Mushroom body efferent neurons responsible for aversive olfactory memory retrieval in Drosophila

Nature Neuroscience

Volumn 14, Issue 7, 2011, Pages 903-910

  Séjourn, Julien ^a   Plaçais, Pierre Yves ^a   Aso, Yoshinori ^b,c   Siwanowicz, Igor ^b   Trannoy, Séverine ^a   Thoma, Vladimiros ^b   Tedjakumala, Stevanus R ^b   Rubin, Gerald M ^c   Tchénio, Paul ^a,d   Ito, Kei ^e   Isabel, Guillaume ^a   Tanimoto, Hiromu ^b   Preat, Thomas ^a  

^a CNRS   (France)

^b MAX PLANCK INSTITUTE OF NEUROBIOLOGY   (Germany)

^c HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^d UNIVERSITÉ PARIS SACLAY   (France)

^e UNIVERSITY OF TOKYO   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AVERSION; CHOLINERGIC NERVE CELL; DROSOPHILA MELANOGASTER; EFFERENT NERVE; FEMALE; IMMUNOHISTOCHEMISTRY; MALE; MEMORY CONSOLIDATION; MUSHROOM BODY; NEUROTRANSMISSION; NONHUMAN; OLFACTORY MEMORY; PRIORITY JOURNAL; RECALL;

AFFERENT PATHWAYS; ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, GENETICALLY MODIFIED; ANTIGENS, CD8; AVOIDANCE LEARNING; BEHAVIOR, ANIMAL; CHOLINE O-ACETYLTRANSFERASE; CONDITIONING (PSYCHOLOGY); DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; GENE EXPRESSION REGULATION; GLUTAMATE DECARBOXYLASE; GREEN FLUORESCENT PROTEINS; MEMORY, SHORT-TERM; MENTAL RECALL; MODELS, BIOLOGICAL; MOTOR NEURONS; MUSHROOM BODIES; ODORS; OLFACTORY PATHWAYS; SMELL; SYNAPSINS; TEMPERATURE; TIME FACTORS; TRANSCRIPTION FACTORS; TYROSINE 3-MONOOXYGENASE; VESICULAR GLUTAMATE TRANSPORT PROTEINS;

EID: 79959673615     PISSN: 10976256     EISSN: 15461726     Source Type: Journal    
DOI: 10.1038/nn.2846     Document Type: Article

References (50)

