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Olfactory Systems in Insects: Similarities and Differences Between Species

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Olfactory Concepts of Insect Control - Alternative to insecticides

Abstract

Many insects rely on their sense of smell to identify food, prey or mates. Odors are detected by the sensory organs and the resulting signals processed by the brains before they can lead to behaviors. A large body of research spanning several decades has generated a wealth of information about olfactory coding and the underlying olfactory systems in many different species of insects. While many features of the olfactory systems are highly conserved, remarkable differences are also found between different insect species. Here we provide a detailed comparison of the molecular, anatomical, and physiological parameters of olfactory systems across species including flies, moths, bees and mosquitoes. We focus on the first three layers of the olfactory system, namely the antenna, the antennal lobe, and the mushroom body. The comparative analysis provides a useful foundation for understanding the role of specific features of olfactory systems in odor coding.

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References

  • Abel R, Rybak J, Menzel R (2001) Structure and response patterns of olfactory interneurons in the honeybee, Apis mellifera. J Comp Neurol 437:363–383

    Article  CAS  PubMed  Google Scholar 

  • Abraham D, Löfstedt C, Picimbon JF (2005) Molecular characterization and evolution of pheromone binding protein genes in Agrotis moths. Insect Biochem Mol Biol 35:1100–1111

    Article  CAS  PubMed  Google Scholar 

  • Abuin L, Bargeton B, Ulbrich MH, Isacoff EY, Kellenberger S, Benton R (2011) Functional architecture of olfactory ionotropic glutamate receptors. Neuron 69:44–60

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ai H, Okada K, Hill ES, Kanzaki R (1998) Spatio-temporal activities in the antennal lobe analyzed by an optical recording method in the male silkworm moth Bombyx mori. Neurosci Lett 258:135–138

    Article  CAS  PubMed  Google Scholar 

  • Andersson MN, Löfstedt C, Newcomb RD (2015) Insect olfaction and the evolution of receptor tuning. Front Ecol Evol 3:1–14

    Google Scholar 

  • Anton S, Hansson BS (1994) Central processing of sex pheromone, host odour, and oviposition deterrent information by interneurons in the antennal lobe of female Spodoptera littoralis (Lepidoptera: Noctuidae). J Comp Neurol 350:199–214

    Article  CAS  PubMed  Google Scholar 

  • Anton S, Homberg U (1999) Antennal lobe structure. In: Hansson BS (ed) Insect olfaction. Springer, Berlin, pp 97–124

    Chapter  Google Scholar 

  • Anton S, Ignell R, Hansson BS (2002) Developmental changes in the structure and function of the central olfactory system in gregarious and solitary desert locusts. Microsc Res Tech 56:281–291

    Article  PubMed  Google Scholar 

  • Arnold G, Masson C, Budharugsa S (1984) Demonstration of a sexual dimorphism in the olfactory pathways of the drones of Apis mellifica L. (Hymenoptera, Apidae). Experientia 40:723–725

    Article  Google Scholar 

  • Aso Y, Hattori D, Yu Y, Johnston RM, Iyer NA, Ngo TT, Dionne H, Abbott L, Axel R, Tanimoto H, Rubin GM (2014) The neuronal architecture of the mushroom body provides a logic for associative learning. elife 3:1–47

    Google Scholar 

  • Benton R, Sachse S, Michnick SW, Vosshall LB (2006) Atypical membrane topology and heteromeric function of Drosophila odorant receptors in vivo. PLoS Biol 4:e20

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bicker G, Schäfer S, Kingan TG (1985) Mushroom body feedback interneurones in the honeybee show GABA-like immunoreactivity. Brain Res 360:394–397

    Article  CAS  PubMed  Google Scholar 

  • Bicker G, Kreissl S, Hofbauer A (1993) Monoclonal antibody labels olfactory and visual pathways in Drosophila and Apis brains. J Comp Neurol 335:413–424

    Article  CAS  PubMed  Google Scholar 

  • Boeckh J, Ernst KD (1987) Contribution of single unit analysis in insects to an understanding of olfactory function. J Comp Physiol A 161:549–565

    Article  Google Scholar 

  • Boeckh J, Ernst KD, Sass H, Waldow U (1984) Anatomical and physiological characteristics of individual neurons in the central antennal pathways of insects. J Insect Physiol 30:15–26

    Article  Google Scholar 

  • Bohbot JD, Pitts RJ (2015) The narrowing olfactory landscape of insect odorant receptors. Front Ecol Evol 3:1–10

