Genes and Circuits for Olfactory-Associated Long-Term Memory in Drosophila

References

• Alberini C. M., Ghirardi M., Metz R., Kandel E. R. C/EBP is an immediate-early gene required for the consolidation of long-term facilitation in Aplysia. Cell 1994; 76: 1099–1114
   PubMed Web of Science ®Google Scholar
• Artavanis-Tsakonas S., Rand M. D., Lake R. J. Notch signaling: cell fate control and signal integration in development. Science 1999; 284: 770–776
   PubMed Web of Science ®Google Scholar
• Ashraf S. I., McLoon A. L., Sclarsic S. M., Kunes S. Synaptic protein synthesis associated with memory is regulated by the RISC pathway in Drosophila. Cell 2006; 124: 191–205
   PubMed Web of Science ®Google Scholar
• Bailey C. H., Alberini C., Ghirardi M., Kandel E. R. Molecular and structural changes underlying long-term memory storage in Aplysia. Adv Sec Mess Phosphoprot Res 1994; 29: 529–544
   PubMedGoogle Scholar
• Barnea G., O'Donnell S., Mancia F., Sun X., Nemes A., Mendelsohn M., Axel R. Odorant receptors on axon termini in the brain. Science 2004; 304: 1468
   PubMed Web of Science ®Google Scholar
• Bartsch D., Ghirardi M., Skehel P. A., Karl K. A., Herder S. P., Chen M., Bailey C. H., Kandel E. R. Aplysia CREB2 represses long-term facilitation: relief of repression converts transient facilitation into long-term functional and structural change. Cell 1995; 83: 979–992
   PubMed Web of Science ®Google Scholar
• Bourtchuladze R., Frenguelli B., Blendy J., Cioffi D., Schutz G., Silva A. J. Deficient long-term memory in mice with a targeted mutation of the cAMP-responsive element-binding protein. Cell 1994; 79: 59–68
   PubMed Web of Science ®Google Scholar
• Boynton S., Tully T. latheo, a new gene involved in associative learning and memory in Drosophila melanogaster, identified from P-element mutagenesis. Genetics 1992; 131: 655–672
   PubMed Web of Science ®Google Scholar
• Brooks D. N., Baddeley A. D. What can amnesic patients learn?. Neuropsychologia 1976; 14: 111–122
   PubMed Web of Science ®Google Scholar
• Carew T. J., Pinsker H. M., Kandel E. R. Long-term habituation of a defensive withdrawal reflex in Aplysia. Science 1972; 175: 451–454
   PubMed Web of Science ®Google Scholar
• Chang K. T., Shi Y. J., Min K. T. The Drosophila homolog of Down syndrome critical region 1 gene regulates learning: implications for mental retardation. Proc Natl Acad Sci U S A 2003; 100: 15794–15799
   PubMed Web of Science ®Google Scholar
• Chen C. N., Denome S., Davis R. L. Molecular analysis of cDNA clones and the corresponding genomic coding sequences of the Drosophila dunce+ gene, the structural gene for cAMP phosphodiesterase. Proc Natl Acad Sci U S A 1986; 83: 9313–9317
   PubMed Web of Science ®Google Scholar
• Cheng Y., Endo K., Wu K., Rodan A. R., Heberlein U., Davis R. L. Drosophila fasciclinII is required for the formation of odor memories and for normal sensitivity to alcohol. Cell 2001; 105: 757–768
   PubMed Web of Science ®Google Scholar
• Comas D., Petit F., Preat T. Drosophila long-term memory formation involves regulation of cathepsin activity. Nature 2004; 430: 460–463
   PubMed Web of Science ®Google Scholar
• Connolly J. B., Roberts I. J., Armstrong J. D., Kaiser K., Forte M., Tully T., O'Kane C. J. Associative learning disrupted by impaired Gs signaling in Drosophila mushroom bodies. Science 1996; 274: 2104–2107
   PubMed Web of Science ®Google Scholar
• Cowan T. M., Siegel R. W. Mutational and pharmacological alterations of neuronal membrane function disrupt conditioning in Drosophila. J Neurogenet 1984; 1: 333–344
