Associative learning between odorants and mechanosensory punishment in larval Drosophila

Journal of Experimental Biology

Volumn 214, Issue 23, 2011, Pages 3897-3905

  Eschbach, Claire ^a   Cano, Carmen ^a   Haberkern, Hannah ^a   Schraut, Karla ^a   Guan, Chonglin ^a   Triphan, Tilman ^a,e   Gerber, Bertram ^a,b,c,d  

^a UNIVERSITY OF WÜRZBURG   (Germany)

^b UNIVERSITY OF LEIPZIG   (Germany)

^c LEIBNIZ INSTITUTE FOR NEUROBIOLOGY   (Germany)

^d OTTO VON GUERICKE UNIVERSITY   (Germany)

^e HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

Drosophila; Learning; Mechanosensation; Memory; Olfaction; Punishment

Indexed keywords

ANIMAL; ANIMAL BEHAVIOR; ARTICLE; CONDITIONING; DROSOPHILA MELANOGASTER; LARVA; LEARNING; MECHANOTRANSDUCTION; MEMORY; ODOR; PHYSIOLOGY; PUNISHMENT; SOUND;

ANIMALS; ASSOCIATION LEARNING; BEHAVIOR, ANIMAL; CONDITIONING (PSYCHOLOGY); DROSOPHILA MELANOGASTER; LARVA; MECHANOTRANSDUCTION, CELLULAR; MEMORY; ODORS; PUNISHMENT; SOUND;

ANIMALIA;

EID: 82055170507     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.060533     Document Type: Article

References (42)