    Article  Google Scholar 

  • Bornhauser BC, Meyer EP (1997) Histamine-like immunoreactivity in the visual system and brain of an orthopteran and a hymenopteran insect. Cell Tissue Res 287:211–221

    Article  CAS  PubMed  Google Scholar 

  • Brandt ME (1876) Anatomical and morphological researches on the nervous system of Hymenopterous insects. J Nat Hist Ser 4(18):504–506

    Google Scholar 

  • Buchner E (1991) Genes expressed in the adult brain of Drosophila and effects of their mutations on behavior: a survey of transmitter- and second messenger-related genes. J Neurogenet 7:153–192

    Article  CAS  PubMed  Google Scholar 

  • Carey AF, Wang G, Su C, Zwiebel LJ, Carlson JR (2010) Odorant reception in the malaria mosquito Anopheles gambiae. Nature 464:66–71

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cayre M, Buckingham SD, Strambi A, Strambi C, Sattelle DB (1998) Adult insect mushroom body neurons in primary culture: cell morphology and characterization of potassium channels. Cell Tissue Res 291:537–547

    Article  CAS  PubMed  Google Scholar 

  • Chou YH, Spletter ML, Yaksi E, Leong JCS, Wilson RI, Luo L (2010) Diversity and wiring variability of olfactory local interneurons in the Drosophila antennal lobe. Nat Neurosci 13:439–449

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Christensen TA, Waldrop BR, Harrow ID, Hildebrand JG (1993) Local interneurons and information processing in the olfactory glomeruli of the moth Manduca sexta. J Comp Physiol A 173:385–399

    Article  CAS  PubMed  Google Scholar 

  • Christensen TA, Waldrop BR, Hildebrand JG (1998) Multitasking in the olfactory system: context-dependent responses to odors reveal dual GABA-regulated coding mechanisms in single olfactory projection neurons. J Neurosci 18:5999–6008

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Crittenden JR, Skoulakis EM, Han KA, Kalderon D, Davis RL (1998) Tripartite mushroom body architecture revealed by antigenic markers. Learn Mem 5:38–51

    CAS  PubMed  PubMed Central  Google Scholar 

  • Croset V, Rytz R, Cummins SF, Budd A, Brawand D, Kaessmann H, Gibson TJ, Benton R (2010) Ancient protostome origin of chemosensory ionotropic glutamate receptors and the evolution of insect taste and olfaction. PLoS Genet 6:e1001064

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dacks AM, Christensen TA, Hildebrand JG (2006) Phylogeny of a serotonin-immunoreactive neuron in the primary olfactory center of the insect brain. J Comp Neurol 498:727–746

    Article  CAS  PubMed  Google Scholar 

  • Demmer H, Kloppenburg P (2009) Intrinsic membrane properties and inhibitory synaptic input of kenyon cells as mechanisms for sparse coding? J Neurophysiol 102:1538–1550

    Article  CAS  PubMed  Google Scholar 

  • Distler P (1989) Histochemical demonstration of GABA-like immunoreactivity in cobalt labeled neuron individuals in the insect olfactory pathway. Histochemistry 91:245–249

    Article  CAS  PubMed  Google Scholar 

  • Distler P (1990) GABA-immunohistochemistry as a label for identifying types of local interneurons and their synaptic contacts in the antennal lobes of the American cockroach. Histochemistry 93:617–626

    Article  CAS  PubMed  Google Scholar 

  • Ernst KD, Boeckh J (1983) A neuroanatomical study on the organization of the central antennal pathways in insects III. Neuroanatomical characterization of physiologically defined response types of deutocerebral neurons in Periplaneta americana. Cell Tissue Res 229:1–22

    Article  CAS  PubMed  Google Scholar 

  • Ernst KD, Boeckh J, Boeckh V (1977) A neuroanatomical study on the organization of the central antennal pathways in insects – II. Deutocerebral Connections in Locusta migratoria and Periplaneta americana. Cell Tissue Res 176:285–308

    Article  CAS  PubMed  Google Scholar 

  • Esslen J, Kaissling KE (1976) Zahl und verteilung antennaler sensillen bei der honigbiene (Apis mellifera L.). Zoomorphologie 83:227–251

    Article  Google Scholar 

  • Flögel JHL (1878) Über den einheitlichen bau des gehirns in den verschiedenen insektenordnungen. Z Wiss Zool 30:556–592

    Google Scholar 

  • Forêt S, Maleszka R (2006) Function and evolution of a gene family encoding odorant binding-like proteins in a social insect, the honey bee (Apis mellifera). Genome Res 16:1404–1413

