Courtship behavior induced by appetitive olfactory memory

References

• Anderson, D.J., & Perona, P. (2014). Toward a science of computational ethology. Neuron, 84, 18–31. doi:10.1016/j.neuron.2014.09.005
   PubMed Web of Science ®Google Scholar
• Aso, Y., Hattori, D., Yu, Y., Johnston, R.M., Iyer, N.A., Ngo, T.-T.B., … 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
• Bitterman, M.E., Menzel, R., Fietz, A., & Schafer, S. (1983). Classical conditioning of proboscis extension in honeybees (Apis mellifera). Journal of Comparative Psychology, 97, 107–119. doi:10.1037/0735-7036.97.2.107
   PubMed Web of Science ®Google Scholar
• Blanchard, R.J., & Blanchard, D.C. (1969). Crouching as an index of fear. Journal of Comparative and Physiological Psychology, 67, 370–375. doi:10.1037/h0026779
   PubMed Web of Science ®Google Scholar
• Branson, K., Robie, A.A., Bender, J., Perona, P., & Dickinson, M.H. (2009). High-throughput ethomics in large groups of Drosophila. Nature Methods, 6, 451. doi:10.1038/nmeth.1328
   PubMed Web of Science ®Google Scholar
• Bravo-Rivera, C., Roman-Ortiz, C., Brignoni-Perez, E., Sotres-Bayon, F., & Quirk, G.J. (2014). Neural structures mediating expression and extinction of platform-mediated avoidance. Journal of Neuroscience, 34, 9736–9742. doi:10.1523/JNEUROSCI.0191-14.2014
   PubMed Web of Science ®Google Scholar
• Cervantes-Sandoval, I., Martin-Pena, A., Berry, J.A., & Davis, R.L. (2013). System-like consolidation of olfactory memories in Drosophila. Journal of Neuroscience, 33, 9846–9854. doi:10.1523/JNEUROSCI.0451-13.2013
   PubMed Web of Science ®Google Scholar
• Chabaud, M.A., Devaud, J.M., Pham-Delegue, M.H., Preat, T., & Kaiser, L. (2006). Olfactory conditioning of pr oboscis activity in Drosophila melanogaster. Journal of Comparative Physiology A: Neuroethology, Sensory, Neural, and Behavioral Physiology, 192, 1335–1348. doi:10.1007/s00359-006-0160-3
   PubMed Web of Science ®Google Scholar
• Chaffiol, A., Laloi, D., & Pham-Delegue, M.H. (2005). Prior classical olfactory conditioning improves odour-cued flight orientation of honey bees in a wind tunnel. Journal of Experimental Biology, 208, 3731–3737. doi:10.1242/jeb.01796
   PubMed Web of Science ®Google Scholar
• Cholé, H., Junca, P., & Sandoz, J.C. (2015). Appetitive but not aversive olfactory conditioning modifies antennal movements in honeybees. Learning & Memory, 22, 604–616. doi:10.1101/lm.038448.115
   PubMed Web of Science ®Google Scholar
• Christopher, J.T., & de Belle, J.S. (2014). Olfactory learning and memory assays. In J. Dubnau (Ed.), Behavioral genetics of the fly (Drosophila melanogaster) (pp. 231–249). Cambridge: Cambridge University Press.
   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
• Datta, S.R., Vasconcelos, M.L., Ruta, V., Luo, S., Wong, A., Demir, E., … Axel, R. (2008). The Drosophila pheromone cVA activates a sexually dimorphic neural circuit. Nature, 452, 473. doi:10.1038/nature06808
   PubMed Web of Science ®Google Scholar
• Dweck, H.K.M., Ebrahim, S.A.M., Thoma, M., Mohamed, A.A.M., Keesey, I.W., Trona, F., … Hansson, B.S. (2015). Pheromones mediating copulation and attraction in Drosophila. Proceedings of the National Academy of Sciences of the United States of America, 112, E2829–E2835. doi:10.1073/pnas.1504527112
   PubMed Web of Science ®Google Scholar
• Estes, W.K., & Skinner, B.F. (1941). Some quantitative properties of anxiety. Journal of Experimental Psychology, 29, 390–400. doi:10.1037/h0062283
   Google Scholar
• Frisch, K. R. V. (1919). Über den Geruchssinn der Bienen und seine blütenbiologische Bedeutung. Zoologische Jahrbücher. Abteilung für Allgemeine Zoologie und Physiologie der Tiere, 37, 1–238.
