexual receptivity in Drosophila , 2013, Nature Communications.

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

[59]  Zhiyuan Lu,et al.  The CNS connectome of a tadpole larva of Ciona intestinalis (L.) highlights sidedness in the brain of a chordate sibling , 2016, eLife.

[60]  L. Vosshall,et al.  Molecular architecture of smell and taste in Drosophila. , 2007, Annual review of neuroscience.

[61]  Raoul LePage Heavy-Tailed Distributions , 2011, International Encyclopedia of Statistical Science.

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

[63]  T. Moriizumi,et al.  Stereological quantification of olfactory receptor neurons in mice , 2014, Neuroscience.

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

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

[66]  K. Hayworth,et al.  Enhanced FIB-SEM systems for large-volume 3D imaging , 2017, eLife.

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

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

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

[70]  J. Sanes,et al.  Ome sweet ome: what can the genome tell us about the connectome? , 2008, Current Opinion in Neurobiology.

[71]  Louis K. Scheffer,et al.  A connectome of a learning and memory center in the adult Drosophila brain , 2017, eLife.

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

[73]  I. Meinertzhagen Of what use is connectomics? A personal perspective on the Drosophila connectome , 2018, Journal of Experimental Biology.

[74]  Dhruv Grover,et al.  Flyception: imaging brain activity in freely walking fruit flies , 2016, Nature Methods.

[75]  H. Reichert,et al.  Identification and analysis of a glutamatergic local interneuron lineage in the adult Drosophila olfactory system , 2011, Neural systems & circuits.

[76]  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.

[77]  James M. Jeanne,et al.  Convergence, Divergence, and Reconvergence in a Feedforward Network Improves Neural Speed and Accuracy , 2015, Neuron.

[78]  J. Royet,et al.  Morphometric study of the glomerular population in the mouse olfactory bulb: Numerical density and size distribution along the rostrocaudal axis , 1988, The Journal of comparative neurology.

[79]  Rachel I. Wilson Early olfactory processing in Drosophila: mechanisms and principles. , 2013, Annual review of neuroscience.

[80]  Lin Tian,et al.  Neural activity imaging with genetically encoded calcium indicators. , 2012, Progress in brain research.

[81]  Silke Sachse,et al.  Olfactory Preference for Egg Laying on Citrus Substrates in Drosophila , 2013, Current Biology.

[82]  B. Dickson,et al.  A single class of olfactory neurons mediates behavioural responses to a Drosophila sex pheromone , 2007, Nature.

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