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Galán RF, Weidert M, Menzel R, Herz AVM, Galizia CG (2006) Sensory memory for odors is encoded in spontaneous correlated activity between olfactory glomeruli. Neural Comput 18:10–25

    Article  PubMed  Google Scholar 

  • Galizia CG, Kimmerle B (2004) Physiological and morphological characterization of honeybee olfactory neurons combining electrophysiology, calcium imaging and confocal microscopy. J Comp Physiol A Sens Neural Behav Physiol 190:21–38

    Article  CAS  Google Scholar 

  • Ghaninia M, Hansson BS, Ignell R (2007) The antennal lobe of the African malaria mosquito, Anopheles gambiae – innervation and three-dimensional reconstruction. Arthropod Struct Dev 36:23–39

    Article  PubMed  Google Scholar 

  • Goll W (1967) Strukturuntersuchungen am gehirn von Formica. Z Morph Oekol Tiere 59:143–210

    Article  Google Scholar 

  • Goossen H (1948) Untersuchungen an gehirnen verschieden grosser, jeweils verwandter coleopteren-und Hymenopteren-Arten. Zool Jb, Abt Allg Zool U Physiol 62:1–64

    Google Scholar 

  • Grabe V, Strutz A, Baschwitz A, Hansson BS, Sachse S (2015) Digital in vivo 3D atlas of the antennal lobe of Drosophila melanogaster. J Comp Neurol 523:530–544

    Article  CAS  PubMed  Google Scholar 

  • Gu H (2006) Cholinergic synaptic transmission in adult Drosophila kenyon cells in situ. J Neurosci 26:265–272

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hallem EA, Carlson JR (2006) Coding of odors by a receptor repertoire. Cell 125:14–60

    Article  CAS  Google Scholar 

  • Hekmat-Scafe DS (2002) Genome-wide analysis of the odorant-binding protein gene family in Drosophila melanogaster. Genome Res 12:1357–1369

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hill CA, Fox AN, Pitts RJ, Kent LB, Tan PL, Chrystal MA, Cravchik A, Collins FH, Robertson HM, Zwiebel LJ (2002a) G protein-coupled receptors in Anopheles gambiae. Science 298:176–178

    Article  CAS  PubMed  Google Scholar 

  • Hill ES, Iwano M, Gatellier L, Kanzaki R (2002b) Morphology and physiology of the serotonin-immunoreactive putative antennal lobe feedback neuron in the male silkmoth Bombyx mori. Chem Senses 27:475–483

    Article  PubMed  Google Scholar 

  • Hinke W (1961) Das relative postembryonale wachstum der hirnteile von culex pipiens, drosophila melanogaster und drosophila-mutanten. Z Morphol Oekol Tiere 50:81–118

    Article  Google Scholar 

  • Homberg U, Hildebrand JG (1991) Histamine-immunoreactive neurons in the midbrain and suboesophageal ganglion of the sphinx moth Manduca sexta. J Comp Neurol 307:647–657

    Article  CAS  PubMed  Google Scholar 

  • Homberg U, Kingan TG, Hildebrand JG (1987) Immunocytochemistry of GABA in the brain and suboesophageal ganglion of Manduca sexta. Cell Tissue Res 248:1–24

    Article  CAS  PubMed  Google Scholar 

  • Homberg U, Montague RA, Hildebrand JG (1988) Anatomy of antenno-cerebral pathways in the brain of the sphinx moth Manduca sexta. Cell Tissue Res 254:255–281

    Article  CAS  PubMed  Google Scholar 

  • Homberg U, Christensen TA, Hildebrand JG (1989) Structure and function of the deutocerebrum in insects. Annu Rev Entomol 34:477–501

    Article  CAS  PubMed  Google Scholar 

  • Homberg U, Binkle U, Lehman HK, Vullings HGB, Eckert M, Rapus J, Hildebrand JG (1992) Octopamine-immunoreactive neurons in the brain of two insect species. Rhythm Neurons Netw 477

    Google Scholar 

  • Hoskins S, Homberg U, Kingan T, Christensen T, Hildebrand J (1986) Immunocytochemistry of GABA in the antennal lobes of the sphinx moth Manduca sexta. Cell Tissue Res 244:243–252

    Article  CAS  PubMed  Google Scholar 

  • Howse PE (1974) Design and function in the insect brain. In: Browne LB (ed) Experimental analysis of insect behaviour. Springer, Berlin, pp 180–194

