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Original Articles

Synthesizing Neurophysiology, Genetics, Behaviour and Learning to Produce Whole-Insect Programmable Sensors to Detect Volatile Chemicals

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Pages 179-204 | Published online: 15 Apr 2013

References

  • Angioy , A.M. , Desogus , A. , Barbarossa , I. T. , Anderson , P. and Hansson , B.S. 2003 . Extreme sensitivity in an olfactory system . Chem. Senses , 28 : 279 – 284 .
  • Av-Ron , E. and Rospars , J.P. 1995 . Modeling insect olfactory neuron signaling by a network utilizing disinhibition . Biosystems , 36 : 101 – 108 .
  • Ayyub , C. , Paranjape , J. , Rodrigues , V. and Siddiqi , O. 1990 . Genetics of olfactory behavior in Drosophila melanogaster . Journal of Neurogenetics , 6 : 243 – 262 .
  • Bazhenov , M. , Stopfer , M. , Sejnowski , T. J. and Laurent , G. 2005 . Fast odor learning improves reliability of odor responses in the locust antennal lobe . Neuron , 46 : 483 – 492 .
  • Bhalla , U.S. and Bower , J.M. 1997 . Multiday recordings from olfactory bulb neurons in awake freely moving rats: spatially and temporally organized variability in odorant response properties . Journal of Computational Neuroscience , 4 : 221 – 256 .
  • Bray , S. and Amrein , H. 2003 . A putative Drosophila pheromone receptor expressed in male-specific taste neurons is required for efficient courtship . Neuron , 39 : 1019 – 1029 .
  • Buck , L. and Axel , R. 1991 . A novel multigene family may encode odorant receptors: a molecular basis for odor recognition . Cell , 65 : 175 – 187 .
  • Chang , H.J. and Freeman , W.J. 1996 . Parameter optimization in models of the olfactory neural system . Neural Networks , 9 : 1 – 14 .
  • Chang , H.J. , Freeman , W.J. and Burke , B.C. 1998 . Optimization of olfactory model in software to give 1/f power spectra reveals numerical instabilities in solutions governed by aperiodic (chaotic) attractors . Neural Networks , 11 : 449 – 466 .
  • Cheng , Y. and Nash , H.A. 2008 . Visual mutations reveal opposing effects of illumination on arousal in Drosophila . Genetics , 178 : 2413 – 2416 .
  • Christensen , T.A. , D'Alessandro , G. , Lega , J. and Hildebrand , J.G. 2001 . Morphometric modeling of olfactory circuits in the insect antennal lobe: I. Simulations of spiking local interneurons . Biosystems , 61 : 143 – 153 .
  • Christensen , T.A. , Pawlowski , V.M. , Lei , H. and Hildebrand , J.G. 2000 . Multi-unit recordings reveal context-dependent modulation of synchrony in odor-specific neural ensembles . Nature Neuroscience , 3 : 927 – 931 .
  • Christensen , T.A. and White , J. 2000 . Representation of olfactory information in the brain . The Neurobiology of Taste and Smell , 2 : 201 – 232 .
  • Chyb , S. , Dahanukar , A. , Wickens , A. and Carlson , J.R. 2003 . Drosophila Gr5a encodes a taste receptor tuned to trehalose . National Acad Sciences , 100 : 14526 – 14530 .
  • Clyne , P. , Grant , A. , O'Connell , R. and Carlson , J.R. 1997 . Odorant response of individual sensilla on the Drosophila antenna . Invertebrate Neuroscience , 3 : 127 – 135 .
  • Clyne , P.J. , Warr , C.G. and Carlson , J.R. 2000 . Candidate taste receptors in Drosophila . Science , 287 : 1830
  • Clyne , P.J. , Warr , C.G. , Freeman , M.R. , Lessing , D. , Kim , J. and Carlson , J.R. 1999 . A novel family of divergent seven-transmembrane proteins: candidate odorant receptors in Drosophila . Neuron , 22 : 327 – 338 .
  • Cobb , M. , Bruneau , S. and Jallon , J.M. 1992 . Genetic and developmental factors in the olfactory response of Drosophila melanogaster larvae to alcohols . Proceedings: Biological Sciences , 248 : 103 – 109 .
