Reciprocal synapses between mushroom body and dopamine neurons form a positive feedback loop required for learning

eLife

Volumn 6, Issue , 2017, Pages

  Cervantes Sandoval, Isaac ^a   Phan, Anna ^a   Chakraborty, Molee ^a   Davis, Ronald L ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHOLINERGIC RECEPTOR; INWARDLY RECTIFYING POTASSIUM CHANNEL SUBUNIT KIR2.1; PURINERGIC P2X2 RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BEHAVIOR; CALCIUM TRANSPORT; CHOLINERGIC ACTIVITY; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; DROSOPHILA; FUNCTIONAL CONNECTIVITY; GENE EXPRESSION; GENE SILENCING; GENOTYPE; IMMUNOHISTOCHEMISTRY; KENYON CELL; LOCOMOTION; MUSHROOM BODY; NONHUMAN; OLFACTORY CORTEX; OPTOGENETICS; POSITIVE FEEDBACK; POSTSYNAPTIC POTENTIAL SUMMATION; PROTEIN EXPRESSION; STATE DEPENDENT LEARNING; STIMULUS; SYNAPSE; ANIMAL; CONDITIONED REFLEX; FEEDBACK SYSTEM; LEARNING; NERVE CELL NETWORK; PHYSIOLOGY;

ANIMALS; CONDITIONING, CLASSICAL; DOPAMINERGIC NEURONS; DROSOPHILA; FEEDBACK; LEARNING; MUSHROOM BODIES; NERVE NET; SYNAPSES;

EID: 85019489202     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.23789     Document Type: Article

References (60)