    Chapter  Google Scholar 

  • Huang J, Zhang W, Qiao W, Hu A, Wang Z (2010) Functional connectivity and selective odor responses of excitatory local interneurons in Drosophila antennal lobe. Neuron 67:1021–1033

    Article  CAS  PubMed  Google Scholar 

  • Husch A, Paehler M, Fusca D, Paeger L, Kloppenburg P (2009) Calcium current diversity in physiologically different local interneuron types of the antennal lobe. J Neurosci 29:716–726

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ignell R, Dekker T, Ghaninia M, Hansson BS (2005) Neuronal architecture of the mosquito deutocerebrum. J Comp Neurol 493:207–240

    Article  PubMed  Google Scholar 

  • Jackson FR, Newby LM, Kulkarni SJ (1990) Drosophila GABAergic systems: sequence and expression of glutamic acid decarboxylase. J Neurochem 54:1068–1078

    Article  CAS  PubMed  Google Scholar 

  • Jortner RA, Farivar SS, Laurent G (2007) A simple connectivity scheme for sparse coding in an olfactory system. J Neurosci 27:1659–1669

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kanzaki R, Shibuya T (1983) Olfactory neural pathway and sexual pheromone responses in the deutocerebrum of the male silkworm moth, Bombyx mori (Lepidoptera: Bombycidae). Appl Entomol Zool 18:131–133

    Article  CAS  Google Scholar 

  • Kent KS, Hildebrand JG (1987) Cephalic sensory pathways in the central nervous system of larval manduca sexta (Lepidoptera: Sphingidae). Philos Trans R Soc B Biol Sci 315:1–36

    Article  CAS  Google Scholar 

  • Kenyon FC (1896a) The meaning and structure of the so-called “Mushroom Bodies” of the Hexapod Brain. Am Nat 30:643–650

    Article  Google Scholar 

  • Kenyon FC (1896b) The brain of the bee. A preliminary contribution to the morphology of the nervous system of the arthropoda. J Comp Neurol 6:133–210

    Article  Google Scholar 

  • Klemm N (1976) Histochemistry of putative transmitter substances in the insect brain. Prog Neurobiol 7:99–169

    Article  CAS  PubMed  Google Scholar 

  • Koenig C, Hirsh A, Bucks S, Klinner C, Vogel H, Shukla A, Mansfield JH, Morton B, Hansson BS, Grosse-Wilde E (2015) A reference gene set for chemosensory receptor genes of Manduca sexta. Insect Biochem Mol Biol 66:51–63

    Article  CAS  PubMed  Google Scholar 

  • Kreissl S, Bicker G (1989) Histochemistry of acetylcholinesterase and immunocytochemistry of an acetylcholine receptor-like antigen in the brain of the honeybee. J Comp Neurol 286:71–84

    Article  CAS  PubMed  Google Scholar 

  • Kreissl S, Eichmüller S, Bicker G, Rapus J, Eckert M (1994) Octopamine-like immunoreactivity in the brain and subesophageal ganglion of the honeybee. J Comp Neurol 348:583–595

    Article  CAS  PubMed  Google Scholar 

  • Krieger J, Gänβle H, Raming K, Breer H (1993) Odorant binding proteins of Heliothis virescens. Insect Biochem Mol Biol 23:449–456

    Article  CAS  PubMed  Google Scholar 

  • Krieger J, von Nickisch-Rosenegk E, Mameli M, Pelosi P, Breer H (1996) Binding proteins from the antennae of Bombyx mori. Insect Biochem Mol Biol 26:297–307

    Article  CAS  PubMed  Google Scholar 

  • Krieger J, Raming K, Dewer YME, Bette S, Conzelmann S, Breer H (2002) A divergent gene family encoding candidate olfactory receptors of the moth Heliothis virescens. Eur J Neurosci 16:619–628

    Article  PubMed  Google Scholar 

  • Krieger J, Grosse-Wilde E, Gohl T, Dewer YME, Raming K, Breer H (2004) Genes encoding candidate pheromone receptors in a moth (Heliothis virescens). Proc Natl Acad Sci 101:11845–11850

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Laissue PP, Reiter C, Hiesinger PR, Halter S, Fischbach KF, Stocker RF (1999) Three-dimensional reconstruction of the antennal lobe in Drosophila melanogaster. J Comp Neurol 405:543–552

    Article  CAS  PubMed  Google Scholar 

  • Laurent G, Davidowitz H (1994) Encoding of olfactory information with oscillating neural assemblies. Science 265:1872–1875

