Toward nanoscale localization of memory engrams in Drosophila

References

• Akalal, D.B., Wilson, C.F., Zong, L., Tanaka, N.K., Ito, K., & Davis, R.L. (2006). Roles for Drosophila mushroom body neurons in olfactory learning and memory. Learn & Memory, 13, 659–668. doi:10.1101/lm.221206
   PubMed Web of Science ®Google Scholar
• Aso, Y., Hattori, D., Yu, Y., Johnston, R.M., Iyer, N.A., Ngo, T.T., … Rubin, G.M. (2014). The neuronal architecture of the mushroom body provides a logic for associative learning. Elife, 3, e04577. doi:10.7554/eLife.04577
   PubMed Web of Science ®Google Scholar
• Aso, Y., Ray, R.P., Long, X., Bushey, D., Cichewicz, K., Ngo, T.T., … Rubin, G.M. (2019). Nitric oxide acts as a cotransmitter in a subset of dopaminergic neurons to diversify memory dynamics. Elife, 8, e49257. doi:10.7554/eLife.49257
   PubMed Web of Science ®Google Scholar
• Aso, Y., & Rubin, G.M. (2016). Dopaminergic neurons write and update memories with cell-type-specific rules. Elife, 5, e16135. doi:10.7554/eLife.16135
   PubMed Web of Science ®Google Scholar
• Aso, Y., Sitaraman, D., Ichinose, T., Kaun, K.R., Vogt, K., Belliart-Guerin, G., … Rubin, G.M. (2014). Mushroom body output neurons encode valence and guide memory-based action selection in Drosophila. Elife, 3, e04580. doi:10.7554/eLife.04580
   PubMed Web of Science ®Google Scholar
• Awata, H., Takakura, M., Kimura, Y., Iwata, I., Masuda, T., & Hirano, Y. (2019). The neural circuit linking mushroom body parallel circuits induces memory consolidation in Drosophila. Proceedings of the National Academy of Sciences of the United States of America, 116, 16080–16085. doi:10.1073/pnas.1901292116
   PubMed Web of Science ®Google Scholar
• Benzer, S. (1971). From the gene to behavior. JAMA, 218, 1015–1022. doi:10.1001/jama.1971.03190200047010
   PubMed Web of Science ®Google Scholar
• Berry, J.A., Cervantes-Sandoval, I., Nicholas, E.P., & Davis, R.L. (2012). Dopamine is required for learning and forgetting in Drosophila. Neuron, 74, 530–542. doi:10.1016/j.neuron.2012.04.007
   PubMed Web of Science ®Google Scholar
• Berry, J.A., Phan, A., & Davis, R.L. (2018). Dopamine neurons mediate learning and forgetting through bidirectional modulation of a memory trace. Cell Reports, 25, 651–662.e5. doi:10.1016/j.celrep.2018.09.051
   PubMed Web of Science ®Google Scholar
• Blum, A.L., Li, W.H., Cressy, M., & Dubnau, J. (2009). Short- and long-term memory in Drosophila require cAMP signaling in distinct neuron types. Current Biology, 19, 1341–1350. doi:10.1016/j.cub.2009.07.016
   PubMed Web of Science ®Google Scholar
• Brand, A.H., & Perrimon, N. (1993). Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development, 118, 401–415.