1. Aso Y, Hattori D, Yu Y, Johnston RM, Iyer NA, Ngo TT, Dionne H, Abbott LF, Axel R, Tanimoto H, Rubin GM. 2014a. The neuronal architecture of the mushroom body provides a logic for associative learning. eLife 3: e04577. doi: 10.7554/eLife.04577, PMID: 25535793
2. Aso Y, Herb A, Ogueta M, Siwanowicz I, Templier T, Friedrich AB, Ito K, Scholz H, Tanimoto H. 2012. Three dopamine pathways induce aversive odor memories with different stability. PLoS Genetics 8:e1002768. doi: 10. 1371/journal.pgen.1002768, PMID: 22807684
3. Aso Y, Sitaraman D, Ichinose T, Kaun KR, Vogt K, Belliart-Guérin G, Plaçais PY, Robie AA, Yamagata N, Schnaitmann C, Rowell WJ, Johnston RM, Ngo TT, Chen N, Korff W, Nitabach MN, Heberlein U, Preat T, Branson KM, Tanimoto H, et al. 2014b. Mushroom body output neurons encode Valence and guide memory-based action selection in Drosophila. eLife 3:e04580. doi: 10.7554/eLife.04580, PMID: 25535794
4. Aso Y, Siwanowicz I, Bräcker L, Ito K, Kitamoto T, Tanimoto H. 2010. Specific dopaminergic neurons for the formation of labile aversive memory. Current Biology 20:1445–1451. doi: 10.1016/j.cub.2010.06.048, PMID: 20637624
5. Baines RA, Uhler JP, Thompson A, Sweeney ST, Bate M. 2001. Altered electrical properties in Drosophila neurons developing without synaptic transmission. Journal of Neuroscience 21:1523–1531. PMID: 11222642
6. Bargmann CI, Marder E. 2013. From the connectome to brain function. Nature Methods 10:483–490. doi: 10. 1038/nmeth.2451, PMID: 23866325
7. Barnstedt O, Owald D, Felsenberg J, Brain R, Moszynski JP, Talbot CB, Perrat PN, Waddell S. 2016. Memory-Relevant mushroom body output synapses are cholinergic. Neuron 89:1237–1247. doi: 10.1016/j.neuron.2016.02.015, PMID: 26948892
8. Beck CD, Schroeder B, Davis RL. 2000. Learning performance of normal and mutant Drosophila after repeated conditioning trials with discrete stimuli. Journal of Neuroscience 20:2944–2953. PMID: 10751447
9. Berry JA, Cervantes-Sandoval I, Chakraborty M, Davis RL. 2015. Sleep facilitates memory by blocking dopamine neuron-mediated forgetting. Cell 161:1656–1667. doi: 10.1016/j.cell.2015.05.027, PMID: 26073942
10. Berry JA, Cervantes-Sandoval I, Nicholas EP, Davis RL. 2012. Dopamine is required for learning and forgetting in Drosophila. Neuron 74:530–542. doi: 10.1016/j.neuron.2012.04.007, PMID: 22578504
11. Bouzaiane E, Trannoy S, Scheunemann L, Plaçais PY, Preat T. 2015. Two independent mushroom body output circuits retrieve the six discrete components of Drosophila aversive memory. Cell Reports 11:1280–1292. doi: 10.1016/j.celrep.2015.04.044, PMID: 25981036
12. Burke CJ, Huetteroth W, Owald D, Perisse E, Krashes MJ, Das G, Gohl D, Silies M, Certel S, Waddell S. 2012. Layered reward signalling through octopamine and dopamine in Drosophila. Nature 492:433–437. doi: 10. 1038/nature11614, PMID: 23103875
13. Busto GU, Cervantes-Sandoval I, Davis RL. 2010. Olfactory learning in Drosophila. Physiology 25:338–346. doi: 10.1152/physiol.00026.2010, PMID: 21186278
14. Cervantes-Sandoval I, Chakraborty M, MacMullen C, Davis RL. 2016. Scribble scaffolds a signalosome for active forgetting. Neuron 90:1230–1242. doi: 10.1016/j.neuron.2016.05.010, PMID: 27263975
15. Cervantes-Sandoval I, Martin-Peña A, Berry JA, Davis RL. 2013. System-like consolidation of olfactory memories in Drosophila. Journal of Neuroscience 33:9846–9854. doi: 10.1523/JNEUROSCI.0451-13.2013, PMID: 2373 9981
16. Chen TW, Wardill TJ, Sun Y, Pulver SR, Renninger SL, Baohan A, Schreiter ER, Kerr RA, Orger MB, Jayaraman V, Looger LL, Svoboda K, Kim DS. 2013. Ultrasensitive fluorescent proteins for imaging neuronal activity. Nature 499:295–300. doi: 10.1038/nature12354, PMID: 23868258
17. Claridge-Chang A, Roorda RD, Vrontou E, Sjulson L, Li H, Hirsh J, Miesenböck G. 2009. Writing memories with light-addressable reinforcement circuitry. Cell 139:405–415. doi: 10.1016/j.cell.2009.08.034, PMID: 19837039
18. Cohn R, Morantte I, Ruta V. 2015. Coordinated and compartmentalized neuromodulation shapes sensory processing in Drosophila. Cell 163:1742–1755. doi: 10.1016/j.cell.2015.11.019, PMID: 26687359
19. Davis RL. 1993. Mushroom bodies and Drosophila learning. Neuron 11:1–14. doi: 10.1016/0896-6273(93)90266-T, PMID: 8338661
20. Davis RL. 2005. Olfactory memory formation in Drosophila: from molecular to systems neuroscience. Annual Review of Neuroscience 28:275–302. doi: 10.1146/annurev.neuro.28.061604.135651, PMID: 16022597
21. Davis RL. 2011. Traces of Drosophila memory. Neuron 70:8–19. doi: 10.1016/j.neuron.2011.03.012, PMID: 214 82352