   PubMedGoogle Scholar
• Crittenden J. R., Skoulakis E. M., Han K. A., Kalderon D., Davis R. L. Tripartite mushroom body architecture revealed by antigenic markers. Learn Mem 1998; 5: 38–51
   PubMed Web of Science ®Google Scholar
• Davis H. P., Rosenzweig M. R., Grove E. A., Bennett E. L. Investigation of the reported protective effect of cycloheximide on memory. Pharmacol Biochem Behav 1984; 20: 405–413
   PubMed Web of Science ®Google Scholar
• Davis H. P., Squire L. R. Protein synthesis and memory: a review. Psychol Bull 1984; 96: 518–559
   PubMed Web of Science ®Google Scholar
• Davis R. L. Physiology and biochemistry of Drosophila learning mutants. Physiol Rev 1996; 76: 299–317
   PubMed Web of Science ®Google Scholar
• Davis R. L. Olfactory memory formation in Drosophila: from molecular to systems neuroscience. Annu Rev Neurosci 2005; 28: 275–302
   PubMed Web of Science ®Google Scholar
• de Belle J. S., Heisenberg M. Associative odor learning in Drosophila abolished by chemical ablation of mushroom bodies. Science 1994; 263: 692–695
   PubMed Web of Science ®Google Scholar
• de Belle J. S., Heisenberg M. Expression of Drosophila mushroom body mutations in alternative genetic backgrounds: a case study of the mushroom body miniature gene (mbm). Proc Natl Acad Sci U S A 1996; 93: 9875–9880
   PubMed Web of Science ®Google Scholar
• DeJianne D., McGuire T. R., Pruzan-Hotchkiss A. Conditioned suppression of proboscis extension in Drosophila melanogaster. J Comp Psychol 1985; 99: 74–80
   PubMed Web of Science ®Google Scholar
• DeZazzo J., Sandstrom D., de Belle S., Velinzon K., Smith P., Grady L., DelVecchio M., Ramaswami M., Tully T. nalyot, a mutation of the Drosophila myb-related Adf1 transcription factor, disrupts synapse formation and olfactory memory. Neuron 2000; 27: 145–158
   PubMed Web of Science ®Google Scholar
• DeZazzo J., Xia S., Christensen J., Velinzon K., Tully T. Developmental expression of an amn(+) transgene rescues the mutant memory defect of amnesiac adults. J Neurosci 1999; 19: 8740–8746
   PubMed Web of Science ®Google Scholar
• Didelot G., Molinari F., Tchenio P., Comas D., Milhiet E., Munnich A., Colleaux L., Preat T. Tequila, a neurotrypsin ortholog, regulates long-term memory formation in Drosophila. Science 2006; 313: 851–853
   PubMed Web of Science ®Google Scholar
• Dingledine R., Borges K., Bowie D., Traynelis S. F. The glutamate receptor ion channels. Pharmacol Rev 1999; 51: 7–61
   PubMed Web of Science ®Google Scholar
• Dubnau J., Chiang A. S., Grady L., Barditch J., Gossweiler S., McNeil J., Smith P., Buldoc F., Scott R., Certa U., Broger C., Tully T. The staufen/pumilio pathway is involved in Drosophila long-term memory. Curr Biol 2003; 13: 286–296
   PubMed Web of Science ®Google Scholar
• Dubnau J., Grady L., Kitamoto T., Tully T. Disruption of neurotransmission in Drosophila mushroom body blocks retrieval but not acquisition of memory. Nature 2001; 411: 476–480
   PubMed Web of Science ®Google Scholar
• Dubnau J., Tully T. Gene discovery in Drosophila: new insights for learning and memory. Annu Rev Neurosci 1998; 21: 407–444
   PubMed Web of Science ®Google Scholar
• Dudai Y. The neurobiology of consolidations, or, how stable is the engram?. Annu Rev Psychol 2004; 55: 51–86
   PubMed Web of Science ®Google Scholar
• Dudai Y., Jan Y. N., Byers D., Quinn W. G., Benzer S. dunce, a mutant of Drosophila deficient in learning. Proc Natl Acad Sci U S A,, .1688 1976; 73: 1684
