Representations of Novelty and Familiarity in a Mushroom Body Compartment

Cell

Volumn 169, Issue 5, 2017, Pages 956-969.e17

  Hattori, Daisuke ^a   Aso, Yoshinori ^b   Swartz, Kurtis J ^a   Rubin, Gerald M ^b   Abbott, L F ^a   Axel, Richard ^a  

^a Howard Hughes Medical Institute   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

alerting response; dopamine; Drosophila melanogaster; mushroom body; novelty and familiarity; olfactory learning and memory; repetition suppression

Indexed keywords

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN TISSUE; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; DROSOPHILA; KENYON CELL; MUSHROOM BODY; NERVE CELL; NONHUMAN; OLFACTORY SYSTEM; PRIORITY JOURNAL; ANIMAL; CYTOLOGY; DROSOPHILA MELANOGASTER; LEARNING; MEMORY; ODOR; PHYSIOLOGY;

FRAGRANCE;

ANIMALS; DOPAMINERGIC NEURONS; DROSOPHILA MELANOGASTER; LEARNING; MEMORY; MUSHROOM BODIES; ODORANTS; SMELL;

EID: 85019077864     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2017.04.028     Document Type: Article

References (63)

1. Aso, Y., Rubin, G.M., Dopaminergic neurons write and update memories with cell-type-specific rules. eLife, 2016, 10.7554/eLife.16135 Published July 21, 2016.
2. Aso, Y., Hattori, D., Yu, Y., Johnston, R.M., Iyer, N.A., Ngo, T.T., Dionne, H., Abbott, L.F., Axel, R., Tanimoto, H., Rubin, G.M., The neuronal architecture of the mushroom body provides a logic for associative learning. eLife, 3, 2014, e04577.
3. Aso, Y., Sitaraman, D., Ichinose, T., Kaun, K.R., Vogt, K., Belliart-Guérin, G., Plaçais, P.Y., Robie, A.A., Yamagata, N., Schnaitmann, C., et al. Mushroom body output neurons encode valence and guide memory-based action selection in Drosophila. eLife, 3, 2014, e04580.
4. Baines, R.A., Uhler, J.P., Thompson, A., Sweeney, S.T., Bate, M., Altered electrical properties in Drosophila neurons developing without synaptic transmission. J. Neurosci. 21 (2001), 1523–1531.
5. Berry, J.A., Cervantes-Sandoval, I., Chakraborty, M., Davis, R.L., Sleep facilitates memory by blocking dopamine neuron-mediated forgetting. Cell 161 (2015), 1656–1667.
6. Berry, J.A., Cervantes-Sandoval, I., Nicholas, E.P., Davis, R.L., Dopamine is required for learning and forgetting in Drosophila. Neuron 74 (2012), 530–542.
7. 2 avoidance in Drosophila. Curr. Biol. 23 (2013), 1228–1234.
8. Bromberg-Martin, E.S., Matsumoto, M., Hikosaka, O., Dopamine in motivational control: Rewarding, aversive, and alerting. Neuron 68 (2010), 815–834.
9. Brown, M.W., Banks, P.J., In search of a recognition memory engram. Neurosci. Biobehav. Rev. 50 (2015), 12–28.
10. Buckner, R.L., Goodman, J., Burock, M., Rotte, M., Koutstaal, W., Schacter, D., Rosen, B., Dale, A.M., Functional-anatomic correlates of object priming in humans revealed by rapid presentation event-related fMRI. Neuron 20 (1998), 285–296.
11. Bunzeck, N., Düzel, E., Absolute coding of stimulus novelty in the human substantia nigra/VTA. Neuron 51 (2006), 369–379.
12. Cassenaer, S., Laurent, G., Hebbian STDP in mushroom bodies facilitates the synchronous flow of olfactory information in locusts. Nature 448 (2007), 709–713.
13. Chen, T.W., Wardill, T.J., Sun, Y., Pulver, S.R., Renninger, S.L., Baohan, A., Schreiter, E.R., Kerr, R.A., Orger, M.B., Jayaraman, V., et al. Ultrasensitive fluorescent proteins for imaging neuronal activity. Nature 499 (2013), 295–300.
14. Cohn, R., Morantte, I., Ruta, V., Coordinated and Compartmentalized Neuromodulation Shapes Sensory Processing in Drosophila. Cell 163 (2015), 1742–1755.
15. Desimone, R., Neural mechanisms for visual memory and their role in attention. Proc. Natl. Acad. Sci. USA 93 (1996), 13494–13499.
16. Diao, F., Ironfield, H., Luan, H., Diao, F., Shropshire, W.C., Ewer, J., Marr, E., Potter, C.J., Landgraf, M., White, B.H., Plug-and-play genetic access to Drosophila cell types using exchangeable exon cassettes. Cell Rep. 10 (2015), 1410–1421.
