Re-evaluation of learned information in Drosophila

Nature

Volumn 544, Issue 7649, 2017, Pages 240-244

  Felsenberg, Johannes ^a   Barnstedt, Oliver ^a   Cognigni, Paola ^a   Lin, Suewei ^a,b   Waddell, Scott ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b INSTITUTE OF MOLECULAR BIOLOGY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

CELLS AND CELL COMPONENTS; FLY; LEARNING; MEMORY; ODOR; OLFACTION; OPTIMIZATION; PHYSIOLOGY;

ARTICLE; DOPAMINERGIC NERVE CELL; DROSOPHILA; EVALUATION STUDY; LEARNING; MEMORY; MEMORY CONSOLIDATION; MUSHROOM BODY; NONHUMAN; PREDICTIVE VALUE; PRIORITY JOURNAL; REINFORCEMENT; REWARD; ANIMAL; ANIMAL MODEL; CARBOHYDRATE DIET; CYTOLOGY; DENDRITE; DROSOPHILA MELANOGASTER; FEMALE; LONG TERM MEMORY; MALE; ODOR; PHYSIOLOGY;

ANIMALIA; BASIDIOMYCOTA;

CARBOHYDRATE DIET; FRAGRANCE;

ANIMALS; DENDRITES; DIETARY CARBOHYDRATES; DOPAMINERGIC NEURONS; DROSOPHILA MELANOGASTER; EXTINCTION, PSYCHOLOGICAL; FEMALE; LEARNING; MALE; MEMORY CONSOLIDATION; MEMORY, LONG-TERM; MODELS, ANIMAL; MUSHROOM BODIES; ODORANTS; REINFORCEMENT (PSYCHOLOGY); REWARD; SMELL;

EID: 85027954178     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature21716     Document Type: Article

References (41)