  • Dahanukar , A. and Foster , K. 2001 . A Gr receptor is required for response to the sugar trehalose in taste neurons of Drosophila . Nature Neuroscience , 4 : 1182 – 1186 .
  • Daly , K.C. , Chandra , S. , Durtschi , M.L. and Smith , B.H. 2001 . The generalization of an olfactory-based conditioned response reveals unique but overlapping odour representations in the moth Manduca sexta . Journal of Experimental Biology , 204 : 3085 – 3095 .
  • Daly , K.C. , Christensen , T.A. , Lei , H. , Smith , B.H. and Hildebrand , J.G. 2004 . Learning modulates the ensemble representations for odors in primary olfactory networks . Proceedings of the National Academy of Sciences , 101 : 10476 – 10481 .
  • Daly , K.C. , Durtschi , M.L. and Smith , B.H. 2001 . Olfactory-based discrimination learning in the moth, Manduca sexta . Journal of Insect Physiology , 47 : 375 – 384 .
  • Daly , K.C. and Smith , B.H. 2000 . Associative olfactory learning in the moth Manduca sexta . Journal of Experimental Biology , 203 : 2025 – 2038 .
  • Daly , K.C. , Wright , G.A. and Smith , B.H. 2004 . Molecular features of odorants systematically influence slow temporal responses across clusters of coordinated antennal lobe units in the moth Manduca sexta . Journal of Neurophysiology , 92 : 236 – 254 .
  • Davis , R.L. 2004 . Olfactory learning . Neuron , 44 : 31 – 48 .
  • Davis , R.L. 2005 . Olfactory memory formation in Drosophila: from molecular to systems neuroscience . Neuron , 28 : 275 – 302 .
  • De Bruyne , M. , Clyne , P.J. and Carlson , J.R. 1999 . Odor coding in a model olfactory organ: the Drosophila maxillary palp . Journal of Neuroscience , 19 ( 11 ) : 4520 – 4532 .
  • De Bruyne , M. , Foster , K. and Carlson , J.R. 2001 . Odor coding in the Drosophila antenna . Neuron , 30 : 537 – 552 .
  • Dobritsa , A.A. , van der Goes van Naters , W. , Warr , C. G. , Steinbrecht , R. A. and Carlson , J.R. 2003 . Integrating the molecular and cellular basis of odor coding in the Drosophila antenna . Neuron , 37 : 827 – 841 .
  • Dunipace , L. , Meister , S. , McNealy , C. and Amrein , H. 2001 . Spatially restricted expression of candidate taste receptors in the Drosophila gustatory system . Current Biology , 11 : 822 – 835 .
  • Dukas , R. 2008 . Evolutionary biology of insect learning . Annual Review of Entomology , 53 : 145 – 160 .
  • Eisenberg , J. , Freeman , W.J. and Burke , B. 1989 . Hardware architecture of a neural network model simulating pattern recognition by the olfactory bulb . Neural Networks , 2 : 315 – 325 .
  • Elmore , T. , Ignell , R. , Carlson , J.R. and Smith , D.P. 2003 . Targeted mutation of a Drosophila odor receptor defines receptor requirement in a novel class of sensillum . Journal of Neuroscience , 23 : 9906 – 9912 .
  • Evans , J.D. , Aronstein , K. , Chen , Y.P. , Hetru , J. , Imler , J.L. , Jiang , H. , Kanost , M. , Thompson , G.J. , Zou , Z. and Hultmark , D. 2006 . Immune pathways and defense mechanisms in honey bees Apis mellifera . Insect Molecular Biology , 15 : 645 – 656 .
  • Faber , T. , Joerges , J. and Menzel , R. 1999 . Associative learning modifies neural representations of odors in the insect brain . Nature Neuroscience , 2 : 74 – 78 .
  • Ferguson , H.J. , Cobey , S. and Smith , B.H.. 2001 . Sensitivity to a change in reward is heritable in the honeybee, Apis mellifera . Animal Behavior , 61 : 527 – 534 .
  • Fletcher , M.L. and Wilson , D.A. 2003 . Olfactory bulb mitral-tufted cell plasticity: odorant-specific tuning reflects previous odorant exposure . Journal of Neuroscience , 23 : 6946 – 6955 .