   PubMed Web of Science ®Google Scholar
• Chang, J.Y., Parra-Bueno, P., Laviv, T., Szatmari, E.M., Lee, S.R., & Yasuda, R. (2017). CaMKII autophosphorylation is necessary for optimal integration of Ca(2+) signals during LTP induction, but not maintenance. Neuron, 94, 800–808 e4. doi:10.1016/j.neuron.2017.04.041
   PubMed Web of Science ®Google Scholar
• Chen, B.C., Legant, W.R., Wang, K., Shao, L., Milkie, D.E., Davidson, M.W., … Betzig, E. (2014). Lattice light-sheet microscopy: imaging molecules to embryos at high spatiotemporal resolution. Science, 346, 1257998. doi:10.1126/science.1257998
   PubMed Web of Science ®Google Scholar
• Chen, F., Tillberg, P.W., & Boyden, E.S. (2015). Optical imaging. Expansion microscopy. Science, 347, 543–548. doi:10.1126/science.1260088
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• Connolly, J.B., Roberts, I.J.H., Armstrong, J.D., Kaiser, K., Forte, M., Tully, T., & O'Kane, C.J. (1996). Associative learning disrupted by impaired Gs signaling in Drosophila mushroom bodies. Science, 274, 2104–2107. doi:10.1126/science.274.5295.2104
   PubMed Web of Science ®Google Scholar
• Dionne, H., Hibbard, K.L., Cavallaro, A., Kao, J.C., & Rubin, G.M. (2018). Genetic reagents for making split-GAL4 lines in Drosophila. Genetics, 209, 31–35. doi:10.1534/genetics.118.300682
   PubMed Web of Science ®Google Scholar
• Dolan, M.J., Belliart-Guerin, G., Bates, A.S., Frechter, S., Lampin-Saint-Amaux, A., Aso, Y., … Jefferis, G. (2018). Communication from learned to innate olfactory processing centers is required for memory retrieval in Drosophila. Neuron, 100, 651–668.e8. doi:10.1016/j.neuron.2018.08.037
   PubMed Web of Science ®Google Scholar
• Dudai, Y., Jan, Y.N., Byers, D., Quinn, W.G., & Benzer, S. (1976). Dunce, a mutant of Drosophila deficient in learning. Proceedings of the National Academy of Sciences of the United States of America, 73, 1684–1688. doi:10.1073/pnas.73.5.1684
   PubMed Web of Science ®Google Scholar
• Eichler, K., Li, F., Litwin-Kumar, A., Park, Y., Andrade, I., Schneider-Mizell, C.M., … Cardona, A. (2017). The complete connectome of a learning and memory centre in an insect brain. Nature, 548, 175–182. doi:10.1038/nature23455
   PubMed Web of Science ®Google Scholar
• Felsenberg, J., Jacob, P.F., Walker, T., Barnstedt, O., Edmondson-Stait, A.J., Pleijzier, M.W., … Waddell, S. (2018). Integration of parallel opposing memories underlies memory extinction. Cell, 175, 709–722.e15. doi:10.1016/j.cell.2018.08.021
   PubMed Web of Science ®Google Scholar
• Gao, R., Asano, S.M., Upadhyayula, S., Pisarev, I., Milkie, D.E., Liu, T.L., … Betzig, E. (2019). Cortical column and whole-brain imaging with molecular contrast and nanoscale resolution. Science, 363, eaau8302. doi:10.1126/science.aau8302
   PubMed Web of Science ®Google Scholar
• Gervasi, N., Tchenio, 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, 516–529. doi:10.1016/j.neuron.2010.01.014
   PubMed Web of Science ®Google Scholar
• Han, K.A., Millar, N.S., Grotewiel, M.S., & Davis, R.L. (1996). DAMB, a novel dopamine receptor expressed specifically in Drosophila mushroom bodies. Neuron, 16, 1127–1135. doi:10.1016/S0896-6273(00)80139-7
   PubMed Web of Science ®Google Scholar
• Handler, A., Graham, T.G.W., Cohn, R., Morantte, I., Siliciano, A.F., Zeng, J., … Ruta, V. (2019). Distinct dopamine receptor pathways underlie the temporal sensitivity of associative learning. Cell, 178, 60–75.e19. doi:10.1016/j.cell.2019.05.040