17. Dubnau, J., Grady, L., Kitamoto, T., Tully, T., Disruption of neurotransmission in Drosophila mushroom body blocks retrieval but not acquisition of memory. Nature 411 (2001), 476–480.
18. Fişek, M., Wilson, R.I., Stereotyped connectivity and computations in higher-order olfactory neurons. Nat. Neurosci. 17 (2014), 280–288.
19. Galili, D.S., Dylla, K.V., Lüdke, A., Friedrich, A.B., Yamagata, N., Wong, J.Y., Ho, C.H., Szyszka, P., Tanimoto, H., Converging circuits mediate temperature and shock aversive olfactory conditioning in Drosophila. Curr. Biol. 24 (2014), 1712–1722.
20. Guizar-Sicairos, M., Thurman, S.T., Fienup, J.R., Efficient subpixel image registration algorithms. Opt. Lett. 33 (2008), 156–158.
21. Hampel, S., Franconville, R., Simpson, J.H., Seeds, A.M., A neural command circuit for grooming movement control. eLife, 4, 2015, e08758.
22. Han, K.A., Millar, N.S., Grotewiel, M.S., Davis, R.L., DAMB, a novel dopamine receptor expressed specifically in Drosophila mushroom bodies. Neuron 16 (1996), 1127–1135.
23. Heisenberg, M., Mushroom body memoir: From maps to models. Nat. Rev. Neurosci. 4 (2003), 266–275.
24. Hige, T., Aso, Y., Modi, M.N., Rubin, G.M., Turner, G.C., Heterosynaptic Plasticity Underlies Aversive Olfactory Learning in Drosophila. Neuron 88 (2015), 985–998.
25. Hige, T., Aso, Y., Rubin, G.M., Turner, G.C., Plasticity-driven individualization of olfactory coding in mushroom body output neurons. Nature 526 (2015), 258–262.
26. Honegger, K.S., Campbell, R.A., Turner, G.C., Cellular-resolution population imaging reveals robust sparse coding in the Drosophila mushroom body. J. Neurosci. 31 (2011), 11772–11785.
27. 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, 2015, 10.7554/eLife.11346 Published online December 29, 2015.
28. 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. 5 (1998), 52–77.
29. Joiner, W.J., Crocker, A., White, B.H., Sehgal, A., Sleep in Drosophila is regulated by adult mushroom bodies. Nature 441 (2006), 757–760.
30. Kazama, H., Wilson, R.I., Homeostatic matching and nonlinear amplification at identified central synapses. Neuron 58 (2008), 401–413.
31. Khouri, L., Nelken, I., Detecting the unexpected. Curr. Opin. Neurobiol. 35 (2015), 142–147.
32. Kim, Y.C., Lee, H.G., Seong, C.S., Han, K.A., Expression of a D1 dopamine receptor dDA1/DmDOP1 in the central nervous system of Drosophila melanogaster. Gene Expr. Patterns 3 (2003), 237–245.
33. Kirkhart, C., Scott, K., Gustatory learning and processing in the Drosophila mushroom bodies. J. Neurosci. 35 (2015), 5950–5958.
34. Kitamoto, T., Conditional modification of behavior in Drosophila by targeted expression of a temperature-sensitive shibire allele in defined neurons. J. Neurobiol. 47 (2001), 81–92.
35. Klapoetke, N.C., Murata, Y., Kim, S.S., Pulver, S.R., Birdsey-Benson, A., Cho, Y.K., Morimoto, T.K., Chuong, A.S., Carpenter, E.J., Tian, Z., et al. Independent optical excitation of distinct neural populations. Nat. Methods 11 (2014), 338–346.
36. 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 139 (2009), 416–427.
37. Larsson, M.C., Domingos, A.I., Jones, W.D., Chiappe, M.E., Amrein, H., Vosshall, L.B., Or83b encodes a broadly expressed odorant receptor essential for Drosophila olfaction. Neuron 43 (2004), 703–714.
38. Lin, S., Owald, D., Chandra, V., Talbot, C., Huetteroth, W., Waddell, S., Neural correlates of water reward in thirsty Drosophila. Nat. Neurosci. 17 (2014), 1536–1542.
39. 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 488 (2012), 512–516.
40. Ljungberg, T., Apicella, P., Schultz, W., Responses of monkey dopamine neurons during learning of behavioral reactions. J. Neurophysiol. 67 (1992), 145–163.
41. Malmierca, M.S., Anderson, L.A., Antunes, F.M., The cortical modulation of stimulus-specific adaptation in the auditory midbrain and thalamus: A potential neuronal correlate for predictive coding. Front. Syst. Neurosci., 9, 2015, 19.