  • Freeman , W.J. , Yao , Y. and Burke , B. 1988 . Central pattern generating and recognizing in olfactory bulb: A correlation learning rule . Neural Networks , 1 : 277 – 288 .
  • French , D.A. , Flannery , R.J. , Groetsch , C.W. , Krantz , W.B. and Kleene , S.J. 2006 . Numerical approximation of solutions of a nonlinear inverse problem arising in olfaction experimentation . Mathematical and Computer Modelling , 43 : 945 – 956 .
  • Frisch Von , K. 1950 . Bees, Their Vision, Chemical Senses and Language , Ithaca, New York, Great Seal Books : Cornell University Press .
  • Frisch Von , K. 1915 . Der Farbensinn und formensinn der biene . Zool. Abt. Allg. Zool. Physiol , 35 : 1 – 182 .
  • Galizia , C.G. and Menzel , R. 2000 . Odour perception in honeybees: coding information in glomerular patterns . Current Opinion in Neurobiology , 10 : 504 – 510 .
  • Galizia , C.G. and Menzel , R. 2001 . The role of glomeruli in the neural representation of odours: results from optical recording studies . Journal of Insect Physiology , 47 : 115 – 130 .
  • Gao , Q. and Chess , A. 1999 . Identification of candidate Drosophila olfactory receptors from genomic DNA sequence . Genomics , 60 : 31 – 39 .
  • Getz , W.M. 1991 . A neural network for processing olfactory-like stimuli . Bulletin of Mathematical Biology , 53 : 805 – 823 .
  • Getz , W.M. and Lutz , A. 1999 . A neural network model of general olfactory coding in the insect antennal lobe . Chem. Senses , 24 : 351 – 372 .
  • Godfrey , P.A. , Malnic , B. and Buck , L. B. 2004 . The mouse olfactory receptor gene family . Proceedings of the National Academy of Sciences , 101 : 2156 – 2161 .
  • Goldberg , S.J. and Moulton , D.G. 1987 . Olfactory bulb responses telemetered during an odor discrimination task in rats . Experimental Neurology , 96 : 430
  • Gu , Y. and Liljenström , H. 2007 . Modelling efficiency in insect olfactory information processing . Biosystems , 89 : 236 – 243 .
  • Hallem , E.A. and Carlson , J.R. 2004 . The odor coding system of Drosophila . Trends in Genetics , 20 : 453 – 459 .
  • Hallem , E.A. , Ho , M.G. and Carlson , J. R. 2004 . The molecular basis of odor coding in the Drosophila antenna . Cell , 117 : 965 – 979 .
  • Hammer , M. 1993 . An identified neuron mediates the unconditioned stimulus in associative olfactory learning in honeybees . Nature , 366 : 59 – 63 .
  • Hammer , M. and Menzel , R. 1995 . Learning and memory in the honeybee . Journal of Neuroscience , 15 : 1617 – 1630 .
  • Hammer , M. and Menzel , R. 1998 . Multiple sites of associative odor learning as revealed by local brain microinjections of octopamine in honeybees . Learning & Memory , 5 : 146 – 156 .
  • Hannson , B.S. 1991 . Insect Olfaction. Springer Verlag , 1st New York
  • Heimbeck , G. , Bugnon , V. , Gendre , N. , Haberlin , C. and Stocker , R.F. 1999 . Smell and taste perception in Drosophila melanogaster larva: toxin expression studies in chemosensory neurons . Journal of Neuroscience , 19 : 6599 – 6609 .
  • Heinbockel , T. and Kaissling , K.E. 1996 . Variability of olfactory receptor neuron responses of female silkmoths (Bombyx mori L.) to benzoic acid and (±)-linalool . Journal of Insect Physiology , 42 : 565 – 578 .
  • Hildebrand , J.G. 1995 . Analysis of chemical signals by nervous systems . Proceedings of the National Academy of Sciences , 92 : 67 – 74 .
  • Hildebrand , J.G. and Shepherd , G.M. 1997 . Mechanisms of olfactory discrimination: converging evidence for common principles across phyla . Annual Review of Neuroscience , 20 : 595 – 631 .
