Distinct dopamine neurons mediate reward signals for short- and long-term memories

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 2, 2015, Pages 578-583

  Yamagata, Nobuhiro ^a,b   Ichinose, Toshiharu ^a,b   Aso, Yoshinori ^c   Plaçais, Pierre Yves ^d   Friedrich, Anja B ^b   Sima, Richard J ^e   Preat, Thomas ^d   Rubin, Gerald M ^c   Tanimoto, Hiromu ^a,b  

^a TOHOKU UNIVERSITY   (Japan)

^b MAX PLANCK INSTITUTE OF NEUROBIOLOGY   (Germany)

^c HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^d PSL RESEARCH UNIVERSITY   (France)

^e JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Dopamine; Drosophila; Learning and memory; Mushroom body

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BINOCULAR CONVERGENCE; BRAIN; CONTROLLED STUDY; DIPTERA; DOPAMINERGIC NERVE CELL; DROSOPHILA MELANOGASTER; LONG TERM MEMORY; MEMORY CONSOLIDATION; MUSHROOM BODY; NONHUMAN; NUTRITIONAL VALUE; PRIORITY JOURNAL; REWARD; SHORT TERM MEMORY; SWEETNESS; TRAINING; ANATOMY AND HISTOLOGY; ANIMAL; APPETITE; FEMALE; GENETICS; LEARNING; ODOR; PHYSIOLOGY; TASTE; TRANSGENIC ANIMAL;

BASIDIOMYCOTA; DROSOPHILA MELANOGASTER;

CARBOHYDRATE;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; APPETITIVE BEHAVIOR; CARBOHYDRATES; DOPAMINERGIC NEURONS; DROSOPHILA MELANOGASTER; FEMALE; LEARNING; MEMORY, LONG-TERM; MEMORY, SHORT-TERM; MUSHROOM BODIES; ODORS; REWARD; SMELL; TASTE;

EID: 84920973061     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1421930112     Document Type: Article

References (61)