   Google Scholar
• Gerber, B., Tanimoto, H., & Heisenberg, M. (2004). An engram found? Evaluating the evidence from fruit flies. Current Opinion in Neurobiology, 14, 737–744. doi:10.1016/j.conb.2004.10.014
   PubMed Web of Science ®Google Scholar
• Grosjean, Y., Rytz, R., Farine, J.P., Abuin, L., Cortot, J., Jefferis, G.S.X.E., & Benton, R. (2011). An olfactory receptor for food-derived odours promotes male courtship in Drosophila. Nature, 478, 236–240. doi:10.1038/nature10428
   PubMed Web of Science ®Google Scholar
• Haenicke, J., Yamagata, N., Zwaka, H., Nawrot, M., & Menzel, R. (2018). Neural correlates of odor learning in the presynaptic microglomerular circuitry in the honeybee mushroom body calyx. eNeuro, 5, 1–13. doi:10.1523/ENEURO.0128-18.2018
   PubMed Web of Science ®Google Scholar
• Hall, J.C. (1994). The mating of a fly. Science, 264, 1702–1714. doi:10.1126/science.8209251
   PubMed Web of Science ®Google Scholar
• Hammer, M., & Menzel, R. (1998). Multiple sites of associative odor learning as revealed by local brain microinjections of octopamine in honeybees. Learning & Memory, 5, 146–156. doi:10.1101/lm.5.1.146
   PubMed Web of Science ®Google Scholar
• Heimbeck, G., Bugnon, V., Gendre, N., Keller, A., & Stocker, R.F. (2001). A central neural circuit for experience-independent olfactory and courtship behavior in Drosophila melanogaster. Proceedings of the National Academy of Sciences of the United States of America, 98, 15336–15341. doi:10.1073/pnas.011314898
   PubMed Web of Science ®Google Scholar
• Heisenberg, M. (2003). Mushroom body memoir: from maps to models. Nat Reviews Neuroscience, 4, 266–275. doi:10.1038/nrn1074
   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
• Ichinose, T., & Tanimoto, H. (2016). Dynamics of memory-guided choice behavior in Drosophila. Proceedings of the Japan Academy, Series B, Physical and Biological Sciences, 92, 346–357. doi:10.2183/pjab.92.346
   PubMed Web of Science ®Google Scholar
• Ichinose, T., Tanimoto, H., & Yamagata, N. (2017). Behavioral modulation by spontaneous activity of dopamine neurons. Frontiers in Systems Neuroscience, 11, 88.doi:10.3389/fnsys.2017.00088
   PubMed Web of Science ®Google Scholar
• Jallon, J.M., & Hotta, Y. (1979). Genetic and behavioral studies of female sex appeal in Drosophila. Behavior Genetics, 9, 257–275. doi:10.1007/BF01068205
   PubMed Web of Science ®Google Scholar
• Kabra, M., Robie, A.A., Rivera-Alba, M., Branson, S., & Branson, K. (2013). JAABA: interactive machine learning for automatic annotation of animal behavior. Nature Methods, 10, 64. doi:10.1038/nmeth.2281
   PubMed Web of Science ®Google Scholar
• Kain, J., Stokes, C., Gaudry, Q., Song, X., Foley, J., Wilson, R., & de Bivort, B. (2013). Leg-tracking and automated behavioural classification in Drosophila. Nature Communications, 4, 1910. doi:10.1038/ncomms2908
   PubMed Web of Science ®Google Scholar
• Kitamoto, T. (2001). Conditional modification of behavior in Drosophila by targeted expression of a temperature-sensitive shibire allele in defined neurons. J Neurobiol, 47, 81–92. doi:10.1002/neu.1018
   PubMed Web of Science ®Google Scholar
• Koganezawa, M., Kimura, K., & Yamamoto, D. (2016). The neural circuitry that functions as a switch for courtship versus aggression in Drosophila males. Current Biology, 26, 1395–1403. doi:10.1016/j.cub.2016.04.017
   PubMed Web of Science ®Google Scholar