  • Hill , C.A. , Fox , A.N. , Pitts , R.J. , Kent , L.B. , Tan , P.L. Chrystal , M.A. 2002 . G protein-coupled receptors in Anopheles gambiae . Science , 298 : 176 – 178 .
  • Hoffman , D.S. , Nehrir , A.R. , Repasky , K.S. , Shaw , J.A. and Carlsten , J.L. 2007 . Range-resolved optical detection of honeybees by use of wing-beat modulation of scattered light for locating land mines . Applied Optics , 46 : 3007 – 3012 .
  • Hosler , J.S. and Smith , B.H. 2000 . Blocking and the detection of odor components in blends . Journal of Experimental Biology , 203 : 2797 – 2806 .
  • Ikeno , H. and Usui , S. 1999 . Mathematical description of ionic currents of the Kenyon cell in the mushroom body of honeybee . Neurocomputing , 26 : 177 – 184 .
  • Ishimoto , H and Tanimura , T. 2004 . Molecular Neurophysiology of Taste in Drosophila . Cellular and Molecular Life Sciences , 61 : 10 – 18 .
  • Jefferis , G. , Marin , E.C. , Stocker , R.F. and Luo , L. 2001 . Target neuron prespecification in the olfactory map of Drosophila . Nature , 414 : 204 – 208 .
  • Kaiser , L. , Perez-Maluf , R. , Sandoz , J.C. and Pham-Delegue , M.H. 2003 . Dynamics of odour learning in Leptopilina boulardi, a hymenopterous parasitoid . Animal Behaviour , 66 : 1077 – 1084 .
  • Kaissling , K.E. , Meng , L.Z. and Bestmann , H.J. 1989 . Responses of Bombykol receptor cells to (Z, E)-4, 6-hexadecadiene and linalool . Journal of Comparative Physiology A: Sensory, Neural, and Behavioral Physiology , 165 : 147 – 154 .
  • Kanzaki , R. 1996 . Behavioral and neural basis of instinctive behavior in insects: odorsource searching strategies without memory and learning . Robotics and Autonomous Systems , 18 : 33 – 43 .
  • Kay , L.M. and Laurent , G. 1999 . Odor-and context-dependent modulation of mitral cell activity in behaving rats . Nature Neuroscience , 2 : 1003 – 1009 .
  • Kendrick , K.M. , Levy , F. and Keverne , E.B. 1992 . Changes in the sensory processing of olfactory signals induced by birth in sleep . Science , 256 : 833 – 836 .
  • Kent , K.S. , Hoskins , S.G. and Hildebrand , J.G. 1987 . A novel serotoninimmunoreactive neuron in the antennal lobe of the sphinx moth Manduca sexta persists throughout postembryonic life . Journal of neurobiology , 18 : 451 – 465 .
  • King , T.L. , Horine , F.M. , Daly , K.C. and Smith , B.H. 2004 . Explosives detection with hard-wired moths . IEEE Transactions on Instrumentation and Measurement , 53 : 1113 – 1118 .
  • Laurent , G. 1999 . A systems perspective on early olfactory coding . Science , 286 : 723
  • Laurent , G. , Stopfer , M. , Friedrich , R.W. , Rabinovich , M.I. , Volkovskii , A. and Abarbanel , H.D. I. 2001 . Odor encoding as an active, dynamical process: experiments, computation and theory theory . Annual Review of Neuroscience , 24 : 263 – 297 .
  • Lei , H. , Christensen , T.A. and Hildebrand , J.G. 2002 . Local inhibition modulates odor-evoked synchronization of glomerulus-specific output neurons . Nature Neuroscience , 5 : 557 – 565 .
  • Lei , H. , Christensen , T.A. and Hildebrand , J.G. 2004 . Spatial and temporal organization of ensemble representations for different odor classes in the moth antennal lobe . Journal of Neuroscience , 24 : 11108 – 11119 .
  • Lewis , W.J. and Takasu , K. 1990 . Use of learned odours by a parasitic wasp in accordance with host and food needs . Nature , 348 : 635 – 6 .
  • Li , C. , Geng , C. , Leung , H.T. , Hong , Y.S. Strong , L.L. 1999 . “ INAF, a protein required for transient receptor potential Ca(2+) channel function ” . In Proceedings of the National Academy of Science USA Vol. 96 , 13474 – 13479 .