1. Keene, A.C. & Waddell, S. Drosophila olfactory memory: single genes to complex neural circuits. Nat. Rev. Neurosci. 8, 341-354 (2007). (Pubitemid 46652464)
2. McGuire, S.E., Deshazer, M. & Davis, R.L. Thirty years of olfactory learning and memory research in Drosophila melanogaster. Prog. Neurobiol. 76, 328-347 (2005). (Pubitemid 41612176)
3. Tully, T., Preat, T., Boynton, S.C. & Del Vecchio, M. Genetic dissection of consolidated memory in Drosophila. Cell 79, 35-47 (1994). (Pubitemid 24309511)
4. Masse, N.Y., Turner, G.C. & Jefferis, G.S. Olfactory information processing in Drosophila. Curr. Biol. 19, R700-R713 (2009).
5. Aso, Y. et al. Specific dopaminergic neurons for the formation of labile aversive memory. Curr. Biol. 20, 1445-1451 (2010).
6. Claridge-Chang, A. et al. Writing memories with light-addressable reinforcement circuitry. Cell 139, 405-415 (2009).
7. Schwaerzel, M. et al. Dopamine and octopamine differentiate between aversive and appetitive olfactory memories in Drosophila. J. Neurosci. 23, 10495-10502 (2003). (Pubitemid 37485262)
8. de Belle, J.S. & Heisenberg, M. Associative odor learning in Drosophila abolished by chemical ablation of mushroom bodies. Science 263, 692-695 (1994). (Pubitemid 24076299)
9. Wang, Y. et al. Blockade of neurotransmission in Drosophila mushroom bodies impairs odor attraction, but not repulsion. Curr. Biol. 13, 1900-1904 (2003). (Pubitemid 37347934)
10. Crittenden, J.R., Skoulakis, E.M., Han, K.A., Kalderon, D. & Davis, R.L. Tripartite mushroom body architecture revealed by antigenic markers. Learn. Mem. 5, 38-51 (1998). (Pubitemid 29108269)
11. Gervasi, N., Tchenio, P. & Preat, T. PKA dynamics in Drosophila olfactory learning and memory center: coincidence detection by Rutabaga adenylyl cyclase and regulation by Dunce phosphodiesterase. Neuron 65, 516-529 (2010).
12. Tomchik, S.M. & Davis, R.L. Dynamics of learning-related cAMP signaling and stimulus integration in the Drosophila olfactory pathway. Neuron 64, 510-521 (2009).
13. Wang, Y., Mamiya, A., Chiang, A.S. & Zhong, Y. Imaging of an early memory trace in the Drosophila mushroom body. J. Neurosci. 28, 4368-4376 (2008).
14. 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 52, 845-855 (2006). (Pubitemid 44828452)
15. Isabel, G., Pascual, A. & Preat, T. Exclusive consolidated memory phases in Drosophila. Science 304, 1024-1027 (2004). (Pubitemid 38638103)
16. McGuire, S.E., Le, P.T. & Davis, R.L. The role of Drosophila mushroom body signaling in olfactory memory. Science 293, 1330-1333 (2001). (Pubitemid 32777425)
17. Ito, K. et al. The organization of extrinsic neurons and their implications in the functional roles of the mushroom bodies in Drosophila melanogaster Meigen. Learn. Mem. 5, 52-77 (1998). (Pubitemid 29108270)
18. Tanaka, N.K., Tanimoto, H. & Ito, K. Neuronal assemblies of the Drosophila mushroom body. J. Comp. Neurol. 508, 711-755 (2008). (Pubitemid 351693558)
19. Kitamoto, T. Conditional modification of behavior in Drosophila by targeted expression of a temperature-sensitive shibire allele in defined neurons. J. Neurobiol. 47, 81-92 (2001).
20. Zhang, Y.Q., Rodesch, C.K. & Broadie, K. Living synaptic vesicle marker: synaptotagmin-GFP. Genesis 34, 142-145 (2002).
21. Robinson, I.M., Ranjan, R. & Schwarz, T.L. Synaptotagmins I and IV promote transmitter release independently of Ca2+ binding in the C(2)A domain. Nature 418, 336-340 (2002). (Pubitemid 34790685)
22. Lee, T. & Luo, L. Mosaic analysis with a repressible cell marker for studies of gene function in neuronal morphogenesis. Neuron 22, 451-461 (1999). (Pubitemid 29159845)
23. 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. 28, 3103-3113 (2008). (Pubitemid 351442287)
24. Colomb, J., Kaiser, L., Chabaud, M.A. & Preat, T. Parametric and genetic analysis of Drosophila appetitive long-term memory and sugar motivation. Genes Brain Behav. 8, 407-415 (2009).
25. Kitamoto, T. Conditional disruption of synaptic transmission induces male-male courtship behavior in Drosophila. Proc. Natl. Acad. Sci. USA 99, 13232-13237 (2002).
26. Sepp, K.J. & Auld, V.J. Conversion of lacZ enhancer trap lines to GAL4 lines using targeted transposition in Drosophila melanogaster. Genetics 151, 1093-1101 (1999). (Pubitemid 29118118)