1. Carew TJ, Kandel ER (1973) Acquisition and retention of long-term habituation in Aplysia: Correlation of behavioral and cellular processes. Science 182(4117): 1158-1160.
2. Carew TJ, Pinsker HM, Kandel ER (1972) Long-term habituation of a defensive withdrawal reflex in aplysia. Science 175(4020):451-454.
3. Tully T, Preat T, Boynton SC, Del Vecchio M (1994) Genetic dissection of consolidated memory in Drosophila. Cell 79(1):35-47.
4. Garcia J, Kimeldorf DJ, Koelling RA (1955) Conditioned aversion to saccharin resulting from exposure to gamma radiation. Science 122(3160):157-158.
5. Alexander J Jr, Audesirk TE, Audesirk GJ (1984) One-trial reward learning in the snail Lymnea stagnalis. J Neurobiol 15(1):67-72.
6. Krashes MJ, Waddell S (2008) Rapid consolidation to a radish and protein synthesisdependent long-term memory after single-session appetitive olfactory conditioning in Drosophila. J Neurosci 28(12):3103-3113.
7. Colomb J, Kaiser L, Chabaud MA, Preat T (2009) Parametric and genetic analysis of Drosophila appetitive long-term memory and sugar motivation. Genes Brain Behav 8(4):407-415.
8. Pagani MR, Oishi K, Gelb BD, Zhong Y (2009) The phosphatase SHP2 regulates the spacing effect for long-term memory induction. Cell 139(1):186-198.
9. Plaçais PY, et al. (2012) Slow oscillations in two pairs of dopaminergic neurons gate long-term memory formation in Drosophila. Nat Neurosci 15(4):592-599.
10. Zhang Y, et al. (2012) Computational design of enhanced learning protocols. Nat Neurosci 15(2):294-297.
11. Huang C, et al. (2012) A permissive role of mushroom body α/β core neurons in longterm memory consolidation in Drosophila. Curr Biol 22(21):1981-1989.
12. Hirano Y, et al. (2013) Fasting launches CRTC to facilitate long-term memory formation in Drosophila. Science 339(6118):443-446.
13. Turner GC, Bazhenov M, Laurent G (2008) Olfactory representations by Drosophila mushroom body neurons. J Neurophysiol 99(2):734-746.
14. Heisenberg M (2003) Mushroom body memoir: From maps to models. Nat Rev Neurosci 4(4):266-275.
15. Gerber B, Tanimoto H, Heisenberg M (2004) An engram found? Evaluating the evidence from fruit flies. Curr Opin Neurobiol 14(6):737-744.
16. Tomchik SM, Davis RL (2009) Dynamics of learning-related cAMP signaling and stimulus integration in the Drosophila olfactory pathway. Neuron 64(4):510-521.
17. Gervasi N, Tchénio P, Preat T (2010) PKA dynamics in a Drosophila learning center: Coincidence detection by rutabaga adenylyl cyclase and spatial regulation by dunce phosphodiesterase. Neuron 65(4):516-529.
18. Burke CJ, et al. (2012) Layered reward signalling through octopamine and dopamine in Drosophila. Nature 492(7429):433-437.
19. Liu C, et al. (2012) A subset of dopamine neurons signals reward for odour memory in Drosophila. Nature 488(7412):512-516.
20. Pauls D, Selcho M, Gendre N, Stocker RF, Thum AS (2010) Drosophila larvae establish appetitive olfactory memories via mushroom body neurons of embryonic origin. J Neurosci 30(32):10655-10666.
21. Krashes MJ, Keene AC, Leung B, Armstrong JD, Waddell S (2007) Sequential use of mushroom body neuron subsets during drosophila odor memory processing. Neuron 53(1):103-115.
22. Trannoy S, Redt-Clouet C, Dura JM, Preat T (2011) Parallel processing of appetitive short- and long-term memories in Drosophila. Curr Biol 21(19):1647-1653.
23. Cervantes-Sandoval I, Martin-Peña A, Berry JA, Davis RL (2013) System-like consolidation of olfactory memories in Drosophila. J Neurosci 33(23):9846-9854.
24. Xie Z, Huang C, Ci B, Wang L, Zhong Y (2013) Requirement of the combination of mushroom body γ lobe and α/β lobes for the retrieval of both aversive and appetitive early memories in Drosophila. Learn Mem 20(9):474-481.
25. Huang C, Wang P, Xie Z, Wang L, Zhong Y (2013) The differential requirement of mushroom body α/β subdivisions in long-term memory retrieval in Drosophila. Protein Cell 4(7):512-519.
26. Roeper J (2013) Dissecting the diversity of midbrain dopamine neurons. Trends Neurosci 36(6):336-342.
27. Lammel S, Lim BK, Malenka RC (2014) Reward and aversion in a heterogeneous midbrain dopamine system. Neuropharmacology 76(Pt B):351-359.
28. Tanaka NK, Tanimoto H, Ito K (2008) Neuronal assemblies of the Drosophila mushroom body. J Comp Neurol 508(5):711-755.
29. Aso Y, et al. (2010) Specific dopaminergic neurons for the formation of labile aversive memory. Curr Biol 20(16):1445-1451.
30. Aso Y, et al. (2012) Three dopamine pathways induce aversive odor memories with different stability. PLoS Genet 8(7):e1002768.