  • Linster , C. and Smith , B.H. 1997 . A computational model of the response of honey bee antennal lobe circuitry to odor mixtures: overshadowing, blocking and unblocking can arise from lateral inhibition . Behavioural Brain Research , 87 : 1 – 14 .
  • Liu , X. and Davis , R.L. 2006 . Insect olfactory memory in time and space . Current Opinion in Neurobiology , 16 : 679 – 685 .
  • Ma , Z. and Krings , A.W. 2009 . Insect sensory systems inspired computing and communications . Ad Hoc Networks , 7 : 742 – 755 .
  • Malnic , B. , Godfrey , P.A. and Buck , L.B. 2004 . The human olfactory receptor gene family . Proceedings of the National Academy of Sciences , 101 : 2584 – 2589 .
  • Malnic , B. , Hirono , J. , Sato , T. and Buck , L. B. 1999 . Combinatorial receptor codes for odors . Cell , 96 : 713 – 724 .
  • Marin , E.C. , Jefferis , G. , Komiyama , T. , Zhu , H. and Luo , L. 2002 . Representation of the glomerular olfactory map in the Drosophila brain . Cell , 109 : 243 – 255 .
  • McGuire , S.E. , Deshazer , M. and Davis , R.L. 2005 . Thirty years of olfactory learning and memory research in Drosophila melanogaster . Progress in Neurobiology , 76 : 328 – 347 .
  • Meiners , T. , Wackers , F. and Lewis , W.J. 2002 . The effect of molecular structure on olfactory discrimination by the parasitoid Microplitis croceipes . Chem. Senses , 27 : 811 – 816 .
  • Menzel , R. 1985 . “ Learning in Honeybees in an Ecological and Behavioral Context. Pages 55–74 ” . In Experimental Behavioral Ecology , Edited by: Hölldobler , B. and Lindauer , M. Stuttgart : Gustav Fischer .
  • Monte , P. , Woodard , C. , Ayer , R. , Lilly , M. , Sun , H. and Carlson , J. 1989 . Characterization of the larval olfactory response in Drosophila and its genetic basis . Behavior Genetics , 19 : 267 – 283 .
  • Morgan , P.G. , Sedensky , M.M. , Meneely , P.M. and Cascorbi , H.F. 1988 . The effect of two genes on anesthetic response in the nematode Caenorhabditis elegans . Anesthesiology , 69 : 246 – 251 .
  • Mori , K. , Nagao , H. and Yoshihara , Y. 1999 . The olfactory bulb: coding and processing of odor molecule information . Science , 286 : 711 – 715 .
  • Nikonov , A.A. and Leal , W.S. 2002 . Peripheral coding of sex pheromone and a behavioral antagonist in the Japanese beetle, Popillia japonica . Journal of Chemical Ecology , 28 : 1075 – 1089 .
  • Oldroyd , B.P. and Thompson , G.J. 2006 . Behavioural genetics of the honey bee Apis mellifera . Advanced Insect Physiology , 33 : 1 – 49 .
  • Olsen , S.R. and Wislon , R.I. 2008 . Cracking neural circuits in a tiny brain: new approaches for understanding the neural circuitry of Drosophila . Trends in Neuroscience , 31 : 512 – 520 .
  • Olson , D.M. , Rains , G. C. , Meiners , T. , Takasu , K. , Tertuliano , M. , Tumlinson , J.H , Wackers , F.L. and Lewis , W.J. 2003 . Parasitic wasps learn and report diverse chemicals with unique conditionable behaviors . Chem. Senses , 28 : 545 – 549 .
  • Oppliger , F.Y. , Guerin , P. M. and Vlimant , M. 2000 . Neurophysiological and behavioural evidence for an olfactory function for the dorsal organ and a gustatory one for the terminal organ in Drosophila melanogaster larvae . Journal of Insect Physiology , 46 : 135 – 144 .
  • Patterson , T.A. , Thomas , L. , Wilcox , C. , Ovaskainen , O. and Matthiopoulos , J. 2008 . State-space models of individual animal movement . Trends in Ecology & Evolution , 23 : 87 – 94 .
