A permissive role of mushroom body α/β core neurons in long-term memory consolidation in Drosophila

Current Biology

Volumn 22, Issue 21, 2012, Pages 1981-1989

  Huang, Cheng ^a   Zheng, Xingguo ^a   Zhao, Hong ^a   Li, Min ^b   Wang, Pengzhi ^a   Xie, Zhiyong ^a   Wang, Lei ^a   Zhong, Yi ^a,c  

^a TSINGHUA UNIVERSITY   (China)

^b THE FIRST AFFILIATED HOSPITAL OF NANJING MEDICAL UNIVERSITY   (China)

^c Howard Hughes Medical Institute Cold Spring Harbor Laboratory Cold Spring Harbor   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DROSOPHILA PROTEIN; EPHRIN RECEPTOR A5; HIGHWIRE PROTEIN, DROSOPHILA; MITOGEN ACTIVATED PROTEIN KINASE KINASE KINASE; NERVE PROTEIN; SMALL INTERFERING RNA; STRESS ACTIVATED PROTEIN KINASE; UBIQUITIN PROTEIN LIGASE; WALLENDA PROTEIN, DROSOPHILA;

ANIMAL; ARTICLE; CONDITIONING; DROSOPHILA; DRUG ANTAGONISM; GENETICS; LONG TERM MEMORY; METABOLISM; MUSHROOM BODY; NERVE CELL; ODOR; OLFACTORY SYSTEM; PHYSIOLOGY; RNA INTERFERENCE;

ANIMALS; CONDITIONING (PSYCHOLOGY); DROSOPHILA; DROSOPHILA PROTEINS; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MAP KINASE KINASE KINASES; MEMORY, LONG-TERM; MUSHROOM BODIES; NERVE TISSUE PROTEINS; NEURONS; OLFACTORY PATHWAYS; RECEPTOR, EPHA5; RNA INTERFERENCE; RNA, SMALL INTERFERING; SMELL; UBIQUITIN-PROTEIN LIGASES;

BASIDIOMYCOTA;

EID: 84868518423     PISSN: 09609822     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cub.2012.08.048     Document Type: Article

References (50)