   PubMed Web of Science ®Google Scholar
• Dura J. M., Preat T., Tully T. Identification of linotte, a new gene affecting learning and memory in Drosophila melanogaster. J Neurogenet 1993; 9: 1–14
   PubMed Web of Science ®Google Scholar
• Feany M. B., Quinn W. G. A neuropeptide gene defined by the Drosophila memory mutant amnesiac. Science 1995; 268: 869–873
   PubMed Web of Science ®Google Scholar
• Fiala A. Olfaction and olfactory learning in Drosophila: recent progress. Curr Opin Neurobiol 2007; 17: 720–726
   PubMed Web of Science ®Google Scholar
• Flood J. F., Jarvik M. E., Bennett E. L., Orme A. E., Rosenzweig M. R. Protein synthesis inhibition and memory for pole jump active avoidance and extinction. Pharmacol Biochem Behav 1977; 7: 71–77
   PubMed Web of Science ®Google Scholar
• Folkers E., Waddell S., Quinn W. G. The Drosophila radish gene encodes a protein required for anesthesia-resistant memory. Proc Natl Acad Sci U S A 2006; 103: 17496–17500
   PubMed Web of Science ®Google Scholar
• Frankland P. W., Bontempi B. The organization of recent and remote memories. Nat Rev Neurosci 2005; 6: 119–130
   PubMed Web of Science ®Google Scholar
• Frost W. N., Castellucci V. F., Hawkins R. D., Kandel E. R. Monosynaptic connections made by the sensory neurons of the gill- and siphon-withdrawal reflex in Aplysia participate in the storage of long-term memory for sensitization. Proc Natl Acad Sci U S A 1985; 82: 8266–8269
   PubMed Web of Science ®Google Scholar
• Fuentes J. J., Pritchard M. A., Planas A. M., Bosch A., Ferrer I., Estivill X. A new human gene from the Down syndrome critical region encodes a proline-rich protein highly expressed in fetal brain and heart. Hum Mol Genet 1995; 4: 1935–1944
   PubMed Web of Science ®Google Scholar
• Gailey D. A., Villella A., Tully T. Reassessment of the effect of biological rhythm mutations on learning in Drosophila melanogaster. J Comp Physiol [A] 1991; 169: 685–697
   PubMed Web of Science ®Google Scholar
• Ge H., Krishnan P., Liu L., Krishnan B., Davis R. L., Hardin P. E., Roman G. A Drosophila nonvisual arrestin is required for the maintenance of olfactory sensitivity. Chem Senses 2006; 31: 49–62
   PubMed Web of Science ®Google Scholar
• Ge X., Hannan F., Xie Z., Feng C., Tully T., Zhou H., Zhong Y. Notch signaling in Drosophila long-term memory formation. Proc Natl Acad Sci U S A 2004; 101: 10172–10176
   PubMed Web of Science ®Google Scholar
• Godenschwege T. A., Reisch D., Diegelmann S., Eberle K., Funk N., Heisenberg M., Hoppe V., Hoppe J., Klagges B. R., Martin J. R., Nikitina E. A., Putz G., Reifegerste R., Reisch N., Rister J., Schaupp M., Scholz H., Schwarzel M., Werner U., Zars T. D., Buchner S., Buchner E. Flies lacking all synapsins are unexpectedly healthy but are impaired in complex behaviour. Eur J Neurosci 2004; 20: 611–622
   PubMed Web of Science ®Google Scholar
• Gold P. E., Hankins L., Edwards R. M., Chester J., McGaugh J. L. Memory interference and facilitation with post-trial amygdala stimulation: effect on memory varies with footshock level. Brain Res 1975; 86: 509–513
   PubMed Web of Science ®Google Scholar
• Goodwin S. F., Del Vecchio M., Velinzon K., Hogel C., Russell S. R., Tully T., Kaiser K. Defective learning in mutants of the Drosophila gene for a regulatory subunit of cAMP-dependent protein kinase. J Neurosci 1997; 17: 8817–8827
   PubMed Web of Science ®Google Scholar
• Grotewiel M. S., Beck C. D., Wu K. H., Zhu X. R., Davis R. L. Integrin-mediated short-term memory in Drosophila. Nature 1998; 391: 455–460