    Article  CAS  PubMed  Google Scholar 

  • Laurent G, Naraghi M (1994) Odorant-induced oscillations in the mushroom bodies of the locust. J Neurosci 14:2993–3004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Leiss F, Koper E, Hein I, Fouquet W, Lindner J, Sigrist S, Tavosanis G (2009) Characterization of dendritic spines in the Drosophila central nervous system. Dev Neurobiol 69:221–234

    Article  CAS  PubMed  Google Scholar 

  • Leitch B, Laurent G (1996) GABAergic synapses in the antennal lobe and mushroom body of the locust olfactory system. J Comp Neurol 372:487–514

    Article  CAS  PubMed  Google Scholar 

  • Lemon WC, Getz WM (1998) Responses of cockroach antennal lobe projection neurons to pulsatile olfactory stimuli. Ann N Y Acad Sci 855:517–520

    Article  CAS  PubMed  Google Scholar 

  • Li Y, Strausfeld NJ (1997) Morphology and sensory modality of mushroom body extrinsic neurons in the brain of the cockroach, Periplaneta americana. J Comp Neurol 387:631–650

    Article  CAS  PubMed  Google Scholar 

  • Liu X, Davis RL (2009) The GABAergic anterior paired lateral neuron suppresses and is suppressed by olfactory learning. Nat Neurosci 12:53–59

    Article  CAS  PubMed  Google Scholar 

  • Lutz EM, Tyrer NM (1987) Immunohistochemical localization of choline acetyltransferase in the central nervous system of the locust. Brain Res 407:173–179

    Article  CAS  PubMed  Google Scholar 

  • MacLeod K, Laurent G (1996) Distinct mechanisms for synchronization and temporal patterning of odor-encoding neural assemblies. Science 274:976–979

    Article  CAS  PubMed  Google Scholar 

  • Malun D (1991) Synaptic relationships between GABA-immunoreactive neurons and an identified uniglomerular projection neuron in the antennal lobe of Periplaneta americana: a double-labeling electron microscopic study. Histochemistry 96:197–207

    Article  CAS  PubMed  Google Scholar 

  • Masuda-Nakagawa LM, Ito K, Awasaki T, O’Kane CJ (2014) A single GABAergic neuron mediates feedback of odor-evoked signals in the mushroom body of larval Drosophila. Front Neural Circuits 8:35

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mizunami M, Okada R, Li Y, Strausfeld NJ (1998a) Mushroom bodies of the cockroach: activity and identities of neurons recorded in freely moving animals. J Comp Neurol 402:501–519

    Article  CAS  PubMed  Google Scholar 

  • Mizunami M, Iwasaki M, Okada R, Nishikawa M (1998b) Topography of four classes of kenyon cells in the mushroom bodies of the cockroach. J Comp Neurol 399:162–175

    Article  CAS  PubMed  Google Scholar 

  • Mobbs PG (1982) The brain of the honeybee Apis mellifera. I. The connections and spatial organization of the mushroom bodies. Philos Trans R Soc B Biol Sci 298:309–354

    Article  Google Scholar 

  • Nässel DR (1988) Serotonin and serotonin-immunoreactive neurons in the nervous system of insects. Prog Neurobiol 30:1–85

    Article  PubMed  Google Scholar 

  • Nässel DR, Elekes K (1992) Aminergic neurons in the brain of blowflies and Drosophila: dopamine- and tyrosine hydroxylase-immunoreactive neurons and their relationship with putative histaminergic neurons. Cell Tissue Res 267:147–167

    Article  PubMed  Google Scholar 

  • Neder R (1957) Allometrisches wachstum von hirnteilen bei drei verschieden großen schabenarten. Zool Jahrb Anat 4:411–464

    Google Scholar 

  • Ng M, Roorda RD, Lima SQ, Zemelman BV, Morcillo P, Miesenböck G (2002) Transmission of olfactory information between three populations of neurons in the antennal lobe of the fly. Neuron 36:463–474

    Article  CAS  PubMed  Google Scholar 

  • Oland LA, Tolbert LP (1988) Effects of hydroxyurea parallel the effects of radiation in developing olfactory glomeruli in insects. J Comp Neurol 278:377–387

    Article  CAS  PubMed  Google Scholar 

  • Papadopoulou M, Cassenaer S, Nowotny T, Laurent G (2011) Normalization for sparse encoding of odors by a wide-field interneuron. Science 332:721–725

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pearson L (1971) The corpora pedunculata of Sphinx ligustri L. and other lepidoptera: an anatomical study. Philos Trans R Soc B Biol Sci 259:477–516