42. Mao, Z., Davis, R.L., Eight different types of dopaminergic neurons innervate the Drosophila mushroom body neuropil: Anatomical and physiological heterogeneity. Front. Neural Circuits, 3, 2009, 5.
43. Nern, A., Pfeiffer, B.D., Rubin, G.M., Optimized tools for multicolor stochastic labeling reveal diverse stereotyped cell arrangements in the fly visual system. Proc. Natl. Acad. Sci. USA 112 (2015), E2967–E2976.
44. 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 (2007), 11736–11747.
45. Owald, D., Felsenberg, J., Talbot, C.B., Das, G., Perisse, E., Huetteroth, W., Waddell, S., Activity of defined mushroom body output neurons underlies learned olfactory behavior in Drosophila. Neuron 86 (2015), 417–427.
46. Parnas, M., Lin, A.C., Huetteroth, W., Miesenböck, G., Odor discrimination in Drosophila: From neural population codes to behavior. Neuron 79 (2013), 932–944.
47. Perisse, E., Owald, D., Barnstedt, O., Talbot, C.B., Huetteroth, W., Waddell, S., Aversive learning and appetitive motivation toggle feed-forward inhibition in the Drosophila mushroom body. Neuron 90 (2016), 1086–1099.
48. Perkins, L.A., Holderbaum, L., Tao, R., Hu, Y., Sopko, R., McCall, K., Yang-Zhou, D., Flockhart, I., Binari, R., Shim, H.S., et al. The transgenic RNAi Project at Harvard Medical School: Resources and validation. Genetics 201 (2015), 843–852.
49. Pfeiffer, B.D., Ngo, T.T., Hibbard, K.L., Murphy, C., Jenett, A., Truman, J.W., Rubin, G.M., Refinement of tools for targeted gene expression in Drosophila. Genetics 186 (2010), 735–755.
50. Pitman, J.L., McGill, J.J., Keegan, K.P., Allada, R., A dynamic role for the mushroom bodies in promoting sleep in Drosophila. Nature 441 (2006), 753–756.
51. 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. 15 (2012), 592–599.
52. Riemensperger, T., Völler, T., Stock, P., Buchner, E., Fiala, A., Punishment prediction by dopaminergic neurons in Drosophila. Curr. Biol. 15 (2005), 1953–1960.
53. Ruta, V., Datta, S.R., Vasconcelos, M.L., Freeland, J., Looger, L.L., Axel, R., A dimorphic pheromone circuit in Drosophila from sensory input to descending output. Nature 468 (2010), 686–690.
54. Seeds, A.M., Ravbar, P., Chung, P., Hampel, S., Midgley, F.M. Jr., Mensh, B.D., Simpson, J.H., A suppression hierarchy among competing motor programs drives sequential grooming in Drosophila. eLife, 3, 2014, e02951.
55. 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. 14 (2011), 903–910.
56. Sokolov, E.N., Higher nervous functions; the orienting reflex. Annu. Rev. Physiol. 25 (1963), 545–580.
57. Stopfer, M., Laurent, G., Short-term memory in olfactory network dynamics. Nature 402 (1999), 664–668.
58. Tanaka, N.K., Tanimoto, H., Ito, K., Neuronal assemblies of the Drosophila mushroom body. J. Comp. Neurol. 508 (2008), 711–755.
59. Turner, G.C., Bazhenov, M., Laurent, G., Olfactory representations by Drosophila mushroom body neurons. J. Neurophysiol. 99 (2008), 734–746.
60. Venken, K.J., Schulze, K.L., Haelterman, N.A., Pan, H., He, Y., Evans-Holm, M., Carlson, J.W., Levis, R.W., Spradling, A.C., Hoskins, R.A., Bellen, H.J., MiMIC: A highly versatile transposon insertion resource for engineering Drosophila melanogaster genes. Nat. Methods 8 (2011), 737–743.
61. Vosshall, L.B., Stocker, R.F., Molecular architecture of smell and taste in Drosophila. Annu. Rev. Neurosci. 30 (2007), 505–533.
62. Waddell, S., Reinforcement signalling in Drosophila; dopamine does it all after all. Curr. Opin. Neurobiol. 23 (2013), 324–329.
63. Wan, Y., Otsuna, H., Chien, C.B., and Hansen, C. (2012). FluoRender: An application of 2D image space methods for 3D and 4D confocal microscopy data visualization in neurobiology researchIn Proceedings of the IEEE Pacific Visualisation Symposium (IEEE Pacific Visualization Symposium), pp. 201–208.