The Drosophila larva as a model for studying chemosensation and chemosensory learning: a review.

Understanding the relationship between brain and behavior is the fundamental challenge in neuroscience. We focus on chemosensation and chemosensory learning in larval Drosophila and review what is known about its molecular and cellular bases. Detailed analyses suggest that the larval olfactory system, albeit much reduced in cell number, shares the basic architecture, both in terms of receptor gene expression and neuronal circuitry, of its adult counterpart as well as of mammals. With respect to the gustatory system, less is known in particular with respect to processing of gustatory information in the central nervous system, leaving generalizations premature. On the behavioral level, a learning paradigm for the association of odors with food reinforcement has been introduced. Capitalizing on the knowledge of the chemosensory pathways, we review the first steps to reveal the genetic and cellular bases of olfactory learning in larval Drosophila. We argue that the simplicity of the larval chemosensory system, combined with the experimental accessibility of Drosophila on the genetic, electrophysiological, cellular, and behavioral level, makes this system suitable for an integrated understanding of chemosensation and chemosensory learning.

[1]  W. A. Johnson,et al.  Contribution of Drosophila DEG/ENaC Genes to Salt Taste , 2003, Neuron.

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

[3]  B. Hommel,et al.  Effect anticipation and action control. , 2001, Journal of experimental psychology. Human perception and performance.

[4]  Karel Svoboda,et al.  Stereotyped Odor-Evoked Activity in the Mushroom Body of Drosophila Revealed by Green Fluorescent Protein-Based Ca2+ Imaging , 2004, The Journal of Neuroscience.

[5]  I. Meinertzhagen,et al.  The Extraretinal Eyelet of Drosophila: Development, Ultrastructure, and Putative Circadian Function , 2002, The Journal of Neuroscience.

[6]  Kristin Scott,et al.  Imaging Taste Responses in the Fly Brain Reveals a Functional Map of Taste Category and Behavior , 2006, Neuron.

[7]  M. Pankratz,et al.  Candidate Gustatory Interneurons Modulating Feeding Behavior in the Drosophila Brain , 2005, PLoS biology.

[8]  The function of the proneural genes achaete and scute in the spatio-temporal patterning of the adult labellar bristles of Drosophila melanogaster , 1994, Roux's archives of developmental biology.

[9]  P. Greengard,et al.  Different Presynaptic Roles of Synapsins at Excitatory and Inhibitory Synapses , 2004, The Journal of Neuroscience.

[10]  M Heisenberg,et al.  Expression of Drosophila mushroom body mutations in alternative genetic backgrounds: a case study of the mushroom body miniature gene (mbm). , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[11]  Liqun Luo,et al.  Olfactory receptor neuron axon targeting: intrinsic transcriptional control and hierarchical interactions , 2004, Nature Neuroscience.

[12]  Sumiti Saharan,et al.  Positioning sensory terminals in the olfactory lobe of Drosophila by Robo signaling , 2004, Development.

[13]  G. Nagel,et al.  Light-Induced Activation of Distinct Modulatory Neurons Triggers Appetitive or Aversive Learning in Drosophila Larvae , 2006, Current Biology.

[14]  D. Jhaveri,et al.  Sensory neurons of the Atonal lineage pioneer the formation of glomeruli within the adult Drosophila olfactory lobe. , 2002, Development.

[15]  J. Truman.  8 – Metamorphosis of the Insect Nervous System , 1996 .

[16]  R. Axtell,et al.  Fine structure of the terminal organ of the house fly larva, Musca domestica L. , 2004, Zeitschrift für Zellforschung und Mikroskopische Anatomie.

[17]  R. Levine,et al.  Remodeling of the insect nervous system , 1995, Current Opinion in Neurobiology.

[18]  R. Stocker,et al.  Integration of complex larval chemosensory organs into the adult nervous system of Drosophila , 2004, Development.

[19]  R. N. Singh,et al.  Fine structure of the sensory organs of Drosophila melanogaster Meigen larva (Diptera : Drosophilidae) , 1984 .

[20]  M. Heisenberg,et al.  Visual learning in individually assayed Drosophila larvae , 2004, Journal of Experimental Biology.