  • Pearce , T.C. , Verschure , P. , White , J. and Kauer , J.S. 2001 . Stimulus encoding during the early stages of olfactory processing: A modeling study using an artificial olfactory system . Neurocomputing , 38 : 299 – 306 .
  • Python , F. and Stocker , R.F. 2002 . Adult-like complexity of the larval antennal lobe of D. melanogaster despite markedly low numbers of odorant receptor neurons . The Journal of Comparative Neurology , 445 : 374 – 387 .
  • Quenet , B. , Dubois , R. , Sirapian , S. , Dreyfus , G. and Horn , D. 2002 . Modelling spatiotemporal olfactory data in two steps: from binary to Hodgkin-Huxley neurones . Biosystems , 67 : 203 – 211 .
  • Rains , G.C. , Tomberlin , J.K. , D'Alessandro , M. and Lewis , W.J. 2004 . Limits of Volatile Chemical Detection of a Parasitoid Wasp, Microplitis croceipes, and an Electronic Nose: A Comparative Study . Transactions of the ASAE , 47 : 2145 – 2152 .
  • Rains , G.C. , Utley , S.L. and Lewis , W.J. 2006 . Behavioral monitoring of trained insects for chemical detection . Biotechnology Progress , 22 : 2 – 8 .
  • Rains , G.C. , Tomberlin , J.K. and Kulasiri , D. 2008 . Using insect sniffing devices for detection . Trends in Biotechnology , 26 ( 6 ) : 288 – 294 .
  • Reinhard , J. , Srinivasan , M.V. and Zhang , S. 2004 . Olfaction: Scent-triggered navigation in honeybees . Nature , 427 : 411 – 412 .
  • Ribeiro , L.F.C. , Zanatta , D.B. , Bravo , J.P. , Brancalhão , R.M.C. and Fernandez , M.A. 2009 . Molecular markers in commercial Bombyx mori (Lepidoptera: Bombycidae) hybrids susceptible to multiple nucleopolyhedrovirus . Genetics and Molecular Research , 8 : 144 – 153 .
  • Robertson , H.M. , Warr , C.G. and Carlson , J.R. 2003 . Molecular evolution of the insect chemoreceptor gene superfamily in Drosophila melanogaster . National Acad Sciences , 100 : 14537 – 14542 .
  • Rospars , J.P. and Hildebrand , J.G. 2000 . Sexually dimorphic and isomorphic glomeruli in the antennal lobes of the sphinx moth Manduca sexta . Chemical senses , 25 : 119 – 129 .
  • Rospars , J.P. , Lansky , P. , Duchamp-Viret , P. and Duchamp , A. 2001 . Characterizing and modeling concentration-response curves olfactory receptor cells . Neurocomputing , 38–40 : 319 – 325 .
  • Rospars , J.P. , Lucas , P. and Coppey , M. 2007 . Modelling the early steps of transduction in insect olfactory receptor neurons . Biosystems , 89 : 101 – 109 .
  • Rossokhin , A.V. and Tsitolovsky , L.E. 1997 . A mathematical model of neural information processing at the cellular level . Biosystems , 40 : 159 – 167 .
  • Sachse , S. and Galizia , C.G. 2002 . Role of inhibition for temporal and spatial odor representation in olfactory output neurons: a calcium imaging study . Journal of neurophysiology , 87 : 1106 – 1117 .
  • Scott , K. , Brady , R. , Cravchik , A. , Morozov , P. , Rzhetsky , A. Zuker , C. 2001 . A chemosensory gene family encoding candidate gustatory and olfactory receptors in Drosophila . Cell , 104 : 661 – 673 .
  • Shanbhag , S.R. , Müller , B. and Steinbrecht , R.A. 1999 . Atlas of olfactory organs of Drosophila melanogaster 1. Types, external organization, innervation and distribution of olfactory sensilla . International Journal of Insect Morphology and Embryology , 28 : 377 – 397 .
  • Shanbhag , S.R. , Müller , B. and Steinbrecht , R.A. 2000 . Atlas of olfactory organs of Drosophila melanogaster 2. Internal organization and cellular architecture of olfactory sensilla . Arthropod Structure and Development , 29 : 211 – 229 .