1. Dunsmoor, J. E., Niv, Y., Daw, N. & Phelps, E. A. Rethinking extinction. Neuron 88, 47-63 (2015).
2. Nader, K. Reconsolidation and the dynamic nature of memory. Cold Spring Harb. Perspect. Biol. 7, a021782 (2015).
3. Kindt, M., Soeter, M. & Vervliet, B. Beyond extinction: erasing human fear responses and preventing the return of fear. Nat. Neurosci. 12, 256-258 (2009).
4. Schiller, D. et al. Preventing the return of fear in humans using reconsolidation update mechanisms. Nature 463, 49-53 (2010).
5. Xue, Y. X. et al. A memory retrieval-extinction procedure to prevent drug craving and relapse. Science 336, 241-245 (2012).
6. Aso, Y. et al. Mushroom body output neurons encode valence and guide memory-based action selection in Drosophila. eLife 3, e04580 (2014).
7. Owald, D. & Waddell, S. Olfactory learning skews mushroom body output pathways to steer behavioral choice in Drosophila. Curr. Opin. Neurobiol. 35, 178-184 (2015).
8. Liu, C. et al. A subset of dopamine neurons signals reward for odour memory in Drosophila. Nature 488, 512-516 (2012).
9. Burke, C. J. et al. Layered reward signalling through octopamine and dopamine in Drosophila. Nature 492, 433-437 (2012).
10. Owald, D. et al. Activity of defined mushroom body output neurons underlies learned olfactory behavior in Drosophila. Neuron 86, 417-427 (2015).
11. Claridge-Chang, A. et al. Writing memories with light-addressable reinforcement circuitry. Cell 139, 405-415 (2009).
12. Aso, Y. et al. Three dopamine pathways induce aversive odour memories with different stability. PLoS Genet. 8, e1002768 (2012).
13. Séjourné, J. et al. Mushroom body efferent neurons responsible for aversive olfactory memory retrieval in Drosophila. Nat. Neurosci. 14, 903-910 (2011).
14. Tempel, B. L., Bonini, N., Dawson, D. R. & Quinn, W. G. Reward learning in normal and mutant Drosophila. Proc. Natl Acad. Sci. USA 80, 1482-1486 (1983).
15. Schwaerzel, M., Heisenberg, M. & Zars, T. Extinction antagonizes olfactory memory at the subcellular level. Neuron 35, 951-960 (2002).
16. Lagasse, F., Devaud, J. M. & Mery, F. A switch from cycloheximide-resistant consolidated memory to cycloheximide-sensitive reconsolidation and extinction in Drosophila. J. Neurosci. 29, 2225-2230 (2009).
17. 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).
18. 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).
19. Schultz, W., Dayan, P. & Montague, P. R. A neural substrate of prediction and reward. Science 275, 1593-1599 (1997).
20. Díaz-Mataix, L., Ruiz Martinez, R. C., Schafe, G. E., LeDoux, J. E. & Doyère, V. Detection of a temporal error triggers reconsolidation of amygdala-dependent memories. Curr. Biol. 23, 467-472 (2013).
21. Pedreira, M. E., Pérez-Cuesta, L. M. & Maldonado, H. Mismatch between what is expected and what actually occurs triggers memory reconsolidation or extinction. Learn. Mem. 11, 579-585 (2004).
22. Aso, Y. et al. The neuronal architecture of the mushroom body provides a logic for associative learning. eLife 3, e04577 (2014).
23. Hige, T., Aso, Y., Modi, M. N., Rubin, G. M. & Turner, G. C. Heterosynaptic plasticity underlies aversive olfactory learning in Drosophila. Neuron 88, 985-998 (2015).
24. Perisse, E. et al. Aversive learning and appetitive motivation toggle feed-forward inhibition in the Drosophila mushroom body. Neuron 90, 1086-1099 (2016).
25. Riemensperger, T., V?ller, T., Stock, P., Buchner, E. & Fiala, A. Punishment prediction by dopaminergic neurons in Drosophila. Curr. Biol. 15, 1953-1960 (2005).
26. Sevenster, D., Beckers, T. & Kindt, M. Prediction error demarcates the transition from retrieval, to reconsolidation, to new learning. Learn. Mem. 21, 580-584 (2014).
27. Merlo, E., Milton, A. L., Goozée, Z. Y., Theobald, D. E. & Everitt, B. J. Reconsolidation and extinction are dissociable and mutually exclusive processes: behavioral and molecular evidence. J. Neurosci. 34, 2422-2431 (2014).
28. Reichelt, A. C., Exton-McGuinness, M. T. & Lee, J. L. Ventral tegmental dopamine dysregulation prevents appetitive memory destabilization. J. Neurosci. 33, 14205-14210 (2013).
29. Steinberg, E. E. et al. A causal link between prediction errors, dopamine neurons and learning. Nat. Neurosci. 16, 966-973 (2013).
30. Chang, C. Y. et al. Brief optogenetic inhibition of dopamine neurons mimics endogenous negative reward prediction errors. Nat. Neurosci. 19, 111-116 (2016).
31. Friggi-Grelin, F. et al. Targeted gene expression in Drosophila dopaminergic cells using regulatory sequences from tyrosine hydroxylase. J. Neurobiol. 54, 618-627 (2003).
32. Jenett, A. et al. A GAL4-driver line resource for Drosophila neurobiology. Cell Reports 2, 991-1001 (2012).
33. Krashes, M. J. et al. A neural circuit mechanism integrating motivational state with memory expression in Drosophila. Cell 139, 416-427 (2009).
34. Chen, T. W. et al. Ultrasensitive fluorescent proteins for imaging neuronal activity. Nature 499, 295-300 (2013).
35. Klapoetke, N. C. et al. Independent optical excitation of distinct neural populations. Nat. Methods 11, 338-346 (2014).
36. Hoopfer, E. D., Jung, Y., Inagaki, H. K., Rubin, G. M. & Anderson, D. J. P1 interneurons promote a persistent internal state that enhances inter-male aggression in Drosophila. eLife 4, e11346 (2015).
37. Folkers, E., Drain, P. & Quinn, W. G. Radish, a Drosophila mutant deficient in consolidated memory. Proc. Natl Acad. Sci. USA 90, 8123-8127 (1993).
38. Pologruto, T. A., Sabatini, B. L. & Svoboda, K. ScanImage: flexible software for operating laser scanning microscopes. Biomed. Eng. Online 2, 13 (2003).
39. Shang, Y., Claridge-Chang, A., Sjulson, L., Pypaert, M. & Miesenb?ck, G. Excitatory local circuits and their implications for olfactory processing in the fly antennal lobe. Cell 128, 601-612 (2007).
40. Wu, J. S. & Luo, L. A protocol for dissecting Drosophila melanogaster brains for live imaging or immunostaining. Nat. Protocols 1, 2110-2115 (2006).
41. Hirano, Y. et al. Shifting transcriptional machinery is required for long-term memory maintenance and modification in Drosophila mushroom bodies. Nat. Commun. 7, 13471 (2016).