   PubMed Web of Science ®Google Scholar
• Guo H. F., Tong J., Hannan F., Luo L., Zhong Y. A neurofibromatosis-1-regulated pathway is required for learning in Drosophila. Nature 2000; 403: 895–898
   PubMed Web of Science ®Google Scholar
• Hammer M., Menzel R. Learning and memory in the honeybee. J Neurosci 1995; 15: 1617–1630
   PubMed Web of Science ®Google Scholar
• Han P. L., Levin L. R., Reed R. R., Davis R. L. Preferential expression of the Drosophila rutabaga gene in mushroom bodies, neural centers for learning in insects. Neuron 1992; 9: 619–627
   PubMed Web of Science ®Google Scholar
• Hanesch U., Fischback K.-F., Heisenberg M. Neuronal architecture of the central complex in Drosophila melanogaster. Cell Tissue Res 1989; 257: 343–366
   Web of Science ®Google Scholar
• Hannan F., Ho I., Tong J. J., Zhu Y., Nurnberg P., Zhong Y. Effect of neurofibromatosis type I mutations on a novel pathway for adenylyl cyclase activation requiring neurofibromin and Ras. Hum Mol Genet 2006; 15: 1087–1098
   PubMed Web of Science ®Google Scholar
• Heisenberg M. Mutants of brain structure and function: what is the significance of the mushroom bodies for behavior?. Basic Life Sci 1980; 16: 373–390
   PubMedGoogle Scholar
• Heisenberg M. Mushroom body memoir: from maps to models. Nat Rev Neurosci 2003; 4: 266–275
   PubMed Web of Science ®Google Scholar
• Heisenberg M., Borst A., Wagner S., Byers D. Drosophila mushroom body mutants are deficient in olfactory learning. J Neurogenet 1985; 2: 1–30
   PubMed Web of Science ®Google Scholar
• Hirsch J., Tryon R. C. Mass screening and reliable individual measurement in the experimental behavior genetics of lower organisms. Psychol Bull 1956; 53: 402–410
   PubMed Web of Science ®Google Scholar
• Ho I. S., Hannan F., Guo H. F., Hakker I., Zhong Y. Distinct functional domains of neurofibromatosis type 1 regulate immediate versus long-term memory formation. J Neurosci 2007; 27: 6852–6857
   PubMed Web of Science ®Google Scholar
• Huang Y. Y., Li X. C., Kandel E. R. cAMP contributes to mossy fiber LTP by initiating both a covalently mediated early phase and macromolecular synthesis-dependent late phase. Cell 1994; 79: 69–79
   PubMed Web of Science ®Google Scholar
• Isabel G., Pascual A., Preat T. Exclusive consolidated memory phases in Drosophila. Science 2004; 304: 1024–1027
   PubMed Web of Science ®Google Scholar
• Ito K., Suzuki K., Estes P., Ramaswami M., Yamamoto D., Strausfeld N. J. The organization of extrinsic neurons and their implications in the functional roles of the mushroom bodies in Drosophila melanogaster Meigen. Learn Mem 1998; 5: 52–77
   PubMed Web of Science ®Google Scholar
• Karni A., Sagi D. The time course of learning a visual skill. Nature 1993; 365: 250–252
   PubMed Web of Science ®Google Scholar
• Keene A. C., Krashes M. J., Leung B., Bernard J. A., Waddell S. Drosophila dorsal paired medial neurons provide a general mechanism for memory consolidation. Curr Biol 2006; 16: 1524–1530
   PubMed Web of Science ®Google Scholar
• Keene A. C., Waddell S. Drosophila olfactory memory: single genes to complex neural circuits. Nat Rev Neurosci 2007; 8: 341–354
   PubMed Web of Science ®Google Scholar
• Kogan J. H., Frankland P. W., Blendy J. A., Coblentz J., Marowitz Z., Schutz G., Silva A. J. Spaced training induces normal long-term memory in CREB mutant mice. Curr Biol 1997; 7: 1–11
   PubMed Web of Science ®Google Scholar