   PubMed Web of Science ®Google Scholar
• Hattori, D., Aso, Y., Swartz, K.J., Rubin, G.M., Abbott, L.F., & Axel, R. (2017). Representations of Novelty and familiarity in a mushroom body compartment. Cell, 169, 956–969.e17. doi:10.1016/j.cell.2017.04.028
   PubMed Web of Science ®Google Scholar
• Heisenberg, M., Borst, A., Wagner, S., & Byers, D. (1985). Drosophila mushroom body mutants are deficient in olfactory learning. Journal of Neurogenetics, 2, 1–30. doi:10.3109/01677068509100140
   PubMed Web of Science ®Google Scholar
• Hige, T., Aso, Y., Modi, M.N., Rubin, G.M., & Turner, G.C. (2015). Heterosynaptic plasticity underlies aversive olfactory learning in Drosophila. Neuron, 88, 985–998. doi:10.1016/j.neuron.2015.11.003
   PubMed Web of Science ®Google Scholar
• Hige, T., Aso, Y., Rubin, G.M., & Turner, G.C. (2015). Plasticity-driven individualization of olfactory coding in mushroom body output neurons. Nature, 526, 258–262. doi:10.1038/nature15396
   PubMed Web of Science ®Google Scholar
• Huetteroth, W., Perisse, E., Lin, S.W., Klappenbach, M., Burke, C., & Waddell, S. (2015). Sweet taste and nutrient value subdivide rewarding dopaminergic neurons in Drosophila. Current Biology, 25, 751–758. doi:10.1016/j.cub.2015.01.036
   PubMed Web of Science ®Google Scholar
• Ichinose, T., Aso, Y., Yamagata, N., Abe, A., Rubin, G.M., & Tanimoto, H. (2015). Reward signal in a recurrent circuit drives appetitive long-term memory formation. Elife, 4, e10719. doi:10.7554/eLife.10719
   PubMed Web of Science ®Google Scholar
• Keene, A.C., & Waddell, S. (2007). Drosophila olfactory memory: Single genes to complex neural circuits. Nature Reviews Neuroscience, 8, 341–354. doi:10.1038/nrn2098
   PubMed Web of Science ®Google Scholar
• Kim, Y.C., Lee, H.G., & Han, K.A. (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
   PubMed Web of Science ®Google Scholar
• Kim, Y.K., Saver, M., Simon, J., Kent, C.F., Shao, L., Eddison, M., … Heberlein, U. (2018). Repetitive aggressive encounters generate a long-lasting internal state in Drosophila melanogaster males. Proceedings of the National Academy of Sciences of the United States of America, 115, 1099–1104. doi:10.1073/pnas.1716612115
   PubMed Web of Science ®Google Scholar
• Knapek, S., Sigrist, S., & Tanimoto, H. (2011). Bruchpilot, a synaptic active zone protein for anesthesia-resistant memory. Journal of Neuroscience, 31, 3453–3458. doi:10.1523/JNEUROSCI.2585-10.2011
   PubMed Web of Science ®Google Scholar
• Konig, C., Khalili, A., Ganesan, M., Nishu, A.P., Garza, A.P., Niewalda, T., … Yarali, A. (2018). Reinforcement signaling of punishment versus relief in fruit flies. Learn and Memory, 25, 247–257. doi:10.1101/lm.047308.118
   PubMed Web of Science ®Google Scholar
• Kruttner, S., Traunmuller, L., Dag, U., Jandrasits, K., Stepien, B., Iyer, N., … Keleman, K. (2015). Synaptic Orb2A bridges memory acquisition and late memory consolidation in Drosophila. Cell Rep, 11, 1953–1965. doi:10.1016/j.celrep.2015.05.037
   PubMed Web of Science ®Google Scholar
• Lewis, L.P.C., Siju, K.P., Aso, Y., Friedrich, A.B., Bulteel, A.J.B., Rubin, G.M., & Kadow, I.C.G. (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
   PubMed Web of Science ®Google Scholar