1. T.J. Carew, H.M. Pinsker, and E.R. Kandel Long-term habituation of a defensive withdrawal reflex in aplysia Science 175 1972 451 454
2. T. Tully, T. Preat, S.C. Boynton, and M. Del Vecchio Genetic dissection of consolidated memory in Drosophila Cell 79 1994 35 47
3. E.R. Kandel The molecular biology of memory storage: a dialogue between genes and synapses Science 294 2001 1030 1038
4. R.D. Hawkins, E.R. Kandel, and C.H. Bailey Molecular mechanisms of memory storage in Aplysia Biol. Bull. 210 2006 174 191
5. D. Fulton, I. Kemenes, R.J. Andrew, and P.R. Benjamin A single time-window for protein synthesis-dependent long-term memory formation after one-trial appetitive conditioning Eur. J. Neurosci. 21 2005 1347 1358
6. R. Sugai, S. Azami, H. Shiga, T. Watanabe, H. Sadamoto, S. Kobayashi, D. Hatakeyama, Y. Fujito, K. Lukowiak, and E. Ito One-trial conditioned taste aversion in Lymnaea: good and poor performers in long-term memory acquisition J. Exp. Biol. 210 2007 1225 1237
7. M.J. Krashes, and S. Waddell Rapid consolidation to a radish and protein synthesis-dependent long-term memory after single-session appetitive olfactory conditioning in Drosophila J. Neurosci. 28 2008 3103 3113
8. J. Colomb, L. Kaiser, M.A. Chabaud, and T. Preat Parametric and genetic analysis of Drosophila appetitive long-term memory and sugar motivation Genes Brain Behav. 8 2009 407 415
9. J. Garcia, D.J. Kimeldorf, and R.A. Koelling Conditioned aversion to saccharin resulting from exposure to gamma radiation Science 122 1955 157 158
10. S.M. McBride, G. Giuliani, C. Choi, P. Krause, D. Correale, K. Watson, G. Baker, and K.K. Siwicki Mushroom body ablation impairs short-term memory and long-term memory of courtship conditioning in Drosophila melanogaster Neuron 24 1999 967 977
11. F. Mery, and T.J. Kawecki A cost of long-term memory in Drosophila Science 308 2005 1148
12. T. Tully, and W.G. Quinn Classical conditioning and retention in normal and mutant Drosophila melanogaster J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 157 1985 263 277
13. C. Margulies, T. Tully, and J. Dubnau Deconstructing memory in Drosophila Curr. Biol. 15 2005 R700 R713
14. J.C.P. Yin, J.S. Wallach, M. Del Vecchio, E.L. Wilder, H. Zhou, W.G. Quinn, and T. Tully Induction of a dominant negative CREB transgene specifically blocks long-term memory in Drosophila Cell 79 1994 49 58
15. A. Pascual, and T. Préat Localization of long-term memory within the Drosophila mushroom body Science 294 2001 1115 1117
16. M.J. Krashes, A.C. Keene, B. Leung, J.D. Armstrong, and S. Waddell Sequential use of mushroom body neuron subsets during Drosophila odor memory processing Neuron 53 2007 103 115
17. C.C. Chen, J.K. Wu, H.W. Lin, T.P. Pai, T.F. Fu, C.L. Wu, T. Tully, and A.S. Chiang Visualizing long-term memory formation in two neurons of the Drosophila brain Science 335 2012 678 685
18. H.I. Wan, A. DiAntonio, R.D. Fetter, K. Bergstrom, R. Strauss, and C.S. Goodman Highwire regulates synaptic growth in Drosophila Neuron 26 2000 313 329
19. C.A. Collins, Y.P. Wairkar, S.L. Johnson, and A. DiAntonio Highwire restrains synaptic growth by attenuating a MAP kinase signal Neuron 51 2006 57 69
20. C. Wu, Y.P. Wairkar, C.A. Collins, and A. DiAntonio Highwire function at the Drosophila neuromuscular junction: spatial, structural, and temporal requirements J. Neurosci. 25 2005 9557 9566
21. J.E. Shin, and A. DiAntonio Highwire regulates guidance of sister axons in the Drosophila mushroom body J. Neurosci. 31 2011 17689 17700
22. H. Zhao, X. Zheng, X. Yuan, L. Wang, X. Wang, Y. Zhong, Z. Xie, and T. Tully ben Functions with scamp during synaptic transmission and long-term memory formation in Drosophila J. Neurosci. 29 2009 414 424
23. W.G. Quinn, and Y. Dudai Memory phases in Drosophila Nature 262 1976 576 577
24. G. Roman, K. Endo, L. Zong, and R.L. Davis P[Switch], a system for spatial and temporal control of gene expression in Drosophila melanogaster Proc. Natl. Acad. Sci. USA 98 2001 12602 12607
25. T. Riemensperger, T. Völler, P. Stock, E. Buchner, and A. Fiala Punishment prediction by dopaminergic neurons in Drosophila Curr. Biol. 15 2005 1953 1960