• Kohatsu, S., & Yamamoto, D. (2015). Visually induced initiation of Drosophila innate courtship-like following pursuit is mediated by central excitatory state. Nature Communications, 6, 6457. doi:10.1038/ncomms7457
   PubMed Web of Science ®Google Scholar
• Kohl, J., Ostrovsky, Aaron, D., Frechter, S., & Jefferis, G.S.X.E. (2013). A bidirectional circuit switch reroutes pheromone signals in male and female brains. Cell, 155, 1610–1623. doi:10.1016/j.cell.2013.11.025
   PubMed Web of Science ®Google Scholar
• Krstic, D., Boll, W., & Noll, M. (2009). Sensory integration regulating male courtship behavior in Drosophila. PLoS One, 4, e4457. doi:10.1371/journal.pone.0004457
   PubMed Web of Science ®Google Scholar
• Lihoreau, M., Clarke, I.M., Buhl, J., Sumpter, D.J.T., & Simpson, S.J. (2016). Collective selection of food patches in Drosophila. The Journal of Experimental Biology, 219, 668–675. doi:10.1242/jeb.127431
   PubMed Web of Science ®Google Scholar
• Lin, H.-H., Cao, D.-S., Sethi, S., Zeng, Z., Chin, J.S.R., Chakraborty, T.S., … Wang, J.W. (2016). Hormonal modulation of pheromone detection enhances male courtship success. Neuron, 90, 1272–1285. doi:10.1016/j.neuron.2016.05.004
   PubMed Web of Science ®Google Scholar
• Liu, C., Plaçais, P.-Y., Yamagata, N., Pfeiffer, B.D., Aso, Y., Friedrich, A.B., … Tanimoto, H. (2012). A subset of dopamine neurons signals reward for odour memory in Drosophila. Nature, 488, 512–516. doi:10.1038/nature11304
   PubMed Web of Science ®Google Scholar
• McRobert, S.P., & Tompkins, L. (1983). Courtship of young males is ubiquitous in Drosophila melanogaster. Behavior Genetics, 13, 517–523. doi:10.1007/BF01065927
   PubMed Web of Science ®Google Scholar
• Owald, D., Felsenberg, J., Talbot, C.B., 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
   PubMed Web of Science ®Google Scholar
• Perisse, E., Burke, C., Huetteroth, W., & Waddell, S. (2013). Shocking revelations and saccharin sweetness in the study of Drosophila olfactory memory. Current Biology, 23, R752–R763. doi:10.1016/j.cub.2013.07.060
   PubMed Web of Science ®Google Scholar
• Pfeiffer, B.D., Truman, J.W., & Rubin, G.M. (2012). Using translational enhancers to increase transgene expression in Drosophila. Proceedings of the National Academy of Sciences of the United States of America, 109, 6626–6631. doi:10.1073/pnas.1204520109
   PubMed Web of Science ®Google Scholar
• Qiao, B., Li, C., Allen, V.W., Shirasu-Hiza, M., & Syed, S. (2018). Automated analysis of long-term grooming behavior in Drosophila using a k-nearest neighbors classifier. eLIFE, 7, e34497. doi:10.7554/eLife.34497 doi:10.7554/eLife.34497
   PubMed Web of Science ®Google Scholar
• Ramdya, P., Lichocki, P., Cruchet, S., Frisch, L., Tse, W., Floreano, D., & Benton, R. (2015). Mechanosensory interactions drive collective behaviour in Drosophila. Nature, 519, 233–236. doi:10.1038/nature14024
   PubMed Web of Science ®Google Scholar
• Ruta, V., Datta, S.R., Vasconcelos, M.L., Freeland, J., Looger, L.L., & Axel, R. (2010). A dimorphic pheromone circuit in Drosophila from sensory input to descending output. Nature, 468, 686. doi:10.1038/nature09554
   PubMed Web of Science ®Google Scholar
• Sayin, S., De Backer, J.F., Wosniack, M.E., Lewis, L., Siju, K.P., Frisch, L.M., … Grunwald Kadow, I. (2018). Specific octopaminergic neurons arbitrate between perseverance and reward in hungry. bioRxiv. Feb. 2, 1–102. doi:10.1101/259119
   Google Scholar
