Place memory formation in Drosophila is independent of proper octopamine signaling

Journal of Comparative Physiology A: Neuroethology, Sensory, Neural, and Behavioral Physiology

Volumn 196, Issue 4, 2010, Pages 299-305

  Sitaraman, Divya ^a   Zars, Melissa ^a   Zars, Troy ^a  

^a UNIVERSITY OF MISSOURI   (United States)

Author keywords

Drosophila; Learning; Memory; Octopamine; Tyramine

Indexed keywords

MIXED FUNCTION OXIDASE; OCTOPAMINE; TYRAMINE BETA HYDROXYLASE; TYRAMINE BETA-HYDROXYLASE;

ANIMAL; ANIMAL BEHAVIOR; ARTICLE; DROSOPHILA; GENETICS; LEARNING; MEMORY; MUTATION; OLFACTORY SYSTEM; PHYSIOLOGY; SYNAPTIC TRANSMISSION; TEMPERATURE;

ANIMALS; BEHAVIOR, ANIMAL; DROSOPHILA; LEARNING; MEMORY; MIXED FUNCTION OXYGENASES; MUTATION; OCTOPAMINE; OLFACTORY PATHWAYS; SYNAPTIC TRANSMISSION; TEMPERATURE;

EID: 77951710005     PISSN: 03407594     EISSN: 14321351     Source Type: Journal    
DOI: 10.1007/s00359-010-0517-5     Document Type: Article

References (56)

1. Armstrong GA, Shoemaker KL, Money TG, Robertson RM (2006) Octopamine mediates thermal preconditioning of the locust ventilatory central pattern generator via a cAMP/protein kinase A signaling pathway. J Neurosci 26: 12118-12126.
2. Blenau W, Baumann A (2001) Molecular and pharmacological properties of insect biogenic amine receptors: lessons from Drosophila melanogaster and Apis mellifera. Arch Insect Biochem Physiol 48: 13-38.
3. Brembs B, Christiansen F, Pfluger HJ, Duch C (2007) Flight initiation and maintenance deficits in flies with genetically altered biogenic amine levels. J Neurosci 27: 11122-11131.
4. Busch S, Selcho M, Ito K, Tanimoto H (2009) A map of octopaminergic neurons in the Drosophila brain. J Comp Neurol 513: 643-667.
5. Certel SJ, Savella MG, Schlegel DC, Kravitz EA (2007) Modulation of Drosophila male behavioral choice. Proc Natl Acad Sci USA 104: 4706-4711.
6. Chen CN, Denome S, Davis RL (1986) Molecular analysis of cDNA clones and the corresponding genomic coding sequences of the Drosophila dunce + gene, the structural gene for cAMP phosphodiesterase. Proc Natl Acad Sci USA 83: 9313-9517.
7. Claridge-Chang A, Roorda RD, Vrontou E, Sjulson L, Li H, Hirsh J, Miesenbock G (2009) Writing memories with light-addressable reinforcement circuitry. Cell 139: 405-415.
8. Cole SH, Carney GE, McClung CA, Willard SS, Taylor BJ, Hirsh J (2005) Two functional but noncomplementing Drosophila tyrosine decarboxylase genes: distinct roles for neural tyramine and octopamine in female fertility. J Biol Chem 280: 14948-14955.
9. Diegelmann S, Zars M, Zars T (2006) Genetic dissociation of acquisition and memory strength in the heat-box spatial learning paradigm in Drosophila. Learn Mem 13: 72-83.
10. Feany MB, Quinn WG (1995) A neuropeptide gene defined by the Drosophila memory mutant amnesiac. Science 268: 869-873.
11. Fox LE, Soll DR, Wu CF (2006) Coordination and modulation of locomotion pattern generators in Drosophila larvae: effects of altered biogenic amine levels by the tyramine beta hydroxlyase mutation. J Neurosci 26: 1486-1498.
12. Gervasi N, Tchenio P, 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.
13. Gioia A, Zars T (2009) Thermotolerance and place memory in adult Drosophila are independent of natural variation at the foraging locus. J Comp Physiol A 195: 777-782.
14. 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.
15. Hirsh J (1989) Molecular genetics of dopa decarboxylase and biogenic amines in Drosophila. Dev Genet 10: 232-238.
16. Hoyer SC, Eckart A, Herrel A, Zars T, Fischer SA, Hardie SL, Heisenberg M (2008) Octopamine in male aggression of Drosophila. Curr Biol 18: 159-167.
17. Kim H, Shimojo S, O'Doherty JP (2006) Is avoiding an aversive outcome rewarding? Neural substrates of avoidance learning in the human brain. PLoS Biol 4: e233.
18. Laferriere H, Guarnieri DJ, Sitaraman D, Diegelmann S, Heberlein U, Zars T (2008) Genetic dissociation of ethanol sensitivity and memory formation in Drosophila melanogaster. Genetics 178: 1895-1902.
19. Lebestky T, Chang JS, Dankert H, Zelnik L, Kim YC, Han KA, Wolf FW, Perona P, Anderson DJ (2009) Two different forms of arousal in Drosophila are oppositely regulated by the dopamine D1 receptor ortholog DopR via distinct neural circuits. Neuron 64: 522-536.
20. Lee T, Luo L (1999) Mosