Learning and memory in Drosophila: behavior, genetics, and neural systems.

The rich behavioral repertoire that Drosophila use to navigate in their natural environment suggests that flies can use memories to inform decisions. Development of paradigms to examine memories that restrict behavioral choice was essential in furthering our understanding of the genetics and neural systems of memory formation in the fly. Olfactory, visual, and place memory paradigms have proven influential in determining principles for the mechanisms of memory formation. Several parts of the nervous system have been shown to be important for different types of memories, including the mushroom bodies and the central complex. Thus far, about 40 genes have been linked to normal olfactory short-term memory. A subset of these genes have also been tested for a role in visual and place memory. Some genes have a common function in memory formation, specificity of action comes from where in the nervous system these genes act. Alternatively, some genes have a more restricted role in different types of memories.

[1]  T. Tully,et al.  Ethanol Intoxication in Drosophila: Genetic and Pharmacological Evidence for Regulation by the cAMP Signaling Pathway , 1998, Cell.

[2]  Ronald L. Davis,et al.  Frontiers in Neural Circuits Neural Circuits , 2022 .

[3]  M Heisenberg,et al.  Behavioral manipulation of retrieval in a spatial memory task for Drosophila melanogaster. , 1997, Learning & memory.

[4]  Rapid matching in Drosophila place learning , 2009, Naturwissenschaften.

[5]  M Heisenberg,et al.  Associative odor learning in Drosophila abolished by chemical ablation of mushroom bodies. , 1994, Science.

[6]  B. Gerber,et al.  A Neurogenetic Dissociation between Punishment-, Reward-, and Relief-Learning in Drosophila , 2010, Front. Behav. Neurosci..

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

[8]  Martin J. Mueller,et al.  Genetic Distortion of the Balance between Punishment and Relief Learning in Drosophila , 2009, Journal of neurogenetics.

[9]  J. Armstrong,et al.  Building the central complex in Drosophila: The generation and development of distinct neural subsets , 2010, The Journal of comparative neurology.

[10]  T. Zars.  Two thermosensors in Drosophila have different behavioral functions , 2001, Journal of Comparative Physiology A.

[11]  D. Yamazaki,et al.  Protein kinase A inhibits a consolidated form of memory in Drosophila , 2008, Proceedings of the National Academy of Sciences.

[12]  Shamik Dasgupta,et al.  A Neural Circuit Mechanism Integrating Motivational State with Memory Expression in Drosophila , 2009, Cell.

[13]  Ann-Shyn Chiang,et al.  NMDA Receptors Mediate Olfactory Learning and Memory in Drosophila , 2005, Current Biology.

[14]  Yueqing Peng,et al.  Dopamine-Mushroom Body Circuit Regulates Saliency-Based Decision-Making in Drosophila , 2007, Science.

[15]  M Heisenberg,et al.  Drosophila mushroom bodies are dispensable for visual, tactile, and motor learning. , 1998, Learning & memory.

[16]  T. Préat,et al.  Mutation of linotte causes behavioral defects independently of pigeon in Drosophila , 2002, NeuroReport.

[17]  N. Strausfeld.  Atlas of an Insect Brain , 1976, Springer Berlin Heidelberg.

[18]  B. Tabashnik,et al.  Development time and resistance to Bt crops , 1999, Nature.

[19]  Ronald L. Davis,et al.  The GABAA Receptor RDL Suppresses the Conditioned Stimulus Pathway for Olfactory Learning , 2009, The Journal of Neuroscience.

[20]  T. Tully,et al.  latheo Encodes a Subunit of the Origin Recognition Complex and Disrupts Neuronal Proliferation and Adult Olfactory Memory When Mutant , 1999, Neuron.

[21]  Ronald L. Davis,et al.  Preferential expression in mushroom bodies of the catalytic subunit of protein kinase A and its role in learning and memory , 1993, Neuron.

[22]  B. Gerber,et al.  Synapsin is selectively required for anesthesia-sensitive memory. , 2010, Learning & memory.