• Liu, Q., Yang, X., Tian, J., Gao, Z., Wang, M., Li, Y., & Guo, A. (2016). Gap junction networks in mushroom bodies participate in visual learning and memory in Drosophila. Elife, 5, e13238. doi:10.7554/eLife.13238
   PubMed Web of Science ®Google Scholar
• Livingstone, M.S., Sziber, P.P., & Quinn, W.G. (1984). Loss of calcium calmodulin responsiveness in adenylate-cyclase of rutabaga, a Drosophila learning mutant. Cell, 37, 205–215. doi:10.1016/0092-8674(84)90316-7
   PubMed Web of Science ®Google Scholar
• Louis, T., Stahl, A., Boto, T., & Tomchik, S.M. (2018). Cyclic AMP-dependent plasticity underlies rapid changes in odor coding associated with reward learning. Proceedings of the National Academy of Sciences of the United States of America, 115, E448–E457. doi:10.1073/pnas.1709037115
   PubMed Web of Science ®Google Scholar
• Luan, H., Peabody, N.C., Vinson, C.R., & White, B.H. (2006). Refined spatial manipulation of neuronal function by combinatorial restriction of transgene expression. Neuron, 52, 425–436. doi:10.1016/j.neuron.2006.08.028
   PubMed Web of Science ®Google Scholar
• Mao, Z., & Davis, R.L. (2009). Eight different types of dopaminergic neurons innervate the Drosophila mushroom body neuropil: Anatomical and physiological heterogeneity. Frontiers in Neural Circuits, 3, 5doi:10.3389/neuro.04.005.2009
   PubMed Web of Science ®Google Scholar
• Margulies, C., Tully, T., & Dubnau, J. (2005). Deconstructing memory in Drosophila. Current Biology, 15, R700–R713. doi:10.1016/j.cub.2005.08.024
   PubMed Web of Science ®Google Scholar
• Masek, P., Worden, K., Aso, Y., Rubin, G.M., & Keene, A.C. (2015). A dopamine-modulated neural circuit regulating aversive taste memory in Drosophila. Current Biology, 25, 1535–1541. doi:10.1016/j.cub.2015.04.027
   PubMed Web of Science ®Google Scholar
• Mcguire, S.E., Deshazer, M., & Davis, R.L. (2005). Thirty years of olfactory learning and memory research in Drosophila melanogaster. Progress in Neurobiology, 76, 328–347. doi:10.1016/j.pneurobio.2005.09.003
   PubMed Web of Science ®Google Scholar
• Mcguire, S.E., Le, P.T., Osborn, A.J., Matsumoto, K., & Davis, R.L. (2003). Spatiotemporal rescue of memory dysfunction in Drosophila. Science, 302, 1765–1768. doi:10.1126/science.1089035
   PubMed Web of Science ®Google Scholar
• Murakoshi, H., Shin, M.E., Parra-Bueno, P., Szatmari, E.M., Shibata, A.C.E., & Yasuda, R. (2017). Kinetics of endogenous CaMKII required for synaptic plasticity revealed by optogenetic kinase inhibitor. Neuron, 94, 690. doi:10.1016/j.neuron.2017.04.027
   PubMed Web of Science ®Google Scholar
• Niewalda, T., Michels, B., Jungnickel, R., Diegelmann, S., Kleber, J., Kahne, T., & Gerber, B. (2015). Synapsin determines memory strength after punishment- and relief-learning. Journal of Neuroscience, 35, 7487–7502. doi:10.1523/JNEUROSCI.4454-14.2015
   PubMed Web of Science ®Google Scholar
• Oliveira, A.F., & Yasuda, R. (2013). An improved Ras sensor for highly sensitive and quantitative FRET-FLIM imaging. PLoS One, 8, e52874. doi:10.1371/journal.pone.0052874
   PubMed Web of Science ®Google Scholar
• Pavot, P., Carbognin, E., & Martin, J.R. (2015). PKA and cAMP/CNG channels independently regulate the cholinergic Ca(2+)-response of Drosophila mushroom body neurons(1,2,3). eNeuro, 2. doi:10.1523/ENEURO.0054-14.2015
   PubMed Web of Science ®Google Scholar