• Korzets A., Sachs D., Gershkovich R., Soimu U., Bartal G., Kessel B., Dudaiav S., Chlibovsky A. Air in the liver?. Nephrol Dial Transpl 2004; 19: 2672
   PubMed Web of Science ®Google Scholar
• Krashes M. J., Keene A. C., Leung B., Armstrong J. D., Waddell S. Sequential use of mushroom body neuron subsets during Drosophila odor memory processing. Neuron 2007; 53: 103–115
   PubMed Web of Science ®Google Scholar
• Krashes M. J., Waddell S. Rapid consolidation to a radish and protein synthesis-dependent long-term memory after single-session appetitive olfactory conditioning in Drosophila. J Neurosci 2008; 28: 3103–3113
   PubMed Web of Science ®Google Scholar
• Lee T., Lee A., Luo L. Development of the Drosophila mushroom bodies: sequential generation of three distinct types of neurons from a neuroblast. Development 1999; 126: 4065–4076
   PubMed Web of Science ®Google Scholar
• Levin L. R., Han P. L., Hwang P. M., Feinstein P. G., Davis R. L., Reed R. R. The Drosophila learning and memory gene rutabaga encodes a Ca2 + /calmodulin-responsive adenylyl cyclase. Cell 1992; 68: 479–489
   PubMed Web of Science ®Google Scholar
• Li W., Tully T., Kalderon D. Effects of a conditional Drosophila PKA mutant on olfactory learning and memory. Learn Mem 1996; 2: 320–333
   PubMed Web of Science ®Google Scholar
• Livingstone M. S., Sziber P. P., Quinn W. G. Loss of calcium/calmodulin responsiveness in adenylate cyclase of rutabaga, a Drosophila learning mutant. Cell 1984; 37: 205–215
   PubMed Web of Science ®Google Scholar
• Lu Y., Lu Y. S., Shuai Y., Feng C., Tully T., Xie Z., Zhong Y., Zhou H. M. The AKAP Yu is required for olfactory long-term memory formation in Drosophila. Proc Natl Acad Sci U S A 2007; 104: 13792–13797
   PubMed Web of Science ®Google Scholar
• McBain C. J., Mayer M. L. N-methyl-D-aspartic acid receptor structure and function. Physiol Rev 1994; 74: 723–760
   PubMed Web of Science ®Google Scholar
• McBride S. M., Giuliani G., Choi C., Krause P., Correale D., Watson K., Baker G., Siwicki K. K. Mushroom body ablation impairs short-term memory and long-term memory of courtship conditioning in Drosophila melanogaster. Neuron 1999; 24: 967–977
   PubMed Web of Science ®Google Scholar
• McGaugh J. L. Time-dependent processes in memory storage. Science 1966; 153: 1351–1358
   PubMed Web of Science ®Google Scholar
• McGaugh J. L. Impairment and facilitation of memory consolidation. Act Nerv Super (Praha) 1972; 14: 64–74
   PubMedGoogle Scholar
• McGaughey R. W., Murray F. A. Properties of blastokinin: amino acid composition, evidence for subunits, and estimation of isoelectric point. Fertil Steril 1972; 23: 399–404
   PubMed Web of Science ®Google Scholar
• McGuire S. E., Le P. T., Davis R. L. The role of Drosophila mushroom body signaling in olfactory memory. Science 2001; 293: 1330–1333
   PubMed Web of Science ®Google Scholar
• McGuire T. R. Learning in three species of Diptera: the blow fly Phormia regina, the fruit fly Drosophila melanogaster, and the house fly Musca domestica. Behav Genet 1984; 14: 479–526
   PubMed Web of Science ®Google Scholar
• Menon K. P., Sanyal S., Habara Y., Sanchez R., Wharton R. P., Ramaswami M., Zinn K. The translational repressor pumilio regulates presynaptic morphology and controls postsynaptic accumulation of translation factor eIF-4E. Neuron 2004; 44: 663–676
   PubMed Web of Science ®Google Scholar
• Menzel, R., Erber, J., & Mousht, T. (1974). Learning and memory in the honeybee. Experimental analysis of insect behaviour (Barton-Browen, L ed), Springer, Berlin, Germany. pp.195–217.