    Article  Google Scholar 

  • Picimbon JF (2003) Biochemistry and evolution of OBP and CSP proteins. In: Vogt RG, Blomquist GJ (eds) Insect pheromone biochemistry and molecular biology – The biosynthesis and detection of pheromones and plant volatiles. Elsevier Academic Press, London/San Diego, pp 539–566

    Chapter  Google Scholar 

  • Picimbon JF, Gadenne C (2002) Evolution of noctuid pheromone binding proteins: identification of PBP in the black cutworm moth, Agrotis ipsilon. Insect Biochem Mol Biol 32:839–846

    Article  CAS  PubMed  Google Scholar 

  • Pollack I, Hofbauer A (1991) Histamine-like immunoreactivity in the visual system and brain of Drosophila melanogaster. Cell Tissue Res 266:391–398

    Article  CAS  PubMed  Google Scholar 

  • Prestwich GD, Du G, LaForest S (1995) How is pheromone specificity encoded in proteins? Chem Senses 20:461–469

    Article  CAS  PubMed  Google Scholar 

  • Python F, Stocker RF (2002) Immunoreactivity against choline acetyltransferase, γ-aminobutyric acid, histamine, octopamine, and serotonin in the larval chemosensory system of Drosophila melanogaster. J Comp Neurol 453:157–167

    Article  CAS  PubMed  Google Scholar 

  • Ramaekers A, Parmentier ML, Lasnier C, Bockaert J, Grau Y (2001) Distribution of metabotropic glutamate receptor DmGlu-A in Drosophila melanogaster central nervous system. J Comp Neurol 438:213–225

    Article  CAS  PubMed  Google Scholar 

  • Rehder V, Bicker G, Hammer M (1987) Serotonin-immunoreactive neurons in the antennal lobes and suboesophageal ganglion of the honeybee. Cell Tissue Res 247:59–66

    Article  Google Scholar 

  • Rein K, Zöckler M, Mader MT, Grübel C, Heisenberg M (2002) The Drosophila standard brain. Curr Biol 12:227–231

    Article  CAS  PubMed  Google Scholar 

  • Robertson HM, Wanner KW (2006) The chemoreceptor superfamily in the honey bee, Apis mellifera: Expansion of the odorant, but not gustatory, receptor family. Genome Res 16:1395–1403

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Robertson HM, Warr CG, Carlson JR (2003) Molecular evolution of the insect chemoreceptor gene superfamily in Drosophila melanogaster. Proc Natl Acad Sci 100:14537–14542

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rospars JP, Hildebrand JG (1992) Anatomical identification of glomeruli in the antennal lobes of the male sphinx moth Manduca sexta. Cell Tissue Res 270:205–227

    Article  CAS  PubMed  Google Scholar 

  • Rybak J, Menzel R (1993) Anatomy of the mushroom bodies in the honey bee brain: The neuronal connections of the alpha-lobe. J Comp Neurol 334:444–465

    Article  CAS  PubMed  Google Scholar 

  • Salecker I, Distler P (1990) Serotonin-immunoreactive neurons in the antennal lobes of the American cockroach Periplaneta americana: light- and electron-microscopic observations. Histochemistry 94:463–473

    Article  CAS  PubMed  Google Scholar 

  • Sato K, Pellegrino M, Nakagawa T, Nakagawa T, Vosshall LB, Touhara K (2008) Insect olfactory receptors are heteromeric ligand-gated ion channels. Nature 452:1002–1006

    Article  CAS  PubMed  Google Scholar 

  • Schäfer S, Bicker G (1986) Distribution of GABA-like immunoreactivity in the brain of the honeybee. J Comp Neurol 246:287–300

    Article  PubMed  Google Scholar 

  • Schäfer S, Rehder V (1989) Dopamine-like immunoreactivity in the brain and suboesophageal ganglion of the honeybee. J Comp Neurol 280:43–58

    Article  PubMed  Google Scholar 

  • Schäfer S, Rosenboom H, Menzel R (1994) Ionic currents of Kenyon cells from the mushroom body of the honeybee. J Neurosci 14:4600–4612

    Article  PubMed  PubMed Central  Google Scholar 

  • Schildberger K (1983) Local interneurons associated with the mushroom bodies and the central body in the brain of Acheta domesticus. Cell Tissue Res 230:573–586

    Article  CAS  PubMed  Google Scholar 

  • Schildberger K (1984) Multimodal interneurons in the cricket brain: properties of identified extrinsic mushroom body cells. J Comp Physiol A 154:71–79