31. Keleman K, et al. (2012) Dopamine neurons modulate pheromone responses in Drosophila courtship learning. Nature 489(7414):145-149.
32. Riemensperger T, et al. (2013) A single dopamine pathway underlies progressive locomotor deficits in a Drosophila model of Parkinson disease. Cell Reports 5(4): 952-960.
33. Aso Y, et al. (2014) The neuronal architecture of the mushroom body provides a logic for associative learning. eLife, 10.7554/eLife.04577.001.
34. Aso Y, et al. (2014) Mushroom body output neurons encode valence and guide memory-based action selection in Drosophila. eLife, 10.7554/eLife.04580.001.
35. Hamada FN, et al. (2008) An internal thermal sensor controlling temperature preference in Drosophila. Nature 454(7201):217-220.
36. Das G, et al. (2014) Drosophila learn opposing components of a compound food stimulus. Curr Biol 24(15):1723-1730.
37. Kitamoto T (2001) Conditional modification of behavior in Drosophila by targeted expression of a temperature-sensitive shibire allele in defined neurons. J Neurobiol 47(2):81-92.
38. Burke CJ, Waddell S (2011) Remembering nutrient quality of sugar in Drosophila. Curr Biol 21(9):746-750.
39. Cervantes-Sandoval I, Davis RL (2012) Distinct traces for appetitive versus aversive olfactory memories in DPM neurons of Drosophila. Curr Biol 22(13):1247-1252.
40. Jenett A, et al. (2012) A GAL4-driver line resource for Drosophila neurobiology. Cell Reports 2(4):991-1001.
41. Lin S, et al. (2014) Neural correlates of water reward in thirsty Drosophila. Nat Neurosci 17(11):1536-1542.
42. Miyamoto T, Slone J, Song X, Amrein H (2012) A fructose receptor functions as a nutrient sensor in the Drosophila brain. Cell 151(5):1113-1125.
43. Boto T, Louis T, Jindachomthong K, Jalink K, Tomchik SM (2014) Dopaminergic modulation of cAMP drives nonlinear plasticity across the Drosophila mushroom body lobes. Curr Biol 24(8):822-831.
44. Murthy M, Fiete I, Laurent G (2008) Testing odor response stereotypy in the Drosophila mushroom body. Neuron 59(6):1009-1023.
45. Caron SJ, Ruta V, Abbott LF, Axel R (2013) Random convergence of olfactory inputs in the Drosophila mushroom body. Nature 497(7447):113-117.
46. Emptage NJ, Carew TJ (1993) Long-term synaptic facilitation in the absence of shortterm facilitation in Aplysia neurons. Science 262(5131):253-256.
47. Martin KC, et al. (1997) Synapse-specific, long-term facilitation of aplysia sensory to motor synapses: A function for local protein synthesis in memory storage. Cell 91(7): 927-938.
48. Wright WG, Jones K, Sharp P, Maynard B (1995) Widespread anatomical projections of the serotonergic modulatory neuron, CB1, in Aplysia. Invert Neurosci 1(2):173-183.
49. Galili DS, et al. (2014) Converging circuits mediate temperature and shock aversive olfactory conditioning in Drosophila. Curr Biol 24(15):1712-1722.
50. Fiorillo CD, Yun SR, Song MR (2013) Diversity and homogeneity in responses of midbrain dopamine neurons. J Neurosci 33(11):4693-4709.
51. Kaun KR, Azanchi R, Maung Z, Hirsh J, Heberlein U (2011) A Drosophila model for alcohol reward. Nat Neurosci 14(5):612-619.
52. Unoki S, Matsumoto Y, Mizunami M (2005) Participation of octopaminergic reward system and dopaminergic punishment system in insect olfactory learning revealed by pharmacological study. Eur J Neurosci 22(6):1409-1416.
53. Dubnau J, et al. (2003) The staufen/pumilio pathway is involved in Drosophila longterm memory. Curr Biol 13(4):286-296.
54. Comas D, Petit F, Preat T (2004) Drosophila long-term memory formation involves regulation of cathepsin activity. Nature 430(6998):460-463.
55. Margulies C, Tully T, Dubnau J (2005) Deconstructing memory in Drosophila. Curr Biol 15(17):R700-R713.
56. Hawkins RD, Kandel ER, Bailey CH (2006) Molecular mechanisms of memory storage in Aplysia. Biol Bull 210(3):174-191.
57. Keene AC, Waddell S (2007) Drosophila olfactory memory: Single genes to complex neural circuits. Nat Rev Neurosci 8(5):341-354.
58. Stafford JW, Lynd KM, Jung AY, Gordon MD (2012) Integration of taste and calorie sensing in Drosophila. J Neurosci 32(42):14767-14774.
59. Peng H, et al. (2011) BrainAligner: 3D registration atlases of Drosophila brains. Nat Methods 8(6):493-500.
60. Tian L, et al. (2009) Imaging neural activity in worms, flies and mice with improved GCaMP calcium indicators. Nat Methods 6(12):875-881.
61. Séjourné J, et al. (2011) Mushroom body efferent neurons responsible for aversive olfactory memory retrieval in Drosophila. Nat Neurosci 14(7):903-910.