Capacity of Visual Classical Conditioning in Drosophila Larvae

Behavioral Neuroscience

Volumn 125, Issue 6, 2011, Pages 921-929

  von Essen, Alina M H J ^a   Pauls, Dennis ^b   Thum, Andreas S ^a   Sprecher, Simon G ^a  

^a UNIVERSITY OF FRIBOURG   (Switzerland)

^b PHILIPPS UNIVERSITY MARBURG   (Germany)

Author keywords

Classical conditioning; Drosophila; Larval behavior; Visual learning

Indexed keywords

ANIMAL EXPERIMENT; ARTHROPOD LARVA; ARTICLE; ASSOCIATION; CONDITIONED REFLEX; CONTROLLED STUDY; DROSOPHILA; ELECTRIC SHOCK; LIGHT DARK CYCLE; MEMORY; NONHUMAN; STIMULUS RESPONSE; TASTE; VISION;

ANIMALS; CONDITIONING, CLASSICAL; DROSOPHILA MELANOGASTER; LARVA; LEARNING; NERVE NET; PHOTIC STIMULATION; TASTE PERCEPTION; VISUAL PERCEPTION;

EID: 83055179986     PISSN: 07357044     EISSN: 19390084     Source Type: Journal    
DOI: 10.1037/a0025758     Document Type: Article

References (42)