[23]  E. Kravitz,et al.  Targeted Manipulation of Serotonergic Neurotransmission Affects the Escalation of Aggression in Adult Male Drosophila melanogaster , 2010, PloS one.

[24]  B. Brembs,et al.  Double Dissociation of PKC and AC Manipulations on Operant and Classical Learning in Drosophila , 2008, Current Biology.

[25]  A. Fiala,et al.  Punishment Prediction by Dopaminergic Neurons in Drosophila , 2005, Current Biology.

[26]  W. Quinn,et al.  A neuropeptide gene defined by the Drosophila memory mutant amnesiac. , 1995, Science.

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

[28]  R. Strauss,et al.  Analysis of a spatial orientation memory in Drosophila , 2008, Nature.

[29]  Ronald L. Davis,et al.  A Dual Role for the Adaptor Protein DRK in Drosophila Olfactory Learning and Memory , 2009, The Journal of Neuroscience.

[30]  S. Waddell,et al.  Sequential Use of Mushroom Body Neuron Subsets during Drosophila Odor Memory Processing , 2007, Neuron.

[31]  B. Dauwalder,et al.  Conditional rescue of the dunce learning/memory and female fertility defects with Drosophila or rat transgenes , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[32]  Li Liu,et al.  Context generalization in Drosophila visual learning requires the mushroom bodies , 1999, Nature.

[33]  B. Gerber,et al.  Behavioral Analyses of Sugar Processing in Choice, Feeding, and Learning in Larval Drosophila , 2008, Chemical senses.

[34]  R. Wolf,et al.  A new paradigm for operant conditioning of Drosophila melanogaster , 1996, Journal of Comparative Physiology A.

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

[36]  Ronald L. Davis,et al.  Pharmacogenetic rescue in time and space of the rutabaga memory impairment by using Gene-Switch , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[37]  Reinhard Wolf,et al.  Visual Pattern Recognition in Drosophila Is Invariant for Retinal Position , 2004, Science.

[38]  Thomas Raabe,et al.  The S6KII (rsk) Gene of Drosophila melanogaster Differentially Affects an Operant and a Classical Learning Task , 2004, The Journal of Neuroscience.

[39]  M Heisenberg,et al.  Flexibility in a single behavioral variable of Drosophila. , 2001, Learning & memory.

[40]  Troy Zars,et al.  Spatial orientation in Drosophila , 2009, Journal of neurogenetics.

[41]  Bruno van Swinderen,et al.  Shared Visual Attention and Memory Systems in the Drosophila Brain , 2009, PloS one.

[42]  Jean-René Martin,et al.  Centrophobism/thigmotaxis, a new role for the mushroom bodies in Drosophila. , 2005, Journal of neurobiology.

[43]  M. Heisenberg,et al.  Identification of mushroom body miniature, a zinc-finger protein implicated in brain development of Drosophila. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[44]  Ronald L. Davis,et al.  Dynamics of Learning-Related cAMP Signaling and Stimulus Integration in the Drosophila Olfactory Pathway , 2009, Neuron.

[45]  J. Armstrong,et al.  Genetic analysis of the Drosophila ellipsoid body neuropil: organization and development of the central complex. , 1999, Journal of neurobiology.

[46]  H. Reichert,et al.  Associative learning of Drosophila melanogaster , 1974, Nature.

[47]  B. Skinner,et al.  Are theories of learning necessary? , 2013, Psychological review.

[48]  Reinhard Wolf,et al.  Visual pattern recognition in Drosophila involves retinotopic matching , 1993, Nature.

[49]  D. Guarnieri,et al.  Genetic Dissociation of Ethanol Sensitivity and Memory Formation in Drosophila melanogaster , 2008, Genetics.

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

[51]  Y. Zhong,et al.  A neurofibromatosis-1-regulated pathway is required for learning in Drosophila , 2000, Nature.

[52]  T. Préat,et al.  Genetic dissection of consolidated memory in Drosophila , 1994, Cell.