[21]  M. Sokolowski.  Drosophila larval foraging behavior: Digging , 1982, Animal Behaviour.

[22]  Gregory S.X.E. Jefferis,et al.  Glomerular Maps without Cellular Redundancy at Successive Levels of the Drosophila Larval Olfactory Circuit , 2005, Current Biology.

[23]  H. L. Carson,et al.  The Genetics and Biology of Drosophila , 1976, Heredity.

[24]  R. Stocker,et al.  Adult‐like complexity of the larval antennal lobe of D. melanogaster despite markedly low numbers of odorant receptor neurons , 2002, The Journal of comparative neurology.

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

[26]  Kei Ito,et al.  Embryonic and larval development of the Drosophila mushroom bodies: concentric layer subdivisions and the role of fasciclin II. , 2002, Development.

[27]  T. Südhof.  The synaptic vesicle cycle , 2004 .

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

[29]  J. Goodship,et al.  Identification of a mutation in synapsin I, a synaptic vesicle protein, in a family with epilepsy , 2004, Journal of Medical Genetics.

[30]  S. Meister,et al.  Spatially restricted expression of candidate taste receptors in the Drosophila gustatory system , 2001, Current Biology.

[31]  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.

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

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

[34]  R. Axel,et al.  A novel multigene family may encode odorant receptors: A molecular basis for odor recognition , 1991, Cell.

[35]  H. Matsunami,et al.  Receptors for bitter and sweet taste , 2002, Current Opinion in Neurobiology.

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

[37]  John R. Carlson,et al.  Coexpression of Two Functional Odor Receptors in One Neuron , 2005, Neuron.

[38]  Leslie B. Vosshall,et al.  Axonal Targeting of Olfactory Receptor Neurons in Drosophila Is Controlled by Dscam , 2003, Neuron.

[39]  S. Sachse,et al.  Role of inhibition for temporal and spatial odor representation in olfactory output neurons: a calcium imaging study. , 2002, Journal of neurophysiology.

[40]  Ronald L. Davis,et al.  Altered Representation of the Spatial Code for Odors after Olfactory Classical Conditioning Memory Trace Formation by Synaptic Recruitment , 2004, Neuron.

[41]  M. Heisenberg,et al.  Flies lacking all synapsins are unexpectedly healthy but are impaired in complex behaviour , 2004, The European journal of neuroscience.

[42]  R. Menzel,et al.  Pharmacological dissociation between the reinforcing, sensitizing, and response-releasing functions of reward in honeybee classical conditioning. , 1999, Behavioral neuroscience.

[43]  P. Guerin,et al.  Neurophysiological and behavioural evidence for an olfactory function for the dorsal organ and a gustatory one for the terminal organ in Drosophila melanogaster larvae. , 2000, Journal of insect physiology.

[44]  G. Technau.  Lineage analysis of transplanted individual cells in embryos of Drosophila melanogaster , 1986, Roux's archives of developmental biology.

[45]  P. Salvaterra,et al.  Dynamic visualization of nervous system in live Drosophila. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[46]  V. Budnik,et al.  Drosophila larval neuromuscular junction: Molecular components and mechanisms underlying synaptic plasticity , 2000, Microscopy research and technique.

[47]  John G Hildebrand,et al.  Olfactory systems: common design, uncommon origins? , 1999, Current Opinion in Neurobiology.

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

[49]  John G Hildebrand,et al.  Spatial and Temporal Organization of Ensemble Representations for Different Odor Classes in the Moth Antennal Lobe , 2004, The Journal of Neuroscience.

[50]  P. Greengard,et al.  Synapsins as regulators of neurotransmitter release. , 1999, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

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

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

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

[54]  A Borst,et al.  Drosophila mushroom body mutants are deficient in olfactory learning. , 1985, Journal of neurogenetics.

[55]  M. Heisenberg,et al.  The carrot, not the stick: appetitive rather than aversive gustatory stimuli support associative olfactory learning in individually assayed Drosophila larvae , 2005, Journal of Comparative Physiology A.