1. Aceves-Pina E.O., Quinn W.G. Learning in normal and mutant Drosophila larvae. Science 1979, October 5, 206:93-96. doi: 10.1126/science.206.4414.93.
2. Ashburner M. Drosophila. A laboratory handbook 1989, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
3. Ashe K.H., Zahs K.R. Probing the biology of Alzheimer's disease in mice. Neuron 2010, 66:631-645. doi: 10.1016/j.neuron.2010.04.031.
4. Bellmann D., Richardt A., Freyberger R., Nuwal N., Schwarzel M., Fiala A., Stortkuhl K.F. Optogenetically induced olfactory stimulation in drosophila larvae reveals the neuronal basis of odor-aversion behavior. Frontiers in Behavioral Neuroscience 2010, 4:27. doi: 10.3389/fnbeh.2010.00027.
5. Fiala A. Olfaction and olfactory learning in Drosophila: Recent progress. Current Opinion in Neurobiology 2007, 17:720-726. doi: 10.1016/j.conb.2007.11.009.
6. Gerber B., Hendel T. Outcome expectations drive learned behaviour in larval Drosophila. Proceedings. Biological Sciences/The Royal Society 2006, 273:2965-2968. doi: 10.1098/rspb.2006.3673.
7. Gerber B., Scherer S., Neuser K., Michels B., Hendel T., Stocker R.F., Heisenberg M. Visual learning in individually assayed Drosophila larvae. Journal of Experimental Biology 2004, 207:179-188. doi: 10.1242/jeb.00718.
8. Gerber B., Stocker R.F. The Drosophila larva as a model for studying chemosensation and chemosensory learning: A review. Chemical Senses 2007, 32:65-89. doi: 10.1093/chemse/bjl030.
9. Gerber B., Stocker R.F., Tanimura T., Thum A.S. Smelling, tasting, learning: Drosophila as a study case. Results and Problems in Cell Differentiation 2009, 47:139-185. doi: 10.1007/400_2008_9.
10. Hassan J., Iyengar B., Scantlebury N., Moncalvo V.R., Campos R. Photic input pathways that mediate the Drosophila larval response to light and circadian rhythmicity are developmentally related but functionally distinct. Journal of Comparative Neurology 2005, 481:266-275. doi: 10.1002/cne.20383.
11. Heisenberg M. Mushroom body memoir: From maps to models. Nature Reviews Neuroscience 2003, 4:266-275. doi: 10.1038/nrn1074.
12. Heisenberg M., Borst A., Wagner S., Byers D. Drosophila mushroom body mutants are deficient in olfactory learning. Journal of Neurogenetics 1985, 2:1-30. doi: 10.3109/01677068509100140.
13. Hendel T., Michels B., Neuser K., Schipanski A., Kaun K., Sokolowski M.B., Gerber B. The carrot, not the stick: Appetitive rather than aversive gustatory stimuli support associative olfactory learning in individually assayed Drosophila larvae. Journal of Comparative Physiology. A, Sensory, Neural, and Behavioral Physiology 2005, 191:265-279. doi: 10.1007/s00359-004-0574-8.
14. Hirth F. Drosophila melanogaster in the study of human neurodegeneration. CNS & Neurological Disorders Drug Targets 2010, 9:504-523.
15. Honjo K., Furukubo-Tokunaga K. Distinctive neuronal networks and biochemical pathways for appetitive and aversive memory in Drosophila larvae. Journal of Neuroscience 2009, 29:852-862. doi: 10.1523/JNEUROSCI.1315-08.2009.
16. Hwang R.Y., Zhong L., Xu Y., Johnson T., Zhang F., Deisseroth K., Tracey W.D. Nociceptive neurons protect Drosophila larvae from parasitoid wasps. Current Biology 2007, 17:2105-2116. doi: 10.1016/j.cub.2007.11.029.
17. Kaun K.R., Hendel T., Gerber B., Sokolowski M.B. Natural variation in Drosophila larval reward learning and memory due to a cGMP-dependent protein kinase. Learning & Memory 2007, 14:342-349. doi: 10.1101/lm.505807.
18. Keene A.C., Mazzoni E.O., Zhen J., Younger M.A., Yamaguchi S., Blau J., Sprecher S. Distinct visual pathways mediate Drosophila larval light avoidance and circadian clock entrainment. Journal of Neuroscience 2011, 31:6527-6534.
19. Keene A.C., Waddell S. Drosophila olfactory memory: Single genes to complex neural circuits. Nature Reviews Neuroscience 2007, 8:341-354. doi: 10.1038/nrn2098.
20. Khurana S., Abu Baker M.B., Siddiqi O. Odour avoidance learning in the larva of Drosophila melanogaster. Journal of Biosciences 2009, 34:621-631. doi: 10.1007/s12038-009-0080-9.
21. Knight D., Iliadi K., Charlton M.P., Atwood H.L., Boulianne G.L. Presynaptic plasticity and associative learning are impaired in a Drosophila presenilin null mutant. Developmental Neurobiology 2007, 67:1598-1613. doi: 10.1002/dneu.20532.
22. Liu G., Seiler H., Wen A., Zars T., Ito K., Wolf R., Liu L. Distinct memory traces for two visual features in the Drosophila brain. Nature 2006, February 2, 439:551-556. doi: 10.1038/nature04381.