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

[54]  T. Préat,et al.  IDENTIFICATION OF LINOTTE, A NEW GENE AFFECTING LEARNING AND MEMORY IN DROSOPHILA MELANOGASTER , 2007, Journal of neurogenetics.

[55]  Y. Zhong.  Mediation of PACAP–like neuropeptide transmission by coactivation of Ras/Raf and cAMP signal transduction pathways in Drosophila , 1995, Nature.

[56]  T. Préat,et al.  Parametric and genetic analysis of Drosophila appetitive long‐term memory and sugar motivation , 2009, Genes, brain, and behavior.

[57]  H. Tanimoto,et al.  Appetitive and Aversive Visual Learning in Freely Moving Drosophila , 2009, Front. Behav. Neurosci..

[58]  W. Quinn,et al.  cAMP-dependent protein kinase and the disruption of learning in transgenic flies , 1991, Neuron.

[59]  I. Hakker,et al.  Distinct Functional Domains of Neurofibromatosis Type 1 Regulate Immediate versus Long-Term Memory Formation , 2007, The Journal of Neuroscience.

[60]  Ronald L. Davis,et al.  Spatiotemporal Rescue of Memory Dysfunction in Drosophila , 2003, Science.

[61]  R. Davis,et al.  Genetic dissection of the learning/memory gene dunce of Drosophila melanogaster. , 1993, Genes & development.

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

[63]  M. Heisenberg,et al.  Distinct memory traces for two visual features in the Drosophila brain , 2006, Nature.

[64]  Martin Heisenberg,et al.  Memories in drosophila heat-box learning. , 2002, Learning & memory.

[65]  T. Zars.  Visualizing PKA Dynamics in a Learning Center , 2010, Neuron.

[66]  T. Tully,et al.  latheo, a new gene involved in associative learning and memory in Drosophila melanogaster, identified from P element mutagenesis. , 1992, Genetics.

[67]  A. Gioia,et al.  Thermotolerance and place memory in adult Drosophila are independent of natural variation at the foraging locus , 2009, Journal of Comparative Physiology A.

[68]  Troy Zars,et al.  Serotonin is necessary for place memory in Drosophila , 2008, Proceedings of the National Academy of Sciences.

[69]  W. Quinn,et al.  The amnesiac Gene Product Is Expressed in Two Neurons in the Drosophila Brain that Are Critical for Memory , 2000, Cell.

[70]  Ronald L. Davis,et al.  Gilgamesh Is Required for rutabaga-Independent Olfactory Learning in Drosophila , 2010, Neuron.

[71]  T. Préat,et al.  Tequila, a Neurotrypsin Ortholog, Regulates Long-Term Memory Formation in Drosophila , 2006, Science.

[72]  N. Perrimon,et al.  The Drosophila 14-3-3 protein Leonardo enhances Torso signaling through D-Raf in a Ras 1-dependent manner. , 1997, Development.

[73]  Ronald L. Davis,et al.  GABAA Receptor RDL Inhibits Drosophila Olfactory Associative Learning , 2007, Neuron.

[74]  W. Quinn,et al.  The Drosophila memory mutant amnesiac , 1979, Nature.

[75]  W. Quinn,et al.  Radish, a Drosophila mutant deficient in consolidated memory. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[76]  Tim Tully,et al.  Associative Learning Disrupted by Impaired Gs Signaling in Drosophila Mushroom Bodies , 1996, Science.

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

[78]  Yoshinori Aso,et al.  The Mushroom Body of Adult Drosophila Characterized by GAL4 Drivers , 2009, Journal of neurogenetics.

[79]  T. Tully,et al.  Fruit flies and intellectual disability , 2009, Fly.

[80]  Wanhe Li,et al.  Short- and Long-Term Memory in Drosophila Require cAMP Signaling in Distinct Neuron Types , 2009, Current Biology.

[81]  D. Nässel,et al.  Aminergic neurons in the brain of blowflies and Drosophila: dopamine- and tyrosine hydroxylase-immunoreactive neurons and their relationship with putative histaminergic neurons , 2004, Cell and Tissue Research.

