Light-Induced Activation of Distinct Modulatory Neurons Triggers Appetitive or Aversive Learning in Drosophila Larvae

Current Biology

Volumn 16, Issue 17, 2006, Pages 1741-1747

  Schroll, Christian ^a   Riemensperger, Thomas ^a   Bucher, Daniel ^a   Ehmer, Julia ^a   Völler, Thomas ^a   Erbguth, Karen ^a   Gerber, Bertram ^a   Hendel, Thomas ^a   Nagel, Georg ^b   Buchner, Erich ^a   Fiala, André ^a  

^a UNIVERSITY OF WÜRZBURG   (Germany)

^b UNIVERSITY OF WÜRZBURG   (Germany)

Author keywords

SYSNEURO

Indexed keywords

ANIMALIA; HEXAPODA; INSECTA;

EID: 33749837676     PISSN: 09609822     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cub.2006.07.023     Document Type: Article

References (32)

1. Hammer M. An identified neuron mediates the unconditioned stimulus in associative olfactory learning in honeybees. Nature 366 (1993) 59-63
2. Hammer M., and Menzel R. Multiple sites of associative odor learning as revealed by local brain microinjections of octopamine in honeybees. Learn. Mem. 5 (1998) 146-156
3. Schwaerzel M., Monastirioti M., Scholz H., Friggi-Grelin F., Birman S., and Heisenberg M. Dopamine and octopamine differentiate between aversive and appetitive olfactory memories in Drosophila. J. Neurosci. 23 (2003) 10495-10502
4. Unoki S., Matsumoto Y., and Mizunami M. Participation of octopaminergic reward system and dopaminergic punishment system in insect olfactory learning revealed by pharmacological study. Eur. J. Neurosci. 22 (2005) 1409-1416
5. Nagel G., Szellas T., Huhn W., Kateriya S., Adeishvili N., Berthold P., Ollig D., Hegemann P., and Bamberg E. Channelrhodopsin-2, a directly light-gated cation-selective membrane channel. Proc. Natl. Acad. Sci. USA 100 (2003) 13940-13945
6. Brand A.H., and Perrimon N. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118 (1993) 401-415
7. Luo L., Liao Y.J., Jan L.Y., and Jan Y.N. Distinct morphogenetic functions of similar small GTPases: Drosophila Drac1 is involved in axonal outgrowth and myoblast fusion. Genes Dev. 8 (1994) 1787-1802
8. Parkes T.L., Elia A.J., Dickinson D., Hilliker A.J., Phillips J.P., and Boulianne G.L. Extension of Drosophila lifespan by overexpression of human SOD1 in motorneurons. Nat. Genet. 19 (1998) 171-174
9. Friggi-Grelin F., Coulom H., Meller M., Gomez D., Hirsh J., and Birman S. Targeted gene expression in Drosophila dopaminergic cells using regulatory sequences from tyrosine hydroxylase. J. Neurobiol. 54 (2003) 618-627
10. Cole S.H., Carney G.E., McClung C.A., Willard S.S., Taylor B.J., and Hirsh J. Two functional but noncomplementing Drosophila tyrosine decarboxylase genes: distinct roles for neural tyramine and octopamine in female fertility. J. Biol. Chem. 280 (2005) 14948-14955
11. Jan L.Y., and Jan Y.N. Properties of the larval neuromuscular junction in Drosophila melanogaster. J. Physiol. 262 (1976) 189-214
12. Fishilevich E., Domingos A.I., Asahina K., Naef F., Vosshall L.B., and Louis M. Chemotaxis behavior mediated by single larval olfactory neurons in Drosophila. Curr. Biol. 15 (2005) 2086-2096
13. Hendel T., Michels B., Neuser K., Schipanski A., Kaun K., Sokolowski M.B., Marohn F., Michel R., Heisenberg M., and Gerber B. The carrot, not the stick: appetitive rather than aversive gustatory stimuli support associative olfactory learning in individually assayed Drosophila larvae. J. Comp. Physiol. [A] 191 (2005) 265-279