    Article  Google Scholar 

  • Schneider D, Kaissling KE (1957) Der Bau der Antenne des Seidenspinners Bombyx mori L., II. Sensillen, cuticulare Bildungen und innerer Bau. Zool Jahrb Anat 76:223–250

    Google Scholar 

  • Seki Y, Kanzaki R (2008) Comprehensive morphological identification and GABA immunocytochemistry of antennal lobe local interneurons in Bombyx mori. J Comp Neurol 506:93–107

    Article  CAS  PubMed  Google Scholar 

  • Seki Y, Rybak J, Wicher D, Sachse S, Hansson BS (2010) Physiological and morphological characterization of local interneurons in the Drosophila antennal lobe. J Neurophysiol 104:1007–1019

    Article  PubMed  Google Scholar 

  • Shang Y, Claridge-Chang A, Sjulson L, Pypaert M, Miesenböck G (2007) Excitatory local circuits and their implications for olfactory processing in the fly antennal lobe. Cell 128:601–612

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smadja C, Shi P, Butlin RK, Robertson HM (2009) Large gene family expansions and adaptive evolution for odorant and gustatory receptors in the pea aphid, Acyrthosiphon pisum. Mol Biol Evol 26:2073–2086

    Google Scholar 

  • Stocker RF, Lienhard MC, Borst A, Fischbach KF (1990) Neuronal architecture of the antennal lobe in Drosophila melanogaster. Cell Tissue Res 262:9–34

    Article  CAS  PubMed  Google Scholar 

  • Stopfer M, Bhagavan S, Smith BH, Laurent G (1997) Impaired odour discrimination on desynchronization of odour-encoding neural assemblies. Nature 390:70–74

    Article  CAS  PubMed  Google Scholar 

  • Strausfeld NJ (1976) Atlas of an insect brain, vol 52. Springer, Berlin, pp 1096–1109

    Book  Google Scholar 

  • Strausfeld NJ, Li Y (1999) Organization of olfactory and multimodal afferent neurons supplying the calyx and pedunculus of the cockroach mushroom bodies. J Comp Neurol 409:603–625

    Article  CAS  PubMed  Google Scholar 

  • Strausfeld NJ, Hansen L, Li Y, Gomez RS, Ito K (1998) Evolution, discovery, and interpretations of arthropod mushroom bodies. Learn Mem 5:11–37

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sun XJ, Fonta C, Masson C (1993) Odour quality processing by bee antennal lobe interneurones. Chem Senses 18:355–377

    Article  CAS  Google Scholar 

  • Svidersky VL, Plotnikova SI (2004) On structural-functional organization of dragonfly mushroom bodies and some general considerations about purpose of these formations. J Evol Biochem Physiol 40:608–624

    Article  Google Scholar 

  • Tabuchi M, Inoue S, Kanzaki R, Nakatani K (2012) Whole-cell recording from kenyon cells in silkmoths. Neurosci Lett 528:61–66

    Article  CAS  PubMed  Google Scholar 

  • Tanaka NK, Tanimoto H, Ito K (2008) Neuronal assemblies of the Drosophila mushroom body. J Comp Neurol 508:711–755

    Article  PubMed  Google Scholar 

  • Tanaka K, Uda Y, Ono Y, Nakagawa T, Suwa M, Yamaoka R, Touhara K (2009) Highly selective tuning of a silkworm olfactory receptor to a key mulberry leaf volatile. Curr Biol 19:881–890

    Article  CAS  PubMed  Google Scholar 

  • Tyrer NM, Turner JD, Altman JS (1984) Identifiable neurons in the locust central nervous system that react with antibodies to serotonin. J Comp Neurol 227:313–330

    Article  CAS  PubMed  Google Scholar 

  • Vieira FG, Sánchez-Gracia A, Rozas J (2007) Comparative genomic analysis of the odorant-binding protein family in 12 Drosophila genomes: purifying selection and birth-and-death evolution. Genome Biol 8:R235

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vogt K, Aso Y, Hige T, Knapek S, Ichinose T, Friedrich AB, Turner GC, Rubin GM, Tanimoto H (2016) Direct neural pathways convey distinct visual information to Drosophila mushroom bodies. Elife 5:e14009

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vogt RG, Riddiford LM (1981) Pheromone binding and inactivation by moth antennae. Nature 293:161–163

    Article  CAS  PubMed  Google Scholar 

  • Vogt RG, Rogers ME, Franco M, Sun M (2002) A comparative study of odorant binding protein genes: differential expression of the PBP1-GOBP2 gene cluster in Manduca sexta (Lepidoptera) and the organization of OBP genes in Drosophila melanogaster (Diptera). J Exp Biol 205:719–744