23. Mazzoni E.O., Desplan C., Blau J. Circadian pacemaker neurons transmit and modulate visual information to control a rapid behavioral response. Neuron 2005, 45:293-300. doi: 10.1016/j.neuron.2004.12.038.
24. McGuire S.E., Deshazer M., Davis R.L. Thirty years of olfactory learning and memory research in Drosophila melanogaster. Progress in Neurobiology 2005, 76:328-347. doi: 10.1016/j.pneurobio.2005.09.003.
25. Nassif C., Noveen A., Hartenstein V. Early development of the Drosophila brain: III. The pattern of neuropile founder tracts during the larval period. Journal of Comparative Neurology 2003, 455:417-434. doi: 10.1002/cne.10482.
26. Niewalda T., Singhal N., Fiala A., Saumweber T., Wegener S., Gerber B. Salt processing in larval Drosophila: Choice, feeding, and learning shift from appetitive to aversive in a concentration-dependent way. Chemical Senses 2008, 33:685-692. doi: 10.1093/chemse/bjn037.
27. Pauls D., Pfitzenmaier J.E., Krebs-Wheaton R., Selcho M., Stocker R.F., Thum A.S. Electric shock-induced associative olfactory learning in Drosophila larvae. Chemical Senses 2010, 35:335-346. doi: 10.1093/chemse/bjq023.
28. Pauls D., Selcho M., Gendre N., Stocker R.F., Thum A.S. Drosophila larvae establish appetitive olfactory memories via mushroom body neurons of embryonic origin. Journal of Neuroscience 2010, 30:10655-10666. doi: 10.1523/JNEUROSCI.1281-10.2010.
29. Renn S.C., Armstrong J.D., Yang M., Wang Z., An X., Kaiser K., Taghert P.H. Genetic analysis of the Drosophila ellipsoid body neuropil: Organization and development of the central complex. Journal of Neurobiology 1999, 41:189-207. doi: 10.1002/(SICI)1097-4695(19991105)41:2<189::AID-NEU3>3.0.CO;2-Q.
30. Saumweber T., Husse J., Gerber B. Innate attractiveness and associative learnability of odors can be dissociated in larval Drosophila. Chemical Senses 2011, 36:223-235. doi: 10.1093/chemse/bjq128.
31. Sawin-McCormack E.P., Sokolowski M.B., Campos A.R. Characterization and genetic analysis of Drosophila melanogaster photobehavior during larval development. Journal of Neurogenetics 1995, 10:119-135. doi: 10.3109/01677069509083459.
32. Schroll C., Riemensperger T., Bucher D., Ehmer J., Voller T., Erbguth K., Fiala A. Light-induced activation of distinct modulatory neurons triggers appetitive or aversive learning in Drosophila larvae. Current Biology 2006, 16:1741-1747. doi: 10.1016/j.cub.2006.07.023.
33. Selcho M., Pauls D., Han K.A., Stocker R.F., Thum A.S. The role of dopamine in Drosophila larval classical olfactory conditioning. PLoS One 2009, 4:e5897. doi: 10.1371/journal.pone.0005897.
34. Sprecher S.G., Desplan C. Switch of rhodopsin expression in terminally differentiated Drosophila sensory neurons. Nature 2008, 454:533-537. doi: 10.1038/nature07062.
35. Sprecher S.G., Reichert H., Hartenstein V. Gene expression patterns in primary neuronal clusters of the Drosophila embryonic brain. Gene Expression Patterns 2007, 7:584-595. doi: 10.1016/j.modgep.2007.01.004.
36. Sprecher S.G., Cardona A., Hartenstein V. The Drosophila larval visual system: High-resolution analysis of a simple visual neuropil. Developmental Biology 2011, 358:33-43. doi: 10.1016/j.ydbio.2011.07.006.
37. Tully T., Cambiazo V., Kruse L. Memory through metamorphosis in normal and mutant Drosophila. Journal of Neuroscience 1994, 14:68-74.
38. Varnam C.J., Strauss R., Belle J.S., Sokolowski M.B. Larval behavior of Drosophila central complex mutants: Interactions between no bridge, foraging, and Chaser. Journal of Neurogenetics 1996, 11:99-115. doi: 10.3109/01677069609107065.
39. Xia W. Exploring Alzheimer's disease in zebrafish. Journal of Alzheimer's Disease 2010, 20:981-990.
40. Xiang Y., Yuan Q., Vogt N., Looger L.L., Jan L.Y., Jan Y.N. Light-avoidance-mediating photoreceptors tile the Drosophila larval body wall. Nature 2010, December 16, 468:921-926. doi: 10.1038/nature09576.
41. Yarali A., Hendel T., Gerber B. Olfactory learning and behaviour are 'insulated' against visual processing in larval Drosophila. Journal of Comparative Physiology. A, Sensory, Neural, and Behavioral Physiology 2006, 192:1133-1145. doi: 10.1007/s00359-006-0140-7.
42. Younossi-Hartenstein A., Nguyen B., Shy D., Hartenstein V. Embryonic origin of the Drosophila brain neuropile. Journal of Comparative Neurology 2006, 497:981-998. doi: 10.1002/cne.20884.