[82]  Todd Charlton Sacktor,et al.  Memory enhancement and formation by atypical PKM activity in Drosophila melanogaster , 2002, Nature Neuroscience.

[83]  Yoshinori Aso,et al.  Specific Dopaminergic Neurons for the Formation of Labile Aversive Memory , 2010, Current Biology.

[84]  S. Fahrbach.  Structure of the mushroom bodies of the insect brain. , 2006, Annual review of entomology.

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

[86]  T. Tully,et al.  Defective Learning in Mutants of the Drosophila Gene for a Regulatory Subunit of cAMP-Dependent Protein Kinase , 1997, The Journal of Neuroscience.

[87]  Michael B. Reiser,et al.  Visual Place Learning in Drosophila melanogaster , 2011, Nature.

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

[89]  Y. Jan,et al.  dunce, a mutant of Drosophila deficient in learning. , 1976, Proceedings of the National Academy of Sciences of the United States of America.

[90]  [Initial activity and voluntary behavior in animals]. , 1983, Die Naturwissenschaften.

[91]  Martin Heisenberg,et al.  Extinction Antagonizes Olfactory Memory at the Subcellular Level , 2002, Neuron.

[92]  W. Quinn,et al.  Classical conditioning and retention in normal and mutantDrosophila melanogaster , 1985, Journal of Comparative Physiology A.

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

[94]  James G. Burns,et al.  Use of Spatial Information and Search Strategies in a Water Maze Analog in Drosophila melanogaster , 2010, PloS one.

[95]  W. Harris,et al.  Conditioned behavior in Drosophila melanogaster. , 1974, Proceedings of the National Academy of Sciences of the United States of America.

[96]  Ronald L. Davis,et al.  Preferential expression of the drosophila rutabaga gene in mushroom bodies, neural centers for learning in insects , 1992, Neuron.

[97]  M. Heisenberg,et al.  Vision in Drosophila: Genetics of Microbehavior , 2011 .

[98]  M. Heisenberg,et al.  The memory template in Drosophila pattern vision at the flight simulator , 1999, Vision Research.

[99]  T. Zars,et al.  The conserved protein kinase-A target motif in synapsin of Drosophila is effectively modified by pre-mRNA editing , 2006, BMC Neuroscience.

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

[101]  N. Strausfeld,et al.  Evolution, discovery, and interpretations of arthropod mushroom bodies. , 1998, Learning & memory.

[102]  N. Philip,et al.  Conditional Rescue of Olfactory Learning and Memory Defects in Mutants of the 14-3-3ζ Gene leonardo , 2001, The Journal of Neuroscience.

[103]  Roland Strauss,et al.  Mushroom Bodies Enhance Initial Motor Activity in drosophila , 2009, Journal of neurogenetics.

[104]  Troy Zars,et al.  High and low temperatures have unequal reinforcing properties in Drosophila spatial learning , 2006, Journal of Comparative Physiology A.

[105]  Ronald L. Davis,et al.  The Drosophila learning and memory gene rutabaga encodes a Ca 2+ calmodulin -responsive , 1992, Cell.

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

[107]  S. Benzer.  BEHAVIORAL MUTANTS OF Drosophila ISOLATED BY COUNTERCURRENT DISTRIBUTION. , 1967, Proceedings of the National Academy of Sciences of the United States of America.

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

[109]  Y. Dudai,et al.  A defective conditioned behavior and a defective adenylate cyclase in theDrosophila mutantrutabaga , 1984, Journal of Comparative Physiology A.

[110]  Shamik Dasgupta,et al.  There are many ways to train a fly , 2009, Fly.

[111]  Y. Zhong,et al.  Requirement of Drosophila NF1 for activation of adenylyl cyclase by PACAP38-like neuropeptides. , 1997, Science.

[112]  John H Byrne,et al.  New Perspectives on Classical Conditioning: a Synthesis of Hebbian and Non-Hebbian Mechanisms , 1998, Neuron.

