Two pairs of mushroom body efferent neurons are required for appetitive long-term memory retrieval in drosophila

Cell Reports

Volumn 5, Issue 3, 2013, Pages 769-780

  Plaçais, Pierre Yves ^a   Trannoy, Séverine ^a,d   Friedrich, Anja B ^b   Tanimoto, Hiromu ^b,c   Preat, Thomas ^a  

^a PSL RESEARCH UNIVERSITY   (France)

^b MAX PLANCK INSTITUTE OF NEUROBIOLOGY   (Germany)

^c TOHOKU UNIVERSITY   (Japan)

^d HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; CHOLINERGIC NERVE CELL; CONTROLLED STUDY; DROSOPHILA; EFFERENT NERVE; EVOKED AUDITORY RESPONSE; LONG TERM MEMORY; MB V3 NEURON; MEMORY DISORDER; MENTAL PERFORMANCE; MUSHROOM BODY; NEUROBIOLOGY; NEUROMODULATION; NONHUMAN; OLFACTORY DISCRIMINATION; PRIORITY JOURNAL; RECALL; SHORT TERM MEMORY; TASK PERFORMANCE; ANIMAL; APPETITE; FEMALE; PHYSIOLOGY; TRANSGENIC ANIMAL;

BASIDIOMYCOTA;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; APPETITIVE BEHAVIOR; DROSOPHILA; FEMALE; MEMORY, LONG-TERM; MUSHROOM BODIES; NEURONS, EFFERENT;

EID: 84887615404     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2013.09.032     Document Type: Article

References (51)