22. Friggi-Grelin F, Coulom H, Meller M, Gomez D, Hirsh J, Birman S. 2003. Targeted gene expression in Drosophila dopaminergic cells using regulatory sequences from tyrosine hydroxylase. Journal of Neurobiology 54:618– 627. doi: 10.1002/neu.10185, PMID: 12555273
23. Heisenberg M. 2003. Mushroom body memoir: from maps to models. Nature Reviews Neuroscience 4:266–275. doi: 10.1038/nrn1074, PMID: 12671643
24. Hige T, Aso Y, Modi MN, Rubin GM, Turner GC. 2015. Heterosynaptic plasticity underlies aversive olfactory Learning in Drosophila. Neuron 88:985–998. doi: 10.1016/j.neuron.2015.11.003, PMID: 26637800
25. Honegger KS, Campbell RA, Turner GC. 2011. Cellular-resolution population imaging reveals robust sparse coding in the Drosophila mushroom body. Journal of Neuroscience 31:11772–11785. doi: 10.1523/JNEUROSCI.1099-11.2011, PMID: 21849538
26. Hoopfer ED, Jung Y, Inagaki HK, Rubin GM, Anderson DJ. 2015. P1 interneurons promote a persistent internal state that enhances inter-male aggression in Drosophila. eLife 4:e11346. doi: 10.7554/eLife.11346, PMID: 26714106
27. Jenett A, Rubin GM, Ngo TT, Shepherd D, Murphy C, Dionne H, Pfeiffer BD, Cavallaro A, Hall D, Jeter J, Iyer N, Fetter D, Hausenfluck JH, Peng H, Trautman ET, Svirskas RR, Myers EW, Iwinski ZR, Aso Y, DePasquale GM, et al. 2012. A GAL4-driver line resource for Drosophila neurobiology. Cell Reports 2:991–1001. doi: 10.1016/j. celrep.2012.09.011, PMID: 23063364
28. Kim YC, Lee HG, Han KA. 2007. D1 dopamine receptor dDA1 is required in the mushroom body neurons for aversive and appetitive learning in Drosophila. Journal of Neuroscience 27:7640–7647. doi: 10.1523/JNEUROSCI.1167-07.2007, PMID: 17634358
29. Lewis LP, Siju KP, Aso Y, Friedrich AB, Bulteel AJ, Rubin GM, Grunwald Kadow IC. 2015. A higher brain circuit for Immediate integration of conflicting sensory information in Drosophila. Current Biology 25:2203–2214. doi: 10.1016/j.cub.2015.07.015, PMID: 26299514
30. Lima SQ, Miesenböck G. 2005. Remote control of behavior through genetically targeted photostimulation of neurons. Cell 121:141–152. doi: 10.1016/j.cell.2005.02.004, PMID: 15820685
31. Lin AC, Bygrave AM, de Calignon A, Lee T, Miesenböck G. 2014a. Sparse, decorrelated odor coding in the mushroom body enhances learned odor discrimination. Nature Neuroscience 17:559–568. doi: 10.1038/nn.3660, PMID: 24561998
32. Lin S, Owald D, Chandra V, Talbot C, Huetteroth W, Waddell S. 2014b. Neural correlates of water reward in thirsty Drosophila. Nature Neuroscience 17:1536–1542. doi: 10.1038/nn.3827, PMID: 25262493
33. Liu C, Plaçais PY, Yamagata N, Pfeiffer BD, Aso Y, Friedrich AB, Siwanowicz I, Rubin GM, Preat T, Tanimoto H. 2012. A subset of dopamine neurons signals reward for odour memory in Drosophila. Nature 488:512–516. doi: 10.1038/nature11304, PMID: 22810589
34. Liu X, Davis RL. 2009. The GABAergic anterior paired lateral neuron suppresses and is suppressed by olfactory learning. Nature Neuroscience 12:53–59. doi: 10.1038/nn.2235, PMID: 19043409
35. Macpherson LJ, Zaharieva EE, Kearney PJ, Alpert MH, Lin TY, Turan Z, Lee CH, Gallio M. 2015. Dynamic labelling of neural connections in multiple colours by trans-synaptic fluorescence complementation. Nature Communications 6:10024. doi: 10.1038/ncomms10024, PMID: 26635273
36. Mao Z, Davis RL. 2009. Eight different types of dopaminergic neurons innervate the Drosophila mushroom body neuropil: anatomical and physiological heterogeneity. Frontiers in Neural Circuits 3:5. doi: 10.3389/neuro.04. 005.2009, PMID: 19597562
37. McGuire SE, Le PT, Osborn AJ, Matsumoto K, Davis RL. 2003. Spatiotemporal rescue of memory dysfunction in Drosophila. Science 302:1765–1768. doi: 10.1126/science.1089035, PMID: 14657498
38. Musso PY, Tchenio P, Preat T. 2015. Delayed dopamine signaling of energy level builds appetitive long-term memory in Drosophila. Cell Reports 10:1023–1031. doi: 10.1016/j.celrep.2015.01.036, PMID: 25704807
39. Owald D, Felsenberg J, Talbot CB, Das G, Perisse E, Huetteroth W, Waddell S. 2015. Activity of defined mushroom body output neurons underlies learned olfactory behavior in Drosophila. Neuron 86:417–427. doi: 10.1016/j.neuron.2015.03.025, PMID: 25864636
40. Pai TP, Chen CC, Lin HH, Chin AL, Lai JS, Lee PT, Tully T, Chiang AS. 2013. Drosophila ORB protein in two mushroom body output neurons is necessary for long-term memory formation. PNAS 110:7898–7903. doi: 10.1073/pnas.1216336110, PMID: 23610406
41. Pech U, Pooryasin A, Birman S, Fiala A. 2013. Localization of the contacts between Kenyon cells and aminergic neurons in the Drosophila melanogaster brain using SplitGFP reconstitution. The Journal of Comparative Neurology 521:3992–4026. doi: 10.1002/cne.23388, PMID: 23784863