26. N.K. Tanaka, H. Tanimoto, and K. Ito Neuronal assemblies of the Drosophila mushroom body J. Comp. Neurol. 508 2008 711 755
27. K.M.C. O'Dell, J.D. Armstrong, M.Y. Yang, and K. Kaiser Functional dissection of the Drosophila mushroom bodies by selective feminization of genetically defined subcompartments Neuron 15 1995 55 61
28. K.J. Sepp, J. Schulte, and V.J. Auld Peripheral glia direct axon guidance across the CNS/PNS transition zone Dev. Biol. 238 2001 47 63
29. T. Adachi-Yamada, M. Nakamura, K. Irie, Y. Tomoyasu, Y. Sano, E. Mori, S. Goto, N. Ueno, Y. Nishida, and K. Matsumoto p38 mitogen-activated protein kinase can be involved in transforming growth factor beta superfamily signal transduction in Drosophila wing morphogenesis Mol. Cell. Biol. 19 1999 2322 2329
30. S.E. McGuire, P.T. Le, A.J. Osborn, K. Matsumoto, and R.L. Davis Spatiotemporal rescue of memory dysfunction in Drosophila Science 302 2003 1765 1768
31. T. Kitamoto Conditional modification of behavior in Drosophila by targeted expression of a temperature-sensitive shibire allele in defined neurons J. Neurobiol. 47 2001 81 92
32. B. Bingol, and M. Sheng Deconstruction for reconstruction: the role of proteolysis in neural plasticity and disease Neuron 69 2011 22 32
33. Y.H. Jiang, D. Armstrong, U. Albrecht, C.M. Atkins, J.L. Noebels, G. Eichele, J.D. Sweatt, and A.L. Beaudet Mutation of the Angelman ubiquitin ligase in mice causes increased cytoplasmic p53 and deficits of contextual learning and long-term potentiation Neuron 21 1998 799 811
34. E. Pavlopoulos, M. Anezaki, and E.M.C. Skoulakis Neuralized is expressed in the α/β lobes of adult Drosophila mushroom bodies and facilitates olfactory long-term memory formation Proc. Natl. Acad. Sci. USA 105 2008 14674 14679
35. T. Abel, K.C. Martin, D. Bartsch, and E.R. Kandel Memory suppressor genes: inhibitory constraints on the storage of long-term memory Science 279 1998 338 341
36. M.R. Pagani, K. Oishi, B.D. Gelb, and Y. Zhong The phosphatase SHP2 regulates the spacing effect for long-term memory induction Cell 139 2009 186 198
37. M. Heisenberg Mushroom body memoir: from maps to models Nat. Rev. Neurosci. 4 2003 266 275
38. J.S. de Belle, and M. Heisenberg Associative odor learning in Drosophila abolished by chemical ablation of mushroom bodies Science 263 1994 692 695
39. J. Dubnau, L. Grady, T. Kitamoto, and T. Tully Disruption of neurotransmission in Drosophila mushroom body blocks retrieval but not acquisition of memory Nature 411 2001 476 480
40. S.E. McGuire, P.T. Le, and R.L. Davis The role of Drosophila mushroom body signaling in olfactory memory Science 293 2001 1330 1333
41. T. Lee, A. Lee, and L. Luo Development of the Drosophila mushroom bodies: sequential generation of three distinct types of neurons from a neuroblast Development 126 1999 4065 4076
42. J.R. Crittenden, E.M. Skoulakis, K.A. Han, D. Kalderon, and R.L. Davis Tripartite mushroom body architecture revealed by antigenic markers Learn. Mem. 5 1998 38 51
43. G. Isabel, A. Pascual, and T. Preat Exclusive consolidated memory phases in Drosophila Science 304 2004 1024 1027
44. Y. Wang, A. Mamiya, A.S. Chiang, and Y. Zhong Imaging of an early memory trace in the Drosophila mushroom body J. Neurosci. 28 2008 4368 4376
45. A.L. Blum, W. Li, M. Cressy, and J. Dubnau Short- and long-term memory in Drosophila require cAMP signaling in distinct neuron types Curr. Biol. 19 2009 1341 1350
46. H. Qin, M. Cressy, W. Li, J.S. Coravos, S.A. Izzi, and J. Dubnau Gamma neurons mediate dopaminergic input during aversive olfactory memory formation in Drosophila Curr. Biol. 22 2012 608 614
47. D. Yu, D.B.G. Akalal, and R.L. Davis Drosophila α/β mushroom body neurons form a branch-specific, long-term cellular memory trace after spaced olfactory conditioning Neuron 52 2006 845 855
48. D.B. Akalal, D. Yu, and R.L. Davis A late-phase, long-term memory trace forms in the γ neurons of Drosophila mushroom bodies after olfactory classical conditioning J. Neurosci. 30 2010 16699 16708
49. R.L. Davis Traces of Drosophila memory Neuron 70 2011 8 19
50. Y. Aso, K. Grübel, S. Busch, A.B. Friedrich, I. Siwanowicz, and H. Tanimoto The mushroom body of adult Drosophila characterized by GAL4 drivers J. Neurogenet. 23 2009 156 172