   Google Scholar
• Menzel R. Neurobiology of learning and memory: the honeybee as a model system. Naturwissenschaften 1983; 70: 504–511
   PubMed Web of Science ®Google Scholar
• Mombaerts P. Seven-transmembrane proteins as odorant and chemosensory receptors. Science 1999; 286: 707–711
   PubMed Web of Science ®Google Scholar
• Montarolo P. G., Goelet P., Castellucci V. F., Morgan J., Kandel E. R., Schacher S. A critical period for macromolecular synthesis in long-term heterosynaptic facilitation in Aplysia. Science 1986; 234: 1249–1254
   PubMed Web of Science ®Google Scholar
• Nakazawa K., McHugh T. J., Wilson M. A., Tonegawa S. NMDA receptors, place cells, and hippocampal spatial memory. Nat Rev Neurosci 2004; 5: 361–372
   PubMed Web of Science ®Google Scholar
• Neuser K., Triphan T., Mronz M., Poeck B., Strauss R. Analysis of a spatial orientation memory in Drosophila. Nature 2008; 453: 1244–1247
   PubMed Web of Science ®Google Scholar
• Nighorn A., Healy M. J., Davis R. L. The cyclic AMP phosphodiesterase encoded by the Drosophila dunce gene is concentrated in the mushroom body neuropil. Neuron 1991; 6: 455–467
   PubMed Web of Science ®Google Scholar
• Pascual A., Huang K. L., Neveu J., Preat T. Neuroanatomy: brain asymmetry and long-term memory. Nature 2004; 427: 605–606
   PubMed Web of Science ®Google Scholar
• Pascual A., Preat T. Localization of long-term memory within the Drosophila mushroom body. Science 2001; 294: 1115–1117
   PubMed Web of Science ®Google Scholar
• Presente A., Boyles R. S., Serway C. N., de Belle J. S., Andres A. J. Notch is required for long-term memory in Drosophila. Proc Natl Acad Sci U S A 2004; 101: 1764–1768
   PubMed Web of Science ®Google Scholar
• Qian M., Pan G., Sun L., Feng C., Xie Z., Tully T., Zhong Y. Receptor-like tyrosine phosphatase PTP10D is required for long-term memory in Drosophila. J Neurosci 2007; 27: 4396–4402
   PubMed Web of Science ®Google Scholar
• Quinn W. G., Dudai Y. Memory phases in Drosophila. Nature 1976; 262: 576–577
   PubMed Web of Science ®Google Scholar
• Quinn W. G., Harris W. A., Benzer S. Conditioned behavior in Drosophila melanogaster. Proc Natl Acad Sci U S A 1974; 71: 708–712
   PubMed Web of Science ®Google Scholar
• Renn S. C., Armstrong J. D., Yang M., Wang Z., An X., Kaiser K., Taghert P. H. Genetic analysis of the Drosophila ellipsoid body neuropil: organization and development of the central complex. J Neurobiol 1999; 41: 189–207
   PubMed Web of Science ®Google Scholar
• Rescorla R. A. Configural” conditioning in discrete-trial bar pressing. J Comp Physiol Psychol 1972; 79: 307–317
   PubMed Web of Science ®Google Scholar
• Rosenblum K., Meiri N., Dudai Y. Taste memory: the role of protein synthesis in gustatory cortex. Behav Neural Biol 1993; 59: 49–56
   PubMedGoogle Scholar
• Siegel R. W., Hall J. C. Conditioned responses in courtship behavior of normal and mutant Drosophila. Proc Natl Acad Sci U S A 1979; 76: 3430–3434
   PubMed Web of Science ®Google Scholar
• Skoulakis E. M., Davis R. L. Olfactory learning deficits in mutants for leonardo, a Drosophila gene encoding a 14-3-3 protein. Neuron 1996; 17: 931–944
   PubMed Web of Science ®Google Scholar
• Skoulakis E. M., Kalderon D., Davis R. L. Preferential expression in mushroom bodies of the catalytic subunit of protein kinase A and its role in learning and memory. Neuron 1993; 11: 197–208
   PubMed Web of Science ®Google Scholar
• Sonderegger, P., & Patthy, L. 2007. Comment on “Tequila, a neurotrypsin ortholog, regulates long-term memory formation in Drosophila.” Science, 316, 1698; author reply, 1698.