[113]  Tim Tully,et al.  nalyot, a Mutation of the Drosophila Myb-Related Adf1 Transcription Factor, Disrupts Synapse Formation and Olfactory Memory , 2000, Neuron.

[114]  Troy Zars,et al.  Place memory formation in Drosophila is independent of proper octopamine signaling , 2010, Journal of Comparative Physiology A.

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

[116]  S. Waddell,et al.  Drosophila olfactory memory: single genes to complex neural circuits , 2007, Nature Reviews Neuroscience.

[117]  Ronald L. Davis,et al.  A Distinct Set of Drosophila Brain Neurons Required for Neurofibromatosis Type 1-Dependent Learning and Memory , 2010, The Journal of Neuroscience.

[118]  Michael J. Krashes,et al.  Drosophila Dorsal Paired Medial Neurons Provide a General Mechanism for Memory Consolidation , 2006, Current Biology.

[119]  Tim Tully,et al.  Excess protein synthesis in Drosophila Fragile X mutants impairs long-term memory , 2008, Nature Neuroscience.

[120]  W. Quinn,et al.  Reward learning in normal and mutant Drosophila. , 1983, Proceedings of the National Academy of Sciences of the United States of America.

[121]  Ronald L. Davis,et al.  Defect in cyclic AMP phosphodiesterase due to the dunce mutation of learning in Drosophila melanogaster , 1981, Nature.

[122]  Jean-René Martin,et al.  Neuropeptides in the Drosophila central complex in modulation of locomotor behavior , 2010, Journal of Experimental Biology.

[123]  Troy Zars,et al.  Reinforcement pre-exposure enhances spatial memory formation in Drosophila , 2007, Journal of Comparative Physiology A.

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

[125]  K. Min,et al.  The Drosophila homolog of Down's syndrome critical region 1 gene regulates learning: Implications for mental retardation , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[126]  Martin Schwaerzel,et al.  Signaling at A-Kinase Anchoring Proteins Organizes Anesthesia-Sensitive Memory in Drosophila , 2007, The Journal of Neuroscience.

[127]  Thomas Preat,et al.  PKA Dynamics in a Drosophila Learning Center: Coincidence Detection by Rutabaga Adenylyl Cyclase and Spatial Regulation by Dunce Phosphodiesterase , 2010, Neuron.

[128]  M Heisenberg,et al.  Mushroom bodies suppress locomotor activity in Drosophila melanogaster. , 1998, Learning & memory.

[129]  Ronald L. Davis,et al.  The cyclic AMP phosphodiesterase encoded by the drosophila dunce gene is concentrated in the mushroom body neuropil , 1991, Neuron.

[130]  Ronald L. Davis,et al.  Integrin-mediated short-term memory in Drosophila , 1998, Nature.

[131]  Martin Heisenberg.  Initiale Aktivität und Willkürverhalten bei Tieren , 2004, Naturwissenschaften.

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

[133]  M. Heisenberg,et al.  Neuronal architecture of the central complex in Drosophila melanogaster , 2004, Cell and Tissue Research.

[134]  Ronald L. Davis,et al.  Drosophila fasciclinII Is Required for the Formation of Odor Memories and for Normal Sensitivity to Alcohol , 2001, Cell.

[135]  Thomas Preat,et al.  Drosophila long-term memory formation involves regulation of cathepsin activity , 2004, Nature.

[136]  P. Greengard,et al.  Writing Memories with Light-Addressable Reinforcement Circuitry , 2009, Cell.

[137]  Ronald L. Davis,et al.  Thirty years of olfactory learning and memory research in Drosophila melanogaster , 2005, Progress in Neurobiology.

[138]  Ann-Shyn Chiang,et al.  Specific requirement of NMDA receptors for long-term memory consolidation in Drosophila ellipsoid body , 2007, Nature Neuroscience.

[139]  H. Bülthoff,et al.  Recurrent inversion of visual orientation in the walking fly,Drosophila melanogaster , 1982, Journal of comparative physiology.

[140]  T. Préat,et al.  The Drosophila learning and memory gene linotte encodes a putative receptor tyrosine kinase homologous to the human RYK gene product , 1995, FEBS letters.