• Perisse, E., Owald, D., Barnstedt, O., Talbot, C.B., 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
   PubMed Web of Science ®Google Scholar
• Pfeiffer, B.D., Ngo, T.T., Hibbard, K.L., Murphy, C., Jenett, A., Truman, J.W., & Rubin, G.M. (2010). Refinement of tools for targeted gene expression in Drosophila. Genetics, 186, 735–755. doi:10.1534/genetics.110.119917
   PubMed Web of Science ®Google Scholar
• Qin, H., Cressy, M., Li, W., Coravos, J.S., Izzi, S.A., & Dubnau, J. (2012). Gamma neurons mediate dopaminergic input during aversive olfactory memory formation in Drosophila. Curr Biol, 22, 608–614. doi:10.1016/j.cub.2012.02.014
   PubMed Web of Science ®Google Scholar
• Scheib, U., Broser, M., Constantin, O.M., Yang, S., Gao, S., Mukherjee, S., … Hegemann, P. (2018). Rhodopsin-cyclases for photocontrol of cGMP/cAMP and 2.3 A structure of the adenylyl cyclase domain. Nature Communications, 9, 2046. doi:10.1038/s41467-018-04428-w
   PubMed Web of Science ®Google Scholar
• Scheunemann, L., Placais, P.Y., Dromard, Y., Schwarzel, M., & Preat, T. (2018). Dunce phosphodiesterase acts as a checkpoint for Drosophila long-term memory in a pair of serotonergic neurons. Neuron, 98, 350–365.e5. doi:10.1016/j.neuron.2018.03.032
   PubMed Web of Science ®Google Scholar
• Scholz-Kornehl, S., & Schwarzel, M. (2016). Circuit analysis of a Drosophila dopamine type 2 receptor that supports anesthesia-resistant memory. Journal of Neuroscience, 36, 7936–7945. doi:10.1523/JNEUROSCI.4475-15.2016
   PubMed Web of Science ®Google Scholar
• Shuai, Y., Lu, B., Hu, Y., Wang, L., Sun, K., & Zhong, Y. (2010). Forgetting is regulated through Rac activity in Drosophila. Cell, 140, 579–589. doi:10.1016/j.cell.2009.12.044
   PubMed Web of Science ®Google Scholar
• Skoulakis, E.M., Kalderon, D., & Davis, R.L. (1993). Preferential expression in mushroom bodies of the catalytic subunit of protein kinase A and its role in learning and memory. Neuron, 11, 197–208. doi:10.1016/0896-6273(93)90178-T
   PubMed Web of Science ®Google Scholar
• Takemura, S.Y., Aso, Y., Hige, T., Wong, A., Lu, Z., Xu, C.S., … Scheffer, L.K. (2017). A connectome of a learning and memory center in the adult Drosophila brain. Elife, 6. doi:10.7554/eLife.26975
   Web of Science ®Google Scholar
• Tanaka, N.K., Tanimoto, H., & Ito, K. (2008). Neuronal assemblies of the Drosophila mushroom body. Journal of Comparative Neurology, 508, 711–755. doi:10.1002/cne.21692
   PubMed Web of Science ®Google Scholar
• Tang, S., & Yasuda, R. (2017). Imaging ERK and PKA activation in single dendritic spines during structural plasticity. Neuron, 93, 1315–1324.e3. doi:10.1016/j.neuron.2017.02.032
   PubMed Web of Science ®Google Scholar
• Thurmond, J., Goodman, J.L., Strelets, V.B., Attrill, H., Gramates, L.S., Marygold, S.J., Matthews, B.B., Millburn, G., Antonazzo, G., Trovisco, V., Kaufman, T.C., Calvi, B.R., & Flybase, C.; FlyBase Consortium. (2019). FlyBase 2.0: The next generation. Nucleic Acids Research, 47, D759–D765. doi:10.1093/nar/gky1003
   PubMed Web of Science ®Google Scholar
• Tillberg, P.W., Chen, F., Piatkevich, K.D., Zhao, Y., Yu, C.C., English, B.P., … Boyden, E.S. (2016). Protein-retention expansion microscopy of cells and tissues labeled using standard fluorescent proteins and antibodies. Nature Biotechnology, 34, 987–992. doi:10.1038/nbt.3625
   PubMed Web of Science ®Google Scholar