14. Gerber B., and Hendel T. Outcome expectations drive learned behavior in larval Drosophila. Proc. Biol. Sci. (2006) in press
15. Brecht M., Schneider M., Sakmann B., and Margrie T.W. Whisker movements evoked by stimulation of single pyramidal cells in rat motor cortex. Nature 427 (2004) 704-710
16. Zemelman B.V., Nesnas N., Lee G.A., and Miesenböck G. Photochemical gating of heterologous ion channels: remote control over genetically designated populations of neurons. Proc. Natl. Acad. Sci. USA 100 (2003) 1352-1357
17. Banghart M., Borges K., Isacoff E., Trauner D., and Kramer R.H. Light-activated ion channels for remote control of neuronal firing. Nat. Neurosci. 7 (2004) 1381-1386
18. Lima S.Q., and Miesenböck G. Remote control of behavior through genetically targeted photostimulation of neurons. Cell 121 (2005) 141-152
19. Nagel G., Brauner M., Liewald J.F., Adeishvili N., Bamberg E., and Gottschalk A. Light activation of channelrhodopsin-2 in excitable cells of Caenorhabditis elegans triggers rapid behavioral responses. Curr. Biol. 15 (2005) 2279-2284
20. Boyden E.S., Zhang F., Bamberg E., Nagel G., and Deisseroth K. Millisecond-timescale, genetically targeted optical control of neural activity. Nat. Neurosci. 8 (2005) 1263-1268
21. Bi A., Cui J., Ma Y.P., Olshevskaya E., Pu M., Dizhoor A.M., and Pan Z.H. Ectopic expression of a microbial-type rhodopsin restores visual responses in mice with photoreceptor degeneration. Neuron 50 (2006) 23-33
22. Kreher S.A., Kwon J.Y., and Carlson J.R. The molecular basis of odor coding in the Drosophila larva. Neuron 46 (2005) 445-456
23. Ramaekers A., Magnenat E., Marin E.C., Gendre N., Jefferis G.S., Luo L., and Stocker R.F. Glomerular maps without cellular redundancy at successive levels of the Drosophila larval olfactory circuit. Curr. Biol. 15 (2005) 982-992
24. Scherer S., Stocker R.F., and Gerber B. Olfactory learning in individually assayed Drosophila larvae. Learn. Mem. 10 (2003) 217-225
25. Honjo K., and Furukubo-Tokunaga K. Induction of cAMP response element-binding protein-dependent medium-term memory by appetitive gustatory reinforcement in Drosophila larvae. J. Neurosci. 25 (2005) 7905-7913
26. Mirenowicz J., and Schultz W. Preferential activation of midbrain dopamine neurons by appetitive rather than aversive stimuli. Nature 379 (1996) 449-451
27. Daw N.D., Kakade S., and Dayan P. Opponent interactions between serotonin and dopamine. Neural Netw. 15 (2002) 603-616
28. Riemensperger T., Völler T., Stock P., Buchner E., and Fiala A. Punishment prediction by dopaminergic neurons in Drosophila. Curr. Biol. 5 (2005) 1953-1960
29. Kreissl S., Eichmüller S., Bicker G., Rapus J., and Eckert M. Octopamine-like immunoreactivity in the brain and subesophageal ganglion of the honeybee. J. Comp. Neurol. 348 (1994) 583-595
30. Sinakevitch I., Niwa M., and Strausfeld N.J. Octopamine-like immunoreactivity in the honey bee and cockroach: comparable organization in the brain and subesophageal ganglion. J. Comp. Neurol. 488 (2005) 233-254
31. Sinakevitch I., and Strausfeld N.J. Comparison of octopamine-like immunoreactivity in the brains of the fruit fly and blow fly. J. Comp. Neurol. 494 (2006) 460-475
32. Stewart B.A., Atwood H.L., Renger J.J., Wang J., and Wu C.F. Improved stability of Drosophila larval neuromuscular preparations in haemolymph-like physiological solutions. J. Comp. Physiol. [A] 175 (1994) 179-191