1. Aceves-Piña, E. O. and Quinn, W. G. (1979). Learning in normal and mutant Drosophila larvae. Science 206, 93-96.
2. Akalal, D. B., Yu, D. and Davis, R. L. (2010). A late-phase, long-term memory trace forms in the y neurons of Drosophila mushroom bodies after olfactory classical conditioning. J. Neurosci. 30, 16699-16708.
3. Cardona, A., Larsen, C. and Hartenstein, V. (2009). Neuronal fiber tracts connecting the brain and ventral nerve cord of the early Drosophila larva. J. Comp. Neurol. 515, 427-440.
4. Diegelmann, S., Bate, M. and Landgraf, M. (2008). Gateway cloning vectors for the LexA-based binary expression system in Drosophila. Fly (Austin) 2, 236-239.
5. Djemai, I., Casas, J. and Magal, C. (2001). Matching host reactions to parasitoid wasp vibrations. Proc. Biol. Sci. 268, 2403-2408.
6. Dorn, S., Wäckers, F., Casas, J. and Bacher, S. (1997). Substrate vibrations elicit defensive behaviour in leafminer pupae. J. Insect Physiol. 43, 945-952.
7. Gerber, B. and Hendel, T. (2006). Outcome expectations drive learned behaviour in larval Drosophila. Proc. Biol. Sci. 273, 2965-2968.
8. Gerber, B. and Stocker, R. F. (2007). The Drosophila larva as a model for studying chemosensation and chemosensory learning: a review. Chem. Senses 32, 65-89.
9. Gerber, B., Scherer, S., Neuser, K., Michels, B., Hendel, T., Stocker, R. F. and Heisenberg, M. (2004). Visual learning in individually assayed Drosophila larvae. J. Exp. Biol. 207, 179-188.
10. Gerber, B., Stocker, R. F., Tanimura, T. and Thum, A. S. (2009). Smelling, tasting learning: Drosophila as a study case. Results Probl. Cell. Differ. 47, 139-185.
11. Gervasi, N., Tchénio, P. and 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.
12. Giurfa, M. (2007). Behavioral and neural analysis of associative learning in the honeybee: a taste from the magic well. J. Comp. Physiol. A 193, 801-824.
13. Hallem, E. A., Dahanukar, A. and Carlson, J. R. (2006). Insect odor and taste receptors. Annu. Rev. Entomol. 51, 113-135.
14. Heisenberg, M. (2003). Mushroom body memoir: from maps to models. Nat. Rev. Neurosci. 4, 266-275.
15. Hwang, R. Y., Zhong, L., Xu, Y., Johnson, T., Zhang, F., Deisseroth, K. and Tracey, W. D. (2007). Nociceptive neurons protect Drosophila larvae from parasitoid wasps. Curr. Biol. 17, 2105-2116.
16. Jarman, A. P. (2002). Studies of mechanosensation using the fly. Hum. Mol. Genet. 11, 1215-1218.
17. Kaun, K. R., Hendel, T., Gerber, B. and Sokolowski, M. B. (2007). Natural variation in Drosophila larval reward learning and memory due to a cGMP-dependent protein kinase. Learn. Mem. 14, 342-349.
18. Keene, A. C. and Waddell, S. (2007). Drosophila olfactory memory: single genes to complex neural circuits. Nat. Rev. Neurosci. 8, 341-354.
19. Kernan, M. J. (2007). Mechanotransduction and auditory transduction in Drosophila. Pflugers Arch. 454, 703-720.
20. Kernan, M., Cowan, D. and Zuker, C. (1994). Genetic dissection of mechanosensory transduction: mechanoreception-defective mutations of Drosophila. Neuron 12, 1195-1206.
21. Lumpkin, E. A., Marshall, K. L. and Nelson, A. M. (2010). The cell biology of touch. J. Cell. Biol. 191, 237-248.
22. Menzel, R. (2001). Searching for the memory trace in a mini-brain, the honeybee. Learn. Mem 8, 53-62.
23. Michels, B., Diegelmann, S., Tanimoto, H., Schwenkert, I., Buchner, E. and Gerber, B. (2005). A role for Synapsin in associative learning: the Drosophila larva as a study case. Learn. Mem. 12, 224-231.
24. Michels, B., Chen, Y. C., Saumweber, T., Mishra, D., Tanimoto, H., Schmid, B., Engmann, O. and Gerber, B. (2011). Cellular site and molecular mode of synapsin action in associative learning. Learn. Mem. 18, 332-344.
25. Mizunami, M., Unoki, S., Mori, Y., Hirashima, D., Hatano, A. and Matsumoto, Y. (2009). Roles of octopaminergic and dopaminergic neurons in appetitive and aversive memory recall in an insect. BMC Biol. 4, 7-46.
26. Olsen, S. R. and Wilson, R. I. (2008). Cracking neural circuits in a tiny brain: new approaches for understanding the neural circuitry of Drosophila. Trends Neurosci. 31, 512-520.
27. Pauls, D., Pfitzenmaier, J. E., Krebs-Wheaton, R., Selcho, M., Stocker, R. F. and Thum, A. S. (2010a). Electric shock-induced associative olfactory learning in Drosophila larvae. Chem. Senses 35, 335-346.
28. Pauls, D., Selcho, M., Gendre, N., Stocker, R. F. and Thum, A. S. (2010b). Drosophila larvae establish appetitive olfactory memories via mushroom body neurons of embryonic origin. J. Neurosci. 30, 10655-10666.
29. Saumweber, T., Weyhersmüller, A., Hallermann, S., Diegelmann, S., Michels, B., Bucher, D., Funk, N., Reisch, D., Krohne, G., Wegener, S. et al. (2011). Behavioral and synaptic plasticity are impaired upon lack of the synaptic protein SAP47. J. Neurosci. 31, 3508-3518.
30. Scherer, S., Stocker, R. F. and Gerber, B. (2003). Olfactory learning in individually assayed Drosophila larvae. Learn. Mem. 10, 217-225.
31. Schleyer, M., Saumweber, T., Nahrendorf, W., Fischer, B., von Alpen, D., Pauls, D., Thum, A. and Gerber, B. (2011). A behavior-based circuit-model of how outcome expectations organize learned behavior in larval Drosophila. Learn. Mem. 18, 639-652.
32. Schnaitmann, C., Vogt, K., Triphan, T. and Tanimoto, H. (2010). Appetitive and aversive visual learning in freely moving Drosophila. Front. Behav. Neurosci. 9, 4-10.
33. Schroll, C., Riemensperger, T., Bucher, D., Ehmer, J., Völler, T., Erbguth, K., Gerber, B., Hendel, T., Nagel, G., Buchner, E. et al. (2006). Light-induced activation of distinct modulatory neurons triggers appetitive or aversive learning in Drosophila larvae. Curr. Biol. 16, 1741-1747.
34. Schwärzel, M. and Müller U. (2006). Dynamic memory networks: dissecting molecular mechanisms underlying associative memory in the temporal domain. Cell. Mol. Life Sci. 63, 989-998.
35. Scott, K. (2005). Taste recognition: food for thought. Neuron 48, 455-464.
36. Selcho, M., Pauls, D., Han, K. A., Stocker, R. F. and Thum, A. S. (2009). The role of dopamine in Drosophila larval classical olfactory conditioning. PLoS One 4, e5897.
37. Smith, S. A. and Shepherd, D. (1996). Central afferent projections of proprioceptive sensory neurons in Drosophila revealed with the enhancer-trap technique. J. Comp. Neurol. 364, 311-323.
38. Tracey, W. D., Jr, Wilson, R. I., Laurent, G. and Benzer, S. (2003). painless, a Drosophila gene essential for nociception. Cell 113, 261-273.
39. Vosshall, L. B. and Stocker, R. F. (2007). Molecular architecture of smell and taste in Drosophila. Ann. Rev. Neurosci. 30, 505-533.
40. Wu, Z., Sweeney, L. B., Ayoob, J. C., Chak, K., Andreone, B. J., Ohyama, T., Kerr, R., Luo, L., Zlatic, M. and Kolodkin, A. L. (2011). A combinatorial semaphorin code instructs the initial steps of sensory circuit assembly in the Drosophila CNS. Neuron 70, 281-298.
41. Yin, J. and Kuebler, W. M. (2010). Mechanotransduction by TRP channels: general concepts and specific role in the vasculature. Cell. Biochem. Biophys. 56, 1-18.
42. Zeng, X., Sun, M., Liu, L., Chen, F., Wei, L. and Xie, W. (2007). Neurexin-1 is required for synapse formation and larvae associative learning in Drosophila. FEBS Lett 581, 2509-2516.