Dopamine and Octopamine Differentiate between Aversive and Appetitive Olfactory Memories in Drosophila

Journal of Neuroscience

Volumn 23, Issue 33, 2003, Pages 10495-10502

  Schwaerzel, Martin ^a,d   Monastirioti, Maria ^b   Scholz, Henrike ^a   Friggi Grelin, Florence ^c   Birman, Serge ^c   Heisenberg, Martin ^a  

^a Biozentrum   (Germany)

^b INSTITUTE OF MOLECULAR BIOLOGY AND BIOTECHNOLOGY   (Greece)

^c AIX MARSEILLE UNIVERSITÉ   (France)

^d UNIVERSITY OF MISSOURI   (United States)

Author keywords

Dopamine; Drosophila; Learning and memory; Memory trace; Octopamine; Reinforcement; Synaptic plasticity

Indexed keywords

CATECHOLAMINE; DOPAMINE; OCTOPAMINE;

ANIMAL EXPERIMENT; APPETITE; ARTICLE; AVERSIVE BEHAVIOR; CELL POPULATION; CONDITIONING; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; FLY; MEMORY; MOTIVATION; MUSHROOM BODY; NERVE CELL; NERVE CELL PLASTICITY; NONHUMAN; OLFACTORY DISCRIMINATION; OLFACTORY SYSTEM; PRIORITY JOURNAL; REINFORCEMENT;

EID: 0344442689     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.23-33-10495.2003     Document Type: Article

References (46)