    CAS  PubMed  Google Scholar 

  • Vowles DM (1955) The structure and connexions of the corpora pedunculata in bees and ants. Q J Microsc Sci 96:239–255

    Google Scholar 

  • Vowles DM (1964) Olfactory learning and brain lesions in the wood ant (Formica rufa). J Comp Physiol Psychol 58:105–111

    Article  CAS  PubMed  Google Scholar 

  • Waldrop B, Christensen TA, Hildebrand JG (1987) GABA-mediated synaptic inhibition of projection neurons in the antennal lobes of the sphinx moth, Manduca sexta. J Comp Physiol A 161:23–32

    Article  CAS  PubMed  Google Scholar 

  • Wang X et al (2014) The locust genome provides insight into swarm formation and long-distance flight. Nat Commun 5:2957

    Article  CAS  PubMed  Google Scholar 

  • Wang Z, Yang P, Chen D, Jiang F, Li Y, Wang X, Kang L (2015) Identification and functional analysis of olfactory receptor family reveal unusual characteristics of the olfactory system in the migratory locust. Cell Mol Life Sci 72:4429–4443

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Watanabe H, Nishino H, Nishikawa M, Mizunami M, Yokohari F (2010) Complete mapping of glomeruli based on sensory nerve branching pattern in the primary olfactory center of the cockroach Periplaneta americana. J Comp Neurol 518:3907–3930

    Article  PubMed  Google Scholar 

  • Weiss MJ (1981) Structural patterns in the corpora pedunculata of orthoptera: a reduced silver analysis. J Comp Neurol 203:515–553

    Article  CAS  PubMed  Google Scholar 

  • Wendt B, Homberg U (1992) Immunocytochemistry of dopamine in the brain of the locust Schistocerca gregaria. J Comp Neurol 321:387–403

    Article  CAS  PubMed  Google Scholar 

  • Werringloer A (1932) Die sehorgane und sehzentren der dorylinen nebst untersuchungen über die facettenaugen der Formiciden. Z Wiss Zool 141:432–520

    Google Scholar 

  • Wilson RI, Laurent G (2005) Role of GABAergic inhibition in shaping odor-evoked spatiotemporal patterns in the Drosophila antennal lobe. J Neurosci 25:9069–9079

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wilson RI, Turner GC, Laurent G (2004) Transformation of olfactory representations in the Drosophila antennal lobe. Science (80-) 303:366–370

    Article  CAS  Google Scholar 

  • Witthöft W (1967) Absolute anzahl und verteilung der zellen im him der honigbiene. Z Morphol Tiere 61:160–184

    Article  Google Scholar 

  • Yasuyama K, Salvaterra PM (1999) Localization of choline acetyltransferase-expressing neurons in Drosophila nervous system. Microsc Res Tech 45:65–79

    Article  CAS  PubMed  Google Scholar 

  • Yasuyama K, Meinertzhagen IA, Schürmann FW (2002) Synaptic organization of the mushroom body calyx in Drosophila melanogaster. J Comp Neurol 445:211–226

    Article  PubMed  Google Scholar 

  • Zhou JJ, He XL, Pickett JA, Field LM (2008) Identification of odorant-binding proteins of the yellow fever mosquito Aedes aegypti: genome annotation and comparative analyses. Insect Mol Biol 17:147–163

    Article  CAS  PubMed  Google Scholar 

  • Zhou JJ, Robertson G, He X, Dufour S, Hooper AM, Pickett JA, Keep NH, Field LM (2009) Characterisation of Bombyx mori odorant-binding proteins reveals that a general odorant-binding protein discriminates between sex pheromone components. J Mol Biol 389:529–545

    Article  CAS  PubMed  Google Scholar 

  • Zhou JJ, Vieira FG, He XL, Smadja C, Liu R, Rozas J, Field LM (2010) Genome annotation and comparative analyses of the odorant-binding proteins and chemosensory proteins in the pea aphid Acyrthosiphon pisum. Insect Mol Biol 19:113–122

    Google Scholar 

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Singh, S.S., Mittal, A.M., Chepurwar, S., Gupta, N. (2019). Olfactory Systems in Insects: Similarities and Differences Between Species. In: Picimbon, JF. (eds) Olfactory Concepts of Insect Control - Alternative to insecticides. Springer, Cham. https://doi.org/10.1007/978-3-030-05165-5_2

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