1. Aso Y., Grübel K., Busch S., Friedrich A.B., Siwanowicz I., Tanimoto H. The mushroom body of adult Drosophila characterized by GAL4 drivers. J.Neurogenet. 2009, 23:156-172.
2. Aso Y., Siwanowicz I., Bräcker L., Ito K., Kitamoto T., Tanimoto H. Specific dopaminergic neurons for the formation of labile aversive memory. Curr. Biol. 2010, 20:1445-1451.
3. Aso Y., Herb A., Ogueta M., Siwanowicz I., Templier T., Friedrich A.B., Ito K., Scholz H., Tanimoto H. Three dopamine pathways induce aversive odor memories with different stability. PLoS Genet. 2012, 8:e1002768.
4. Bailey C.H., Bartsch D., Kandel E.R. Toward a molecular definition of long-term memory storage. Proc. Natl. Acad. Sci. USA 1996, 93:13445-13452.
5. Benito E., Barco A. CREB's control of intrinsic and synaptic plasticity: implications for CREB-dependent memory models. Trends Neurosci. 2010, 33:230-240.
6. Burke C.J., Huetteroth W., Owald D., Perisse E., Krashes M.J., Das G., Gohl D., Silies M., Certel S., Waddell S. Layered reward signalling through octopamine and dopamine in Drosophila. Nature 2012, 492:433-437.
7. Busch S., Selcho M., Ito K., Tanimoto H. A map of octopaminergic neurons in the Drosophila brain. J.Comp. Neurol. 2009, 513:643-667.
8. Cervantes-Sandoval I., Martin-Peña A., Berry J.A., Davis R.L. System-like consolidation of olfactory memories in Drosophila. J.Neurosci. 2013, 33:9846-9854.
9. Chiang A.S., Lin C.Y., Chuang C.C., Chang H.M., Hsieh C.H., Yeh C.W., Shih C.T., Wu J.J., Wang G.T., Chen Y.C., et al. Three-dimensional reconstruction of brain-wide wiring networks in Drosophila at single-cell resolution. Curr. Biol. 2011, 21:1-11.
10. Claridge-Chang A., Roorda R.D., Vrontou E., Sjulson L., Li H., Hirsh J., Miesenböck G. Writing memories with light-addressable reinforcement circuitry. Cell 2009, 139:405-415.
11. 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. 2009, 8:407-415.
12. 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.
13. de Belle J.S., Heisenberg M. Associative odor learning in Drosophila abolished by chemical ablation of mushroom bodies. Science 1994, 263:692-695.
14. Dubnau J., Tully T. Gene discovery in Drosophila: new insights forlearning and memory. Annu. Rev. Neurosci. 1998, 21:407-444.
15. Hamada F.N., Rosenzweig M., Kang K., Pulver S.R., Ghezzi A., Jegla T.J., Garrity P.A. An internal thermal sensor controlling temperature preference in Drosophila. Nature 2008, 454:217-220.
16. Heisenberg M. Mushroom body memoir: from maps to models. Nat. Rev. Neurosci. 2003, 4:266-275.
17. Hirano Y., Masuda T., Naganos S., Matsuno M., Ueno K., Miyashita T., Horiuchi J., Saitoe M. Fasting launches CRTC to facilitate long-term memory formation in Drosophila. Science 2013, 339:443-446.
18. Honegger K.S., Campbell R.A., Turner G.C. Cellular-resolution population imaging reveals robust sparse coding in the Drosophila mushroom body. J.Neurosci. 2011, 31:11772-11785.
19. Isabel G., Pascual A., Preat T. Exclusive consolidated memory phases in Drosophila. Science 2004, 304:1024-1027.
20. 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.
21. Kitamoto T. Conditional modification of behavior in Drosophila by targeted expression of a temperature-sensitive shibire allele in defined neurons. J.Neurobiol. 2001, 47:81-92.
22. 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.
23. 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.
24. Krashes M.J., DasGupta S., Vreede A., White B., Armstrong J.D., Waddell S. A neural circuit mechanism integrating motivational state with memory expression in Drosophila. Cell 2009, 139:416-427.
25. Laurent G. Olfactory network dynamics and the coding of multidimensional signals. Nat. Rev. Neurosci. 2002, 3:884-895.
26. Lee T., Luo L. Mosaic analysis with a repressible cell marker for studies of gene function in neuronal morphogenesis. Neuron 1999, 22:451-461.
27. Liu C., Plaçais P.Y., Yamagata N., Pfeiffer B.D., Aso Y., Friedrich A.B., Siwanowicz I., Rubin G.M., Preat T., Tanimoto H. A subset of dopamine neurons signals reward for odour memory in Drosophila. Nature 2012, 488:512-516.
28. Martin S.J., Grimwood P.D., Morris R.G. Synaptic plasticity and memory: an evaluation of the hypothesis. Annu. Rev. Neurosci. 2000, 23:649-711.
29. Masse N.Y., Turner G.C., Jefferis G.S. Olfactory information processing in Drosophila. Curr. Biol. 2009, 19:R700-R713.
30. Mayford M., Kandel E.R. Genetic approaches to memory storage. Trends Genet. 1999, 15:463-470.
31. Neves G., Cooke S.F., Bliss T.V.P. Synaptic plasticity, memory and the hippocampus: a neural network approach to causality. Nat. Rev. Neurosci. 2008, 9:65-75.
32. Nicolaï L.J.J., Ramaekers A., Raemaekers T., Drozdzecki A., Mauss A.S., Yan J., Landgraf M., Annaert W., Hassan B.A. Genetically encoded dendritic marker sheds light on neuronal connectivity in Drosophila. Proc. Natl. Acad. Sci. USA 2010, 107:20553-20558.
33. Pai T.P., Chen C.C., Lin H.H., Chin A.L., Lai J.S., Lee P.T., Tully T., Chiang A.S. Drosophila ORB protein in two mushroom body output neurons is necessary for long-term memory formation. Proc. Natl. Acad. Sci. USA 2013, 110:7898-7903.
34. Pfeiffer B.D., Truman J.W., Rubin G.M. Using translational enhancers to increase transgene expression in Drosophila. Proc. Natl. Acad. Sci. USA 2012, 109:6626-6631.
35. Pittenger C., Kandel E.R. In search of general mechanisms for long-lasting plasticity: Aplysia and the hippocampus. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2003, 358:757-763.
36. Plaçais P.Y., Preat T. To favor survival under food shortage, the brain disables costly memory. Science 2013, 339:440-442.
37. Plaçais P.Y., Trannoy S., Isabel G., Aso Y., Siwanowicz I., Belliart-Guérin G., Vernier P., Birman S., Tanimoto H., Preat T. Slow oscillations in two pairs of dopaminergic neurons gate long-term memory formation in Drosophila. Nat. Neurosci. 2012, 15:592-599.
38. Robinson I.M., Ranjan R., Schwarz T.L. Synaptotagmins I and IV promote transmitter release independently of Ca(2+) binding in the C(2)A domain. Nature 2002, 418:336-340.
39. Schwaerzel M., Monastirioti M., Scholz H., Friggi-Grelin F., Birman S., Heisenberg M. Dopamine and octopamine differentiate between aversive and appetitive olfactory memories in Drosophila. J.Neurosci. 2003, 23:10495-10502.
40. Séjourné J., Plaçais P.Y., Aso Y., Siwanowicz I., Trannoy S., Thoma V., Tedjakumala S.R., Rubin G.M., Tchénio P., Ito K., et al. Mushroom body efferent neurons responsible for aversive olfactory memory retrieval in Drosophila. Nat. Neurosci. 2011, 14:903-910.
41. Tanaka N.K., Tanimoto H., Ito K. Neuronal assemblies of the Drosophila mushroom body. J.Comp. Neurol. 2008, 508:711-755.
42. Tempel B.L., Bonini N., Dawson D.R., Quinn W.G. Reward learning in normal and mutant Drosophila. Proc. Natl. Acad. Sci. USA 1983, 80:1482-1486.
43. Tian L., Hires S.A., Mao T., Huber D., Chiappe M.E., Chalasani S.H., Petreanu L., Akerboom J., McKinney S.A., Schreiter E.R., et al. Imaging neural activity in worms, flies and mice with improved GCaMP calcium indicators. Nat. Methods 2009, 6:875-881.
44. Trannoy S., Redt-Clouet C., Dura J.M., Preat T. Parallel processing of appetitive short- and long-term memories in Drosophila. Curr. Biol. 2011, 21:1647-1653.
45. Tully T., Quinn W.G. Classical conditioning and retention in normal and mutant Drosophila melanogaster. J.Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 1985, 157:263-277.
46. Tully T., Preat T., Boynton S.C., Del Vecchio M. Genetic dissection of consolidated memory in Drosophila. Cell 1994, 79:35-47.
47. Turner G.C., Bazhenov M., Laurent G. Olfactory representations by Drosophila mushroom body neurons. J.Neurophysiol. 2008, 99:734-746.
48. Wang Y., Guo H.F., Pologruto T.A., Hannan F., Hakker I., Svoboda K., Zhong Y. Stereotyped odor-evoked activity in the mushroom body of Drosophila revealed by green fluorescent protein-based Ca2+ imaging. J.Neurosci. 2004, 24:6507-6514.
49. Wang Y., Mamiya A., Chiang A.S., Zhong Y. Imaging of an early memory trace in the Drosophila mushroom body. J.Neurosci. 2008, 28:4368-4376.
50. Yasuyama K., Meinertzhagen I.A., Schürmann F.W. Synaptic organization of the mushroom body calyx in Drosophila melanogaster. J.Comp. Neurol. 2002, 445:211-226.
51. 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.