[56]  R. Stocker.  Drosophila as a focus in olfactory research: Mapping of olfactory sensilla by fine structure, odor specificity, odorant receptor expression, and central connectivity , 2001, Microscopy research and technique.

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

[58]  Andrey Rzhetsky,et al.  A Spatial Map of Olfactory Receptor Expression in the Drosophila Antenna , 1999, Cell.

[59]  Troy Zars,et al.  Genetic dissociation of acquisition and memory strength in the heat-box spatial learning paradigm in Drosophila. , 2006, Learning & memory.

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

[61]  R. Stocker.  Design of the larval chemosensory system. , 2008, Advances in experimental medicine and biology.

[62]  S. Kreissl,et al.  Octopamine‐like immunoreactivity in the brain and subesophageal ganglion of the honeybee , 1994, The Journal of comparative neurology.

[63]  J. Carlson,et al.  Candidate taste receptors in Drosophila. , 2000, Science.

[64]  Y. Jan,et al.  L‐glutamate as an excitatory transmitter at the Drosophila larval neuromuscular junction. , 1976, The Journal of physiology.

[65]  Leslie B. Vosshall,et al.  Chemotaxis Behavior Mediated by Single Larval Olfactory Neurons in Drosophila , 2005, Current Biology.

[66]  R. Stocker,et al.  Olfactory neurons expressing identified receptor genes project to subsets of glomeruli within the antennal lobe of Drosophila melanogaster. , 2003, Journal of neurobiology.

[67]  D. Jhaveri,et al.  Distinct types of glial cells populate the Drosophila antenna , 2005, BMC Developmental Biology.

[68]  B. Iyengar,et al.  Behavioral Characterization and Genetic Analysis of the Drosophila melanogaster Larval Response to Light as Revealed by a Novel Individual Assay , 2000, Behavior genetics.

[69]  R. Stocker,et al.  Immunoreactivity against choline acetyltransferase, γ‐aminobutyric acid, histamine, octopamine, and serotonin in the larval chemosensory system of Dosophila melanogaster , 2002, The Journal of comparative neurology.

[70]  François Rouyer,et al.  Larval optic nerve and adult extra-retinal photoreceptors sequentially associate with clock neurons during Drosophila brain development. , 2002, Development.

[71]  Ariane Ramaekers,et al.  Developmental origin of wiring specificity in the olfactory system of Drosophila , 2004, Development.

[72]  Y. Zhong,et al.  Morphological plasticity of motor axons in Drosophila mutants with altered excitability , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[73]  R. Denell,et al.  Embryological origin of the antenno-maxillary complex of the larva of Drosophila melanogaster Meigen (Diptera: Drosophilidae) , 1982 .

[74]  Jeffrey C. Hall,et al.  Development and Neurobiology of Drosophila , 1980, Basic Life Sciences.

[75]  R. Axtell,et al.  Fine structure of the ventral organ of the house fly larva, Musca domestica L. , 2004, Zeitschrift für Zellforschung und Mikroskopische Anatomie.

[76]  J. Hildebrand,et al.  A novel serotonin-immunoreactive neuron in the antennal lobe of the sphinx moth Manduca sexta persists throughout postembryonic life. , 1987, Journal of neurobiology.

[77]  P. Simpson,et al.  Larval multidendrite neurons survive metamorphosis and participate in the formation of imaginal sensory axonal pathways in the notum of Drosophila. , 2000, Developmental biology.

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

[79]  N. K. Tanaka,et al.  Stereotypic and random patterns of connectivity in the larval mushroom body calyx of Drosophila. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[80]  W. Quinn,et al.  Learning in Normal and Mutant Drosophila Larvae , 1979, Science.

[81]  T. Kitamoto.  Conditional modification of behavior in Drosophila by targeted expression of a temperature-sensitive shibire allele in defined neurons. , 2001, Journal of neurobiology.

[82]  L. Gilbert,et al.  Metamorphosis : postembryonic reprogramming of gene expression in amphibian and insect cells , 1996 .

[83]  G. Gisselmann,et al.  Odorant receptor heterodimerization in the olfactory system of Drosophila melanogaster , 2005, Nature Neuroscience.