42. Perisse E, Owald D, Barnstedt O, Talbot CB, Huetteroth W, Waddell S. 2016. Aversive Learning and appetitive motivation toggle feed-forward inhibition in the Drosophila Mushroom body. Neuron 90:1086–1099. doi: 10. 1016/j.neuron.2016.04.034, PMID: 27210550
43. Perkins LA, Holderbaum L, Tao R, Hu Y, Sopko R, McCall K, Yang-Zhou D, Flockhart I, Binari R, Shim HS, Miller A, Housden A, Foos M, Randkelv S, Kelley C, Namgyal P, Villalta C, Liu LP, Jiang X, Huan-Huan Q, et al. 2015. The transgenic RNAi project at Harvard Medical School: resources and validation. Genetics 201:843–852. doi: 10.1534/genetics.115.180208, PMID: 26320097
44. Person AL, Khodakhah K. 2016. Recurrent feedback loops in associative learning. Neuron 89:427–430. doi: 10. 1016/j.neuron.2016.01.037, PMID: 26844826
45. Pfeiffer BD, Ngo TT, Hibbard KL, Murphy C, Jenett A, Truman JW, Rubin GM. 2010. Refinement of tools for targeted gene expression in Drosophila. Genetics 186:735–755. doi: 10.1534/genetics.110.119917, PMID: 206 97123
46. Plaçais PY, Trannoy S, Friedrich AB, Tanimoto H, Preat T. 2013. Two pairs of mushroom body efferent neurons are required for appetitive long-term memory retrieval in Drosophila. Cell Reports 5:769–780. doi: 10.1016/j. celrep.2013.09.032, PMID: 24209748
47. Qin H, Cressy M, Li W, Coravos JS, Izzi SA, Dubnau J. 2012. Gamma neurons mediate dopaminergic input during aversive olfactory memory formation in Drosophila. Current Biology 22:608–614. doi: 10.1016/j.cub.2012.02. 014, PMID: 22425153
48. Riemensperger T, Völler T, Stock P, Buchner E, Fiala A. 2005. Punishment prediction by dopaminergic neurons in Drosophila. Current Biology 15:1953–1960. doi: 10.1016/j.cub.2005.09.042, PMID: 16271874
49. Schroll C, Riemensperger T, Bucher D, Ehmer J, Völler T, Erbguth K, Gerber B, Hendel T, Nagel G, Buchner E, Fiala A. 2006. Light-induced activation of distinct modulatory neurons triggers appetitive or aversive learning in Drosophila larvae. Current Biology 16:1741–1747. doi: 10.1016/j.cub.2006.07.023, PMID: 16950113
50. Schwaerzel M, Monastirioti M, Scholz H, Friggi-Grelin F, Birman S, Heisenberg M. 2003. Dopamine and octopamine differentiate between aversive and appetitive olfactory memories in Drosophila. Journal of Neuroscience 23:10495–10502. PMID: 14627633
51. Shaw PJ, Cirelli C, Greenspan RJ, Tononi G. 2000. Correlates of sleep and waking in Drosophila melanogaster. Science 287:1834–1837. doi: 10.1126/science.287.5459.1834, PMID: 10710313
52. Séjourné J, Plaçais PY, Aso Y, Siwanowicz I, Trannoy S, Thoma V, Tedjakumala SR, Rubin GM, Tchénio P, Ito K, Isabel G, Tanimoto H, Preat T. 2011. Mushroom body efferent neurons responsible for aversive olfactory memory retrieval in Drosophila. Nature Neuroscience 14:903–910. doi: 10.1038/nn.2846, PMID: 21685917
53. Tian L, Hires SA, Mao T, Huber D, Chiappe ME, Chalasani SH, Petreanu L, Akerboom J, McKinney SA, Schreiter ER, Bargmann CI, Jayaraman V, Svoboda K, Looger LL. 2009. Imaging neural activity in worms, flies and mice with improved GCaMP calcium indicators. Nature Methods 6:875–881. doi: 10.1038/nmeth.1398, PMID: 1 9898485
54. Tomchik SM, Davis RL. 2009. Dynamics of learning-related cAMP signaling and stimulus integration in the Drosophila olfactory pathway. Neuron 64:510–521. doi: 10.1016/j.neuron.2009.09.029, PMID: 19945393
55. Tomchik SM. 2013. Dopaminergic neurons encode a distributed, asymmetric representation of temperature in Drosophila. Journal of Neuroscience 33:2166–2176. doi: 10.1523/JNEUROSCI.3933-12.2013, PMID: 23365252
56. Waddell S. 2016. Neural plasticity: dopamine tunes the mushroom body output network. Current Biology 26: R109–R112. doi: 10.1016/j.cub.2015.12.023, PMID: 26859265
57. Walkinshaw E, Gai Y, Farkas C, Richter D, Nicholas E, Keleman K, Davis RL. 2015. Identification of genes that promote or inhibit olfactory memory formation in Drosophila. Genetics 199:1173–1182. doi: 10.1534/genetics.114.173575, PMID: 25644700
58. Yagi R, Mabuchi Y, Mizunami M, Tanaka NK. 2016. Convergence of multimodal sensory pathways to the mushroom body calyx in Drosophila melanogaster. Scientific Reports 6:29481. doi: 10.1038/srep29481, PMID: 27404960
59. Yao Z, Macara AM, Lelito KR, Minosyan TY, Shafer OT. 2012. Analysis of functional neuronal connectivity in the Drosophila brain. Journal of Neurophysiology 108:684–696. doi: 10.1152/jn.00110.2012, PMID: 22539819
60. Yoder N. 2011. PeakFinder. http://www.mathworks.com/matlabcentral/fileexchange/25500.