   PubMed Web of Science ®Google Scholar
• Squire L. R. The organization and neural substrates of human memory. Int J Neurol 1987; 21–22: 218–222
   PubMedGoogle Scholar
• Stephens K., Riccardi V. M., Rising M., Ng S., Green P., Collins F. S., Rediker K. S., Powers J. A., Parker C., Donis-Keller H. Linkage studies with chromosome 17 DNA markers in 45 neurofibromatosis 1 families. Genomics 1987; 1: 353–357
   PubMedGoogle Scholar
• Struhl G., Adachi A. Nuclear access and action of notch in vivo. Cell 1998; 93: 649–660
   PubMed Web of Science ®Google Scholar
• Strauss R. The central complex and the genetic dissection of locomotor behaviour. Curr Opin Neurobial. 2002; 12: 633–638
   PubMed Web of Science ®Google Scholar
• Suh G. S., Wong A. M., Hergarden A. C., Wang J. W., Simon A. F., Benzer S., Axel R., Anderson D. J. A single population of olfactory sensory neurons mediates an innate avoidance behaviour in Drosophila. Nature 2004; 431: 854–859
   PubMed Web of Science ®Google Scholar
• Tompkins L., Siegel R. W., Gailey D. A., Hall J. C. Conditioned courtship in Drosophila and its mediation by association of chemical cues. Behav Genet 1983; 13: 565–578
   PubMed Web of Science ®Google Scholar
• Tully T. Drosophila learning: behavior and biochemistry. Behav Genet 1984; 14: 527–557
   PubMed Web of Science ®Google Scholar
• Tully T. Physiology of mutations affecting learning and memory in Drosophila—the missing link between gene product and behavior. Trends Neurosci 1991; 14: 163–164
   PubMed Web of Science ®Google Scholar
• Tully T., Bolwig G., Christensen J., Connolly J., DeZazzo J., Dubnau J., Jones C., Pinto S., Regulski M., Svedberg F., Velinzon K. Genetic dissection of memory in Drosophila. J Physiol Paris 1996; 90: 383
   PubMedGoogle Scholar
• Tully T., Preat T., Boynton S. C., Del Vecchio M. Genetic dissection of consolidated memory in Drosophila. Cell 1994; 79: 35–47
   PubMed Web of Science ®Google Scholar
• Tully T., Quinn W. G. Classical conditioning and retention in normal and mutant Drosophila melanogaster. J Comp Physiol [A] 1985; 157: 263–277
   PubMed Web of Science ®Google Scholar
• Vosshall L. B., Amrein H., Morozov P. S., Rzhetsky A., Axel R. A spatial map of olfactory receptor expression in the Drosophila antenna. Cell 1999; 96: 725–736
   PubMed Web of Science ®Google Scholar
• Waddell S., Armstrong J. D., Kitamoto T., Kaiser K., Quinn W. G. The amnesiac gene product is expressed in two neurons in the Drosophila brain that are critical for memory. Cell 2000; 103: 805–813
   PubMed Web of Science ®Google Scholar
• Wiltgen B. J., Brown R. A., Talton L. E., Silva A. J. New circuits for old memories: the role of the neocortex in consolidation. Neuron 2004; 44: 101–108
   PubMed Web of Science ®Google Scholar
• Wolf R., Heisenberg M. Basic organization of operant behavior as revealed in Drosophila flight orientation. J Comp Physiol [A] 1991; 169: 699–705