[84]  Bertram Gerber,et al.  Olfactory learning in individually assayed Drosophila larvae. , 2003, Learning & memory.

[85]  G. Technau,et al.  Lineage analysis of transplanted individual cells in embryos of Drosophila melanogaster , 1987, Roux's archives of developmental biology.

[86]  J. Steinert,et al.  Experience-Dependent Formation and Recruitment of Large Vesicles from Reserve Pool , 2006, Neuron.

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

[88]  Troy Zars,et al.  Behavioral functions of the insect mushroom bodies , 2000, Current Opinion in Neurobiology.

[89]  Volker Hartenstein,et al.  The Embryonic Development of Drosophila melanogaster , 1985, Springer Berlin Heidelberg.

[90]  Reinhard F. Stocker,et al.  Metamorphosis in Drosophila and other insects: the fate of neurons throughout the stages , 2000, Progress in Neurobiology.

[91]  Andrew B Schwartz,et al.  Cortical neural prosthetics. , 2004, Annual review of neuroscience.

[92]  D. Jhaveri,et al.  Mechanisms underlying olfactory neuronal connectivity in Drosophila-the atonal lineage organizes the periphery while sensory neurons and glia pattern the olfactory lobe. , 2000, Developmental biology.

[93]  Ronald L. Davis,et al.  Olfactory memory formation in Drosophila: from molecular to systems neuroscience. , 2005, Annual review of neuroscience.

[94]  J. Carlson,et al.  Drosophila Gr5a encodes a taste receptor tuned to trehalose , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[95]  L. Tompkins,et al.  Olfactory Adaptation in Drosophila Larvae , 2000, Journal of neurogenetics.

[96]  Anupama Dahanukar,et al.  Insect odor and taste receptors. , 2006, Annual review of entomology.

[97]  Persistent larval sensory neurones are required for the normal development of the adult sensory afferent projections in Drosophila. , 2002, Development.

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

[99]  J. Carlson,et al.  Molecular evolution of the insect chemoreceptor gene superfamily in Drosophila melanogaster , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[100]  R. Stocker,et al.  Complex behavioural changes after odour exposure in Drosophila larvae , 2007, Animal Behaviour.

[101]  V. Rodrigues.  Olfactory behavior of Drosophila melanogaster. , 1980, Basic life sciences.

[102]  R. Axtell,et al.  Fine structure of the dorsal organ of the house fly larva, Musca domestica L. , 2004, Zeitschrift für Zellforschung und Mikroskopische Anatomie.

[103]  D. Soll,et al.  Morphometric description of the wandering behavior in Drosophila larvae: aberrant locomotion in Na+ and K+ channel mutants revealed by computer-assisted motion analysis. , 1997, Journal of neurogenetics.

[104]  R. Delgado,et al.  Synaptic vesicle pools and plasticity of synaptic transmission at the Drosophila synapse , 2004, Brain Research Reviews.

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

[106]  John R. Carlson,et al.  Integrating the Molecular and Cellular Basis of Odor Coding in the Drosophila Antenna , 2003, Neuron.

[107]  Cori Bargmann,et al.  odr-10 Encodes a Seven Transmembrane Domain Olfactory Receptor Required for Responses to the Odorant Diacetyl , 1996, Cell.

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

[109]  Anthony Dickinson,et al.  The 28th Bartlett Memorial Lecture Causal Learning: An Associative Analysis , 2001, The Quarterly journal of experimental psychology. B, Comparative and physiological psychology.

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

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

[112]  L. Luo,et al.  Development of the Drosophila mushroom bodies: sequential generation of three distinct types of neurons from a neuroblast. , 1999, Development.

[113]  R. Dukas.  Ecological relevance of associative learning in fruit fly larvae , 1999, Behavioral Ecology and Sociobiology.

[114]  T. Godenschwege,et al.  Invertebrate Synapsins: A Single Gene Codes for Several Isoforms in Drosophila , 1996, The Journal of Neuroscience.

[115]  Y. Jan,et al.  Properties of the larval neuromuscular junction in Drosophila melanogaster. , 1976, The Journal of physiology.