1. Antonov I, Antonova I, Kandel ER, Hawkins RD (2003) Activity-dependent presynaptic facilitation and Hebbian LTP are both required and interact during classical conditioning in Aplysia. Neuron 37:135-147.
2. Barron AB, Schulz DJ, Robinson GE (2002) Octopamine modulates responsiveness to foraging-related stimuli in honeybees (Apis mellifera). J Comp Physiol A Neuroethol Sens Neural Behav Physiol 188:603-610.
3. Connolly JB, Roberts IJ, Armstrong JD, Kaiser K, Forte M, Tully T, O'Kane CJ (1996) Associative learning disrupted by impaired Gs signaling in Drosophila mushroom bodies. Science 274:2104-107.
4. Crittenden JR, Skoulakis EM, Han KA, Kalderon D, Davis RL (1998) Tripartite mushroom body architecture revealed by antigenic markers. Learn Mem 5:38-51.
5. de Belle JS, Heisenberg M (1994) Associative odor learning in Drosophila abolished by chemical ablation of mushroom bodies. Science 263:692-695.
6. Dubnau J, Grady L, Kitamoto T, Tully T (2001) Disruption of neurotransmission in Drosophila mushroom body blocks retrieval but not acquisition of memory. Nature 411:476-480.
7. Dudai Y, Corfas G, Hazvi S (1988) What is the possible contribution of Ca2+-stimulated adenylate cyclase to acquisition, consolidation and retention of an associative olfactory memory in Drosophila. J Comp Physiol [A] 162:101-109.
8. Feany MB, Quinn WG (1995) A neuropeptide gene defined by the Drosophila memory mutant amnesiac. Science 268:869-873.
9. Friggi-Grelin F, Coulom H, Meller M, Gomez D, Hirsh J, Birman S (2003) Targeted gene expression in Drosophila dopaminergic cells using regulatory sequences from tyrosine hydroxylase. J Neurobiol 54:618-627.
10. Guo A, Li L, Xia SZ, Feng CH, Wolf R, Heisenberg M (1996) Conditioned visual flight orientation in Drosophila: dependence on age, practice, and diet. Learn Mem 3:49-59.
11. Hammer M, Menzel R (1998) Multiple sites of associative odor learning as revealed by local brain microinjections of octopamine in honeybees. Learn Mem 5:146-156.
12. Han K-A, Millar NS, Davis RL (1998) A novel octopamine receptor with preferential expression in Drosophila mushroom bodies. J Neurosci 18:3650-3658.
13. Han KA, Millar NS, Grotewiel MS, Davis RL (1996) DAMB, a novel dopamine receptor expressed specifically in Drosophila mushroom bodies. Neuron 16:1127-1135.
14. Heisenberg M (2003) Mushroom body memoir: from maps to models. Nat Rev Neurosci 4:266-275.
15. Heisenberg M, Borst A, Wagner S, Byers D (1985) Drosophila mushroom body mutants are deficient in olfactory learning. J Neurogenet 2:1-30.
16. Ito K, Sass H, Urban J, Hofbauer A, Schneuwly S (1997) GAL4-responsive UAS-tau as a tool for studying the anatomy and development of the Drosophila central nervous system. Cell Tissue Res 290:1-10.
17. Kandel ER (2001) The molecular biology of memory storage: a dialog between genes and synapses. Science 294:1030-1038.
18. Kim Y-C, Lee H-G, Seong C-S, Han K-A (2003) Expression of a DA1 dopamine receptor dDA1/DmDOP1 in the central nervous system of Drosophila melanogaster. Gene Expr Patterns 3:237-245.
19. 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.
20. Lechner HA, Byrne JH (1998) New perspectives on classical conditioning: a synthesis of Hebbian and non-Hebbian mechanisms. Neuron 20:355-358.
21. McBride SM, Giuliani G, Choi C, Krause P, Correale D, Watson K, Baker G, Siwicki KK (1999) Mushroom body ablation impairs short-term memory and long-term memory of courtship conditioning in Drosophila melanogaster. Neuron 24:967-977.
22. McGuire SE, Le PT, Davis RL (2001) The role of Drosophila mushroom body signaling in olfactory memory. Science 293:1330-1333.
23. Menzel R, Heyne A, Kinzel C, Gerber B, Fiala A (1999) Pharmacological dissociation between the reinforcing, sensitizing, and response-releasing functions of reward in honeybee classical conditioning. Behav Neurosci 113:744-754.
24. Mery F, Kawecki TJ (2002) Experimental evolution of learning ability in fruit flies. Proc Natl Acad Sci USA 99:14274-14279.
25. Mirenowicz J, Schultz W (1996) Preferential activation of midbrain dopamine neurons by appetitive rather than aversive stimuli. Nature 379:449-451.
26. Monastirioti M, Linn Jr CE, White K (1996) Characterization of Drosophila tyramine β-hydroxylase gene and isolation of mutant flies lacking octopamine. J Neurosci 16:3900-3911.
27. Nagaya Y, Kutsukake M, Chigusa SI, Komatsu A (2002) A trace amine, tyramine, functions as a neuromodulator in Drosophila melanogaster. Neurosci Lett 329:324-328.
28. Pankiw T, Page Jr RE (2003) Effect of pheromones, hormones, and handling on sucrose response thresholds of honey bees (Apis mellifera L.). J Comp Physiol [A] 189:675-684.
29. Rein K, Zöckler M, Mader MT, Grubel C, Heisenberg M (2002) The Drosophila standard brain. Curr Biol 12:227-231.
30. Roman G, Davis RL (2001) Molecular biology and anatomy of Drosophila olfactory associative learning. BioEssays 23:571-581.
31. Schulz DJ, Robinson GE (2001) Octopamine influences division of labor in honey bee colonies. J Comp Physiol [A] 187:53-61.
32. Schürmann FW (1987) The architecture of the mushroom bodies and related neuropils in the insect brain. In: Arthropods brains: its evolution, development, structure, and function (Gupta AP, ed), pp 231-264. New York: Wiley.
33. Schwaerzel M, Heisenberg M, Zars T (2002) Extinction antagonizes olfactory memory at the subcellular level. Neuron 35:951-960.
34. Tempel BL, Bonini N, Dawson DR, Quinn WG (1983) Reward learning in normal and mutant Drosophila. Proc Natl Acad Sci USA 80:1482-1486.
35. Tempel BL, Livingstone MS, Quinn WG (1984) Mutations in the dopa decarboxylase gene affect learning in Drosophila. Proc Natl Acad Sci USA 81:3577-3581.
36. Thummel CS, Pirrotta V (1992) Technical notes: new pCaSpeR P-element vectors. Drosophila Information Service 71:150.
37. Tully T (1986) Measuring learning in individual flies is not necessary to study the effects of single-gene mutations in Drosophila: a reply to Holliday and Hirsch. Behav Genet 16:449-455.
38. Tully T (1987) Drosophila learning and memory revisited. Trends Neurosci 10:330-335.
39. Tully T, Quinn WG (1985) Classical conditioning and retention in normal and mutant Drosophila melanogaster. J Comp Physiol [A] 157:263-277.
40. Villacres EC, Wong ST, Chavkin C, Storm RD (1998) Type I adenylyl cyclase mutant mice have impaired mossy fiber long-term potentiation. J Neurosci 18:3186-194.
41. Waddell S, Armstrong JD, Kitamoto T, Kaiser K, Quinn WG (2000) The amnesiac gene product is expressed in two neurons in the Drosophila brain that are critical for memory. Cell 103:805-813.
42. Yasuyama K, Meinertzhagen IA, Schürmann FW (2002) Synaptic organization of the mushroom body calyx in Drosophila melanogaster. J Comp Neurol 445:211-226.
43. Yin JC, Tully T (1996) CREB and the formation of long-term memory. Curr Opin Neurobiol 6:264-268.
44. Zars T, Wolf R, Davis RL, Heisenberg M (2000a) Tissue-specific expression of a type I adenylyl cyclase rescues the rutabaga mutant memory defect: In search of the engram. Learn Mem 7:18-31.
45. Zars T, Fischer M, Schulz R, Heisenberg M (2000b) Localization of a short-term memory in Drosophila. Science 288:672-675.
46. Zhong Y, Wu CF (1991) Altered synaptic plasticity in Drosophila memory mutants with a defective cyclic AMP cascade. Science 251:198-201.