• Schleyer, M., Reid, S.F., Pamir, E., Saumweber, T., Paisios, E., Davies, A., … Louis, M. (2015). The impact of odor-reward memory on chemotaxis in larval Drosophila. Learn Mem, 22, 267–277. doi:10.1101/lm.037978.114
   PubMed Web of Science ®Google Scholar
• Spieth, H.T. (1974). Courtship behavior in Drosophila. Annual Review of Entomology, 19, 385–405. doi:10.1146/annurev.en.19.010174.002125
   PubMed Web of Science ®Google Scholar
• Thum, A.S., Jenett, A., Ito, K., Heisenberg, M., & Tanimoto, H. (2007). Multiple memory traces for olfactory reward learning in Drosophila. The Journal of Neuroscience, 27, 11132–11138. doi:10.1523/JNEUROSCI.2712-07.2007
   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
• Tully, T., & Quinn, W.G. (1985). Classical conditioning and retention in normal and mutant Drosophila melanogaster. Journal of Comparative Physiology A, 157, 263–277. doi:10.1007/BF01350033
   PubMed Web of Science ®Google Scholar
• van Breugel, F., & Dickinson, M.H. (2014). Plume-tracking behavior of flying Drosophila emerges from a set of distinct sensory-motor reflexes. Current Biology, 24, 274–286. 01582-0.pdf doi:10.1016/j.cub.2013.12.023
   PubMed Web of Science ®Google Scholar
• van der Goes van Naters, W., & Carlson, J.R. (2007). Receptors and neurons for fly odors in Drosophila. Current Biology, 17, 606–612. doi:10.1016/j.cub.2007.02.043
   PubMed Web of Science ®Google Scholar
• von Reyn, C.R., Nern, A., Williamson, W.R., Breads, P., Wu, M., Namiki, S., & Card, G.M. (2017). Feature integration drives probabilistic behavior in the Drosophila escape response. Neuron, 94, 1190–1204. e1196. doi:10.1016/j.neuron.2017.05.036
   PubMed Web of Science ®Google Scholar
• Wohr, M., Borta, A., & Schwarting, R.K. (2005). Overt behavior and ultrasonic vocalization in a fear conditioning paradigm: a dose-response study in the rat. Neurobiology of Learning and Memory, 84, 228–240. doi:10.1016/j.nlm.2005.07.004
   PubMed Web of Science ®Google Scholar
• Yamagata, N., Hiroi, M., Kondo, S., Abe, A., & Tanimoto, H. (2016). Suppression of dopamine neurons mediates reward. PLoS Biology, 14, e1002586. doi:10.1371/journal.pbio.1002586
   PubMed Web of Science ®Google Scholar
• Yamagata, N., Ichinose, T., Aso, Y., Plaçais, 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
• Yamamoto, D., & Koganezawa, M. (2013). Genes and circuits of courtship behaviour in Drosophila males. Nature Review of Neuroscience, 14, 681–692. doi:10.1038/nrn3567
   PubMed Web of Science ®Google Scholar
• Yamashita, T., Haupt, S.S., Ikeno, H., & Ai, H. (2016). Walking patterns induced by learned odors in the honeybee, Apis mellifera L. The Journal of Experimental Biology, 219, 12–16. doi:10.1242/jeb.123356
   PubMed Web of Science ®Google Scholar
• Yu, D., Ponomarev, A., & Davis, R.L. (2004). Altered representation of the spatial code for odors after olfactory classical conditioning; memory trace formation by synaptic recruitment. Neuron, 42, 437–449. doi:10.1016/S0896-6273(04)00217-X
   PubMed Web of Science ®Google Scholar
• Yu, J.Y., Kanai, M.I., Demir, E., Jefferis, G.S.X.E., & Dickson, B.J. (2010). Cellular organization of the neural circuit that drives Drosophila courtship behavior. Current Biology, 20, 1602–1614. doi:10.1016/j.cub.2010.08.025
   PubMed Web of Science ®Google Scholar
• Ziegler, A.B., Berthelot-Grosjean, M., & Grosjean, Y. (2013). The smell of love in Drosophila. Frontiers in Physiology, 4, 72. doi:10.3389/fphys.2013.00072
   PubMed Web of Science ®Google Scholar