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

[117]  Bertram Gerber,et al.  Outcome expectations drive learned behaviour in larval Drosophila , 2006, Proceedings of the Royal Society B: Biological Sciences.

[118]  R. Stocker,et al.  Smell and Taste Perception in Drosophila melanogasterLarva: Toxin Expression Studies in Chemosensory Neurons , 1999, The Journal of Neuroscience.

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

[120]  K. Furukubo-Tokunaga,et al.  Induction of cAMP Response Element-Binding Protein-Dependent Medium-Term Memory by Appetitive Gustatory Reinforcement in Drosophila Larvae , 2005, The Journal of Neuroscience.

[121]  J. Hildebrand.  Metamorphosis of the Insect Nervous System , 1985 .

[122]  L. Tolbert,et al.  Development of an identified serotonergic neuron in the antennal lobe of the moth and effects of reduction in serotonin during construction of olfactory glomeruli. , 1995, Journal of neurobiology.

[123]  Joachim Hoffmann,et al.  Anticipatory Behavioral Control , 2003, ABiALS.

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

[125]  Stephan J Sigrist,et al.  Experience-Dependent Strengthening of Drosophila Neuromuscular Junctions , 2003, The Journal of Neuroscience.

[126]  T. Tully,et al.  Memory through metamorphosis in normal and mutant Drosophila , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[127]  B. Ache,et al.  Olfaction: Diverse Species, Conserved Principles , 2005, Neuron.

[128]  John R. Carlson,et al.  The Molecular Basis of Odor Coding in the Drosophila Larva , 2005, Neuron.

[129]  Lei Liu,et al.  Identification and function of thermosensory neurons in Drosophila larvae , 2003, Nature Neuroscience.

[130]  C. Woodard,et al.  Characterization of the larval olfactory response inDrosophila and its genetic basis , 1989, Behavior genetics.

[131]  M. Ito,et al.  Cerebellar long-term depression: characterization, signal transduction, and functional roles. , 2001, Physiological reviews.

[132]  V. Hartenstein,et al.  Development of the taste bristles on the labellum of Drosophila melanogaster. , 1993, Developmental biology.

[133]  Ramón Huerta,et al.  Self-organization in the olfactory system: one shot odor recognition in insects , 2005, Biological Cybernetics.

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

[135]  M. Hammer.  An identified neuron mediates the unconditioned stimulus in associative olfactory learning in honeybees , 1993, Nature.

[136]  D. Reiff,et al.  Differential Regulation of Active Zone Density during Long-Term Strengthening of Drosophila Neuromuscular Junctions , 2002, The Journal of Neuroscience.

[137]  A. Ferreira,et al.  The synapsins: beyond the regulation of neurotransmitter release , 2002, Cellular and Molecular Life Sciences CMLS.

[138]  M. Cobb.  What and how do maggots smell? , 1999 .

[139]  Martin Heisenberg,et al.  Neural reorganization during metamorphosis of the corpora pedunculata in Drosophila melanogaster , 1982, Nature.

[140]  C. Goodman,et al.  Genetic Dissection of Structural and Functional Components of Synaptic Plasticity. III. CREB Is Necessary for Presynaptic Functional Plasticity , 1996, Neuron.

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

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

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

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

[145]  Bertram Gerber,et al.  Olfactory learning and behaviour are ‘insulated’ against visual processing in larval Drosophila , 2006, Journal of Comparative Physiology A.

[146]  Silke Sachse,et al.  Atypical Membrane Topology and Heteromeric Function of Drosophila Odorant Receptors In Vivo , 2006, PLoS biology.

[147]  B. Ganetzky,et al.  Altered synaptic transmission in Drosophila hyperkinetic mutants. , 1989, Journal of neurogenetics.

[148]  M. Mizunami,et al.  Participation of octopaminergic reward system and dopaminergic punishment system in insect olfactory learning revealed by pharmacological study , 2005, The European journal of neuroscience.

[149]  G. Struhl.  A blastoderm fate map of compartments and segments of the Drosophila head. , 1981, Developmental biology.