   PubMed Web of Science ®Google Scholar
• Wolf R., Heisenberg M. Visual space from visual motion: turn integration in tethered flying Drosophila. Learn Mem 1997; 4: 318–327
   PubMed Web of Science ®Google Scholar
• Wu C. L., Xia S., Fu T. F., Wang H., Chen Y. H., Leong D., Chiang A. S., Tully T. Specific requirement of NMDA receptors for long-term memory consolidation in Drosophila ellipsoid body. Nat Neurosci 2007; 10: 1578–1586
   PubMed Web of Science ®Google Scholar
• Xia S., Liu L., Feng C., Guo A. Memory consolidation in Drosophila operant visual learning. Learn Mem 1997; 4: 205–218
   PubMed Web of Science ®Google Scholar
• Xia S., Miyashita T., Fu T. F., Lin W. Y., Wu C. L., Pyzocha L., Lin I. R., Saitoe M., Tully T., Chiang A. S. NMDA receptors mediate olfactory learning and memory in Drosophila. Curr Biol 2005; 15: 603–615
   PubMed Web of Science ®Google Scholar
• Xia S. Z., Feng C. H., Guo A. K. Multiple-phase model of memory consolidation confirmed by behavioral and pharmacological analyses of operant conditioning in Drosophila. Pharmacol Biochem Behav 1998; 60: 809–816
   PubMed Web of Science ®Google Scholar
• Yin J. C., Del Vecchio M., Zhou H., Tully T. CREB as a memory modulator: induced expression of a dCREB2 activator isoform enhances long-term memory in Drosophila. Cell 1995a; 81: 107–115
   PubMed Web of Science ®Google Scholar
• Yin J. C., Wallach J. S., Del Vecchio M., Wilder E. L., Zhou H., Quinn W. G., Tully T. Induction of a dominant negative CREB transgene specifically blocks long-term memory in Drosophila. Cell 1994; 79: 49–58
   PubMed Web of Science ®Google Scholar
• Yin J. C., Wallach J. S., Wilder E. L., Klingensmith J., Dang D., Perrimon N., Zhou H., Tully T., Quinn W. G. A Drosophila CREB/CREM homolog encodes multiple isoforms, including a cyclic AMP-dependent protein kinase-responsive transcriptional activator and antagonist. Mol Cell Biol 1995b; 15: 5123–5130
   PubMed Web of Science ®Google Scholar
• Yu D., Akalal D. B., Davis R. L. Drosophila alpha/beta mushroom body neurons form a branch-specific, long-term cellular memory trace after spaced olfactory conditioning. Neuron 2006; 52: 845–855
   PubMed Web of Science ®Google Scholar
• Yu D., Keene A. C., Srivatsan A., Waddell S., Davis R. L. Drosophila DPM neurons form a delayed and branch-specific memory trace after olfactory classical conditioning. Cell 2005; 123: 945–957
   PubMed Web of Science ®Google Scholar
• Zars T., Fischer M., Schulz R., Heisenberg M. Localization of a short-term memory in Drosophila. Science 2000; 288: 672–675
   PubMed Web of Science ®Google Scholar
• Zhu S., Chiang A. S., Lee T. Development of the Drosophila mushroom bodies: elaboration, remodeling, and spatial organization of dendrites in the calyx. Development 2003; 130: 2603–2610
   PubMed Web of Science ®Google Scholar