• Trannoy, S., Redt-Clouet, C., Dura, J.M., & Preat, T. (2011). Parallel processing of appetitive short- and long-term memories in Drosophila. Current Biology, 21, 1647–1653. doi:10.1016/j.cub.2011.08.032
   PubMed Web of Science ®Google Scholar
• Tsao, C.-H., Chen, C.-C., Lin, C.-H., Yang, H.-Y., & Lin, S. (2018). Drosophila mushroom bodies integrate hunger and satiety signals to control innate food-seeking behavior. Elife, 7, e35264. doi:10.7554/eLife.35264
   PubMed Web of Science ®Google Scholar
• Tumkaya, T., Ott, S., & Claridge-Chang, A. (2018). A systematic review of Drosophila short-term-memory genetics: Meta-analysis reveals robust reproducibility. Neuroscience & Biobehavioral Reviews, 95, 361–382. doi:10.1016/j.neubiorev.2018.07.016
   PubMed Web of Science ®Google Scholar
• Vanover, K.E., Davis, R.E., Zhou, Y., Ye, W., Brasic, J.R., Gapasin, L., … Wong, D.F. (2018). Dopamine D2 receptor occupancy of lumateperone (ITI-007): A Positron Emission Tomography Study in patients with schizophrenia. Neuropsychopharmacology, 44, 598–605. doi:10.1038/s41386-018-0251-1
   PubMed Web of Science ®Google Scholar
• Vogt, K., Aso, Y., Hige, T., Knapek, S., Ichinose, T., Friedrich, A.B., … Tanimoto, H. (2016). Direct neural pathways convey distinct visual information to Drosophila mushroom bodies. Elife, 5, e14009. doi:10.7554/eLife.14009
   PubMed Web of Science ®Google Scholar
• Waddell, S., Armstrong, J.D., Kitamoto, T., Kaiser, K., & Quinn, W.G. (2000). The amnesiac gene product is expressed in two neurons in the Drosophila brain that are critical for memory. Cell, 103, 805–813. doi:10.1016/s0092-8674(00)00183-5
   PubMed Web of Science ®Google Scholar
• Walkinshaw, E., Gai, Y., Farkas, C., Richter, D., Nicholas, E., Keleman, K., & Davis, R.L. (2015). Identification of genes that promote or inhibit olfactory memory formation in Drosophila. Genetics, 199, 1173–1182. doi:10.1534/genetics.114.173575
   PubMed Web of Science ®Google Scholar
• Yamagata, N., Hiroi, M., Kondo, S., Abe, A., Tabata, T., & Tanimoto, H. (2015). Suppression of dopamine neurons for memory formation. Genes & Genetic Systems, 90, 366–366.
   Web of Science ®Google Scholar
• Yamagata, N., Ichinose, T., Aso, Y., Placais, P.Y., Friedrich, A.B., Sima, R.J., … Tanimoto, H. (2015). 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, 112, 578–583. doi:10.1073/pnas.1421930112
   PubMed Web of Science ®Google Scholar
• Youn, H., Kirkhart, C., Chia, J., & Scott, K. (2018). A subset of octopaminergic neurons that promotes feeding initiation in Drosophila melanogaster. Plos One, 13, e0198362. doi:10.1371/journal.pone.0198362
   PubMed Web of Science ®Google Scholar
• Zars, T., Fischer, M., Schulz, R., & Heisenberg, M. (2000). Localization of a short-term memory in Drosophila. Science, 288, 672–675. doi:10.1126/science.288.5466.672
   PubMed Web of Science ®Google Scholar
• Zheng, Z., Lauritzen, J.S., Perlman, E., Robinson, C.G., Nichols, M., Milkie, D., … Bock, D.D. (2018). A complete electron microscopy volume of the brain of adult Drosophila melanogaster. Cell, 174, 730–743 e22. doi:10.1016/j.cell.2018.06.019
   PubMed Web of Science ®Google Scholar
• Zhong, Y., & Wu, C.F. (1991). Altered synaptic plasticity in Drosophila memory mutants with a defective cyclic AMP cascade. Science, 251, 198–201. doi:10.1126/science.1670967
   PubMed Web of Science ®Google Scholar