[150]  A. Fiala,et al.  Genetically Expressed Cameleon in Drosophila melanogaster Is Used to Visualize Olfactory Information in Projection Neurons , 2002, Current Biology.

[151]  R. N. Singh.  Neurobiology of the gustatory systems of Drosophila and some terrestrial insects , 1997, Microscopy research and technique.

[152]  Manfred Forstreuter,et al.  Behavioral responses of Drosophila to biogenic levels of carbon dioxide depend on life-stage, sex and olfactory context , 2006, Journal of Experimental Biology.

[153]  H. Jäckle,et al.  Number, identity, and sequence of the Drosophila head segments as revealed by neural elements and their deletion patterns in mutants. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[154]  M. Sokolowski,et al.  Drosophila larval foraging behavior. II. Selection in the sibling species,D. melanogaster andD. simulans , 1983, Behavior genetics.

[155]  J. Hildebrand,et al.  Olfactory interneurons in the brain of the larval sphinx moth Manduca sexta , 1990, Journal of Comparative Physiology A.

[156]  M. Cobb,et al.  Olfactory coding in a simple system: adaptation in Drosophila larvae , 2000, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[157]  Martin V. Butz,et al.  Anticipatory Behavior in Adaptive Learning Systems , 2003, Lecture Notes in Computer Science.

[158]  W. Quinn,et al.  Flies, genes, and learning. , 2001, Annual review of neuroscience.

[159]  Richard D Fetter,et al.  Genetic Dissection of Structural and Functional Components of Synaptic Plasticity. II. Fasciclin II Controls Presynaptic Structural Plasticity , 1996, Neuron.

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

[161]  Richard D Fetter,et al.  Genetic Dissection of Structural and Functional Components of Synaptic Plasticity. I. Fasciclin II Controls Synaptic Stabilization and Growth , 1996, Neuron.

[162]  E. Buchner,et al.  A role for Synapsin in associative learning: the Drosophila larva as a study case. , 2005, Learning & memory.

[163]  Richard Axel,et al.  Topographic organization of sensory projections to the olfactory bulb , 1994, Cell.

[164]  S. Duan,et al.  Family-based association study of synapsin II and schizophrenia. , 2004, American journal of human genetics.

[165]  L. Luo,et al.  Development of neuronal connectivity in Drosophila antennal lobes and mushroom bodies , 2002, Current Opinion in Neurobiology.

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

[167]  Postembryonic development of γ‐aminobutyric acid‐like Immunoreactivity in the brain of the sphinx moth Manduca sexta , 1994 .

[168]  M. Heisenberg,et al.  An engram found? Evaluating the evidence from fruit flies , 2004, Current Opinion in Neurobiology.

[169]  B. Gerber,et al.  Appetitive olfactory learning in Drosophila larvae: effects of repetition, reward strength, age, gender, assay type and memory span , 2005, Animal Behaviour.

[170]  M. Sokolowski,et al.  Drosophila larval foraging behavior. I. The sibling species,D. melanogaster andD. simulans , 1983, Behavior genetics.

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

[172]  W. Odenwald,et al.  Misexpression of the white (w) gene triggers male-male courtship in Drosophila. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

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

[174]  R. Stocker,et al.  Larval chemosensory projections and invasion of adult afferents in the antennal lobe of Drosophila. , 1997, Journal of neurobiology.

[175]  L. Luo,et al.  Developmentally programmed remodeling of the Drosophila olfactory circuit , 2005, Development.

[176]  Volker Hartenstein,et al.  Neural Lineages of the Drosophila Brain: A Three-Dimensional Digital Atlas of the Pattern of Lineage Location and Projection at the Late Larval Stage , 2006, The Journal of Neuroscience.

[177]  Cori Bargmann,et al.  Divergent seven transmembrane receptors are candidate chemosensory receptors in C. elegans , 1995, Cell.

[178]  M. Cobb,et al.  Olfactory coding in Drosophila larvae investigated by cross-adaptation , 2005, Journal of Experimental Biology.

[179]  J. Armstrong,et al.  Metamorphosis of the mushroom bodies; large-scale rearrangements of the neural substrates for associative learning and memory in Drosophila. , 1998, Learning & memory.