[141]  M Heisenberg,et al.  Tissue-specific expression of a type I adenylyl cyclase rescues the rutabaga mutant memory defect: in search of the engram. , 2000, Learning & memory.

[142]  Zhefeng Gong,et al.  Differential roles of the fan-shaped body and the ellipsoid body in Drosophila visual pattern memory. , 2009, Learning & memory.

[143]  S. Waddell,et al.  Rapid Consolidation to a radish and Protein Synthesis-Dependent Long-Term Memory after Single-Session Appetitive Olfactory Conditioning in Drosophila , 2008, The Journal of Neuroscience.

[144]  M. Mizunami,et al.  Roles of octopaminergic and dopaminergic neurons in mediating reward and punishment signals in insect visual learning , 2006, The European journal of neuroscience.

[145]  Troy Zars,et al.  Short-term memories in Drosophila are governed by general and specific genetic systems. , 2010, Learning & memory.

[146]  T. Tully,et al.  Molecular cloning of linotte in Drosophila: A novel gene that functions in adults during associative learning , 1995, Neuron.

[147]  Ronald L. Davis,et al.  Olfactory Learning Deficits in Mutants for leonardo, a Drosophila Gene Encoding a 14-3-3 Protein , 1996, Neuron.

[148]  M Heisenberg,et al.  Localization of a short-term memory in Drosophila. , 2000, Science.

[149]  T. Tully,et al.  Effects of a conditional Drosophila PKA mutant on olfactory learning and memory. , 1996, Learning & memory.

[150]  R. Davis,et al.  Tripartite mushroom body architecture revealed by antigenic markers. , 1998, Learning & memory.

[151]  J. Armstrong,et al.  Structure of the adult central complex in Drosophila: Organization of distinct neuronal subsets , 2010, The Journal of comparative neurology.

[152]  Zhefeng Gong,et al.  Visual pattern memory requires foraging function in the central complex of Drosophila. , 2008, Learning & memory.

[153]  A. Chiang,et al.  Drosophila PQBP1 Regulates Learning Acquisition at Projection Neurons in Aversive Olfactory Conditioning , 2010, The Journal of Neuroscience.

[154]  D. Guarnieri,et al.  The arouser EPS8L3 Gene Is Critical for Normal Memory in Drosophila , 2011, PloS one.

[155]  K. Han,et al.  D1 Dopamine Receptor dDA1 Is Required in the Mushroom Body Neurons for Aversive and Appetitive Learning in Drosophila , 2007, The Journal of Neuroscience.

[156]  T. Tully,et al.  Developmental Expression of an amn+ Transgene Rescues the Mutant Memory Defect of amnesiacAdults , 1999, The Journal of Neuroscience.

[157]  W. Quinn,et al.  The Drosophila radish gene encodes a protein required for anesthesia-resistant memory , 2006, Proceedings of the National Academy of Sciences.

[158]  G. Roman,et al.  G(o) signaling is required for Drosophila associative learning , 2006, Nature Neuroscience.

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

[160]  T. Zars.  Neuroscience: Flies race to a safe place , 2011, Nature.

[161]  Binyan Lu,et al.  Forgetting Is Regulated through Rac Activity in Drosophila , 2010, Cell.

[162]  Sunhong Kim,et al.  Mitochondrial dysfunction in Drosophila PINK1 mutants is complemented by parkin , 2006, Nature.

[163]  M. Heisenberg,et al.  Vision in Drosophila , 1984 .

[164]  T. Kawecki,et al.  Natural polymorphism affecting learning and memory in Drosophila , 2007, Proceedings of the National Academy of Sciences.

[165]  L. Kahsai,et al.  Chemical neuroanatomy of the Drosophila central complex: Distribution of multiple neuropeptides in relation to neurotransmitters , 2011, The Journal of comparative neurology.

[166]  Troy Zars,et al.  Lack of prediction for high-temperature exposures enhances Drosophila place learning , 2010, Journal of Experimental Biology.