27. Pfeiffer, B.D. et al. Tools for neuroanatomy and neurogenetics in Drosophila. Proc. Natl. Acad. Sci. USA 105, 9715-9720 (2008). (Pubitemid 352031366)
28. Yasuyama, K., Meinertzhagen, I.A. & Schurmann, F.W. Synaptic organization of the mushroom body calyx in Drosophila melanogaster. J. Comp. Neurol. 445, 211-226 (2002). (Pubitemid 34194467)
29. Tian, L. et al. Imaging neural activity in worms, flies and mice with improved GCaMP calcium indicators. Nat. Methods 6, 875-881 (2009).
30. Mauelshagen, J. Neural correlates of olfactory learning paradigms in an identified neuron in the honeybee brain. J. Neurophysiol. 69, 609-625 (1993). (Pubitemid 23064320)
31. Okada, R., Rybak, J., Manz, G. & Menzel, R. Learning-related plasticity in PE1 and other mushroom body-extrinsic neurons in the honeybee brain. J. Neurosci. 27, 11736-11747 (2007). (Pubitemid 350006910)
32. Caporale, N. & Dan, Y. Spike timing-dependent plasticity: a Hebbian learning rule. Annu. Rev. Neurosci. 31, 25-46 (2008).
33. Bender, V.A., Bender, K.J., Brasier, D.J. & Feldman, D.E. Two coincidence detectors for spike timing-dependent plasticity in somatosensory cortex. J. Neurosci. 26, 4166-4177 (2006). (Pubitemid 44315376)
34. Hashimotodani, Y. et al. Phospholipase Cbeta serves as a coincidence detector through its Ca2+ dependency for triggering retrograde endocannabinoid signal. Neuron 45, 257-268 (2005). (Pubitemid 40128119)
35. Menzel, R. & Manz, G. Neural plasticity of mushroom body-extrinsic neurons in the honeybee brain. J. Exp. Biol. 208, 4317-4332 (2005). (Pubitemid 41789757)
36. Liu, X. & Davis, R.L. The GABAergic anterior paired lateral neuron suppresses and is suppressed by olfactory learning. Nat. Neurosci. 12, 53-59 (2009).
37. Bashir, Z.I. On long-term depression induced by activation of G protein-coupled receptors. Neurosci. Res. 45, 363-367 (2003). (Pubitemid 36349093)
38. Tanaka, N.K., Awasaki, T., Shimada, T. & Ito, K. Integration of chemosensory pathways in the Drosophila second-order olfactory centers. Curr. Biol. 14, 449-457 (2004). (Pubitemid 38431279)
39. Pascual, A. & Preat, T. Localization of long-term memory within the Drosophila mushroom body. Science 294, 1115-1117 (2001). (Pubitemid 33041869)
40. Tully, T. & Quinn, W.G. Classical conditioning and retention in normal and mutant Drosophila melanogaster. J. Comp. Physiol. [A] 157, 263-277 (1985).
41. Wong, A.M., Wang, J.W. & Axel, R. Spatial representation of the glomerular map in the Drosophila protocerebrum. Cell 109, 229-241 (2002). (Pubitemid 34518261)
42. Gordon, M.D. & Scott, K. Motor control in a Drosophila taste circuit. Neuron 61, 373-384 (2009).
43. Otsuna, H. & Ito, K. Systematic analysis of the visual projection neurons of Drosophila melanogaster. I. Lobula-specific pathways. J. Comp. Neurol. 497, 928-958 (2006). (Pubitemid 44051510)
44. Featherstone, D.E. et al. Presynaptic glutamic acid decarboxylase is required for induction of the postsynaptic receptor field at a glutamatergic synapse. Neuron 27, 71-84 (2000).
45. Sakai, T., Kasuya, J., Kitamoto, T. & Aigaki, T. The Drosophila TRPA channel, Painless, regulates sexual receptivity in virgin females. Genes Brain Behav. 8, 546-557 (2009).
46. Daniels, R.W., Gelfand, M.V., Collins, C.A. & DiAntonio, A. Visualizing glutamatergic cell bodies and synapses in Drosophila larval and adult CNS. J. Comp. Neurol. 508, 131-152 (2008). (Pubitemid 351532572)
47. Takagawa, K. & Salvaterra, P. Analysis of choline acetyltransferase protein in temperature sensitive mutant flies using newly generated monoclonal antibody. Neurosci. Res. 24, 237-243 (1996). (Pubitemid 26095703)
48. Neckameyer, W.S., Woodrome, S., Holt, B. & Mayer, A. Dopamine and senescence in Drosophila melanogaster. Neurobiol. Aging 21, 145-152 (2000). (Pubitemid 30224796)
49. Klagges, B.R. et al. Invertebrate synapsins: a single gene codes for several isoforms in Drosophila. J. Neurosci. 16, 3154-3165 (1996). (Pubitemid 26142351)
50. Fiala, A. & Spall, T. In vivo calcium imaging of brain activity in Drosophila by transgenic cameleon expression. Sci. STKE 2003, PL6 (2003).