  • Shields , V.D.C. and Hildebrand , J.G. 2001 . Responses of a population of antennal olfactory receptor cells in the female moth Manduca sexta to plant-associated volatile organic compounds . Journal of Comparative Physiology A: Neuroethology, Sensory, Neural, and Behavioral Physiology , 186 : 1135 – 1151 .
  • Snopok , B.A. and Kruglenko , I.V. 2002 . Multisensor systems for chemical analysis: state-of-the-art in electronic nose technology and new trends in machine olfaction . Thin Solid Films , 418 : 21 – 41 .
  • Stensmyr , M.C. , Giordano , E. , Balloi , A. , Angioy , A. M. and Hansson , B.S. 2003 . Novel natural ligands for Drosophila olfactory receptor neurones . Journal of Experimental Biology , 206 : 715 – 724 .
  • Stocker , R.F. 1996 . The organization of the chemosensory system in Drosophila melanogaster: a rewiew . Cell and tissue research , 275 : 3 – 26 .
  • Stocker , R.F. , Lienhard , M.C. , Borst , A. and Fischbach , K.F. 1990 . Neuronal architecture of the antennal lobe in Drosophila melanogaster . Cell and Tissue Research , 262 : 9 – 34 .
  • Störtkuhl , K.F. and Kettler , R. 2001 . Functional analysis of an olfactory receptor in Drosophila melanogaster . Proceedings of the National Academy of Sciences , 98 : 9381 – 9385 .
  • Strausfeld , N.J. , Hansen , L. , Li , Y. , Gomez , R.S. and Ito , K. 1998 . Evolution, discovery, and interpretations of arthropod mushroom bodies . Learning & Memory , 5 : 11 – 37 .
  • Sullivan , R.M. , Wilson , D.A. and Leon , M. 1989 . Norepinephrine and learninginduced plasticity in infant rat olfactory system . Journal of Neuroscience , 9 : 3998 – 4006 .
  • Takasu , K. and Lewis , W.J. 1996 . The role of learning in adult food location by the larval parasitoid, Microplitis croceipes (Hymenoptera: Braconidae) . Journal of Insect Behavior , 9 : 265 – 281 .
  • Takken , W. 1996 . Synthesis and future challenges: the response of mosquitoes to host odours . Ciba Found Symp , 200 : 302 – 312 .
  • Thorpe , W.H. 1963 . Learning and Instinct in Animals , 2nd , Cambridge, MA, USA : Harvard University Press .
  • Tertuliano , M. , Olson , D.M. , Rains , G.C. and Lewis , W.J. 2004 . “Influence of handling and training protocol on learning and memory of Microplitis croceipes (Cresson) (Hymenoptera: Braconidae) . Entomologica Experimentalis et Applicata , 110 : 165 – 172 .
  • Tolbert , L.P. and Hildebrand , J.G. 1981 . Organization and synaptic ultrastructure of glomeruli in the antennal lobes of the moth Manduca sexta: a study using thin sections and freeze-fracture . Proceedings of the Royal Society of London. Series B, Biological Sciences , 213 : 279 – 301 .
  • Tomberlin , J.K. , Sheppard , D.C. and Joyce , J.A. 2002 . A comparison of selected life history traits of the black soldier fly (Diptera: Stratiomyidae) when reared on three diets . Annals of the Entomological Society of America , 95 : 379 – 387 .
  • Tomberlin , J.K. , Rains , G.C. and Sanford , M.R. 2008 . Development of Microplitis croceipes as a biological sensor . Entomologia Experimentalis , 128 : 249 – 257 .
  • Troemel , E.R. , Chou , J.H. , Dwyer , N.D. , Colbert , H.A. and Bargmann , C.I. 1995 . Divergent seven transmembrane receptors are candidate chemosensory receptors in C . elegans. Cell , 83 : 207
  • Ueno , K. , Ohta , M. , Morita , H. , Mikuni , Y. , Nakajima , S. Yamamoto , K. 2001 . Trehalose sensitivity in Drosophila correlates with mutations in and expression of the gustatory receptor gene Gr5a . Current Biology , 11 : 1451 – 1455 .
  • Utley , S.L. , Rains , G.C. and Lewis , W.J. 2007 . Behavioral monitoring of Microplitis croceipes, A parasitoid wasp, for detecting target odorants using a computer vision system . Transactions of ASABE , 50 : 1843 – 1849 .
  • Vassar , R. , Chao , S.K. , Sitcheran , R. , Nunez , J.M. , Vosshall , L.B. and Axel , R. 1994 . Topographic organization of sensory projections to the olfactory bulb . Cell , 79 : 981
  • Vet , L.E.M. , Lewis , W.J. and Cardé , R.T. 1995 . “ Parasitoid Foraging and Learning. Pages 65–101 ” . In Chemical Ecology of Insects 2 , Edited by: Cardé , R.T. and Bell , W.J. New York : Chapman & Hall .
  • Vosshall , L.B. , Amrein , H. , Morozov , P.S. , Rzehtsky , A. and Axel , R. 1999 . A spatial map of olfactory receptor expression in the Drosophila antenna . Cell , 96 : 725 – 736 .
  • Vosshall , L.B. , Wong , A. M. and Axel , R. 2000 . An olfactory sensory map in the fly brain . Cell , 102 : 147 – 159 .
  • Wang , F. , Nemes , A. , Mendelsohn , M. and Axel , R. 1998 . Odorant receptors govern the formation of a precise topographic map . Cell , 93 : 47 – 60 .
  • Wang , J.W. , Wong , A. M. , Flores , J. , Vosshall , L. B. and Axel , R. 2003 . Two-photon calcium imaging reveals an odor-evoked map of activity in the fly brain . Cell , 112 : 271 – 282 .
  • Webb , B. 2004 . Neural mechanisms for prediction: do insects have forward models? . Trends in Neurosciences , 27 : 278 – 282 .
  • Wetzel , C.H. , Behrendt , H.J. , Gisselmann , G. , Störtkuhl , K.F. , Hovemann , B. and Hatt , H. 2001 . Functional expression and characterization of a Drosophila odorant receptor in a heterologous cell system . Proceedings of the National Academy of Sciences , 98 : 9377
  • Wilson , D.A. and Sullivan , R.M. 1994 . Neurobiology of associative learning in the neonate: early olfactory learning . Behavioral and Neural Biology , 61 : 1 – 18 .
  • Wilson , D.A. , Sullivan , R.M. and Leon , M. 1987 . Single-unit analysis of postnatal olfactory learning: Modified olfactory bulb output response patterns to learned attractive odors . Journal of Neuroscience , 7 : 3154 – 3162 .
  • Wilson , R.I. , Turner , G.C. and Laurent , G. 2004 . Transformation of olfactory representations in the Drosophila antennal lobe . American Association for the Advancement of Science , 303 : 366 – 370 .
  • Wright , G.A. and Smith , B.H. 2004 . Variation in complex olfactory stimuli and its influence on odour recognition . Proceedings of the Royal Society B-Biological Sciences , 271 : 147 – 152 .
  • Wright , G.A. , Thomson , M.G. and Smith , B.H. 2005 . Odour concentration affects odour identity in honey bees . Proceedings of the Royal Society B-Biological Sciences , 272 : 2417 – 2422 .
  • Wright , G.A. , Carlton , M. and Smith , B.H. 2009 . A honey bee's ability to learn, recognize and discriminate odours depends upon odour sampling time and concentration . Behavioral Neuroscience , 123 ( 1 ) : 36 – 43 .
  • Wong , A.M. , Wang , J. W. and Axel , R. 2002 . Spatial representation of the glomerular map in the Drosophila protocerebrum . Cell, , 109 : 229 – 241 .
  • Xu , F. , Greer , C.A. and Shepherd , G.M. 2000 . Odor maps in the olfactory bulb . The Journal of Comparative Neurology , 422 : 489 – 495 .
  • Yu , D. , Ponomarev , A. and Davis , R.L. 2004 . Altered Representation of the Spatial Code for Odors after Olfactory Classical Conditioning Memory Trace Formation by Synaptic Recruitment . Neuron , 42 : 437 – 449 .
  • Zhang , X. and Firestein , S. 2002 . The olfactory receptor gene superfamily of the mouse . Nature Neuroscience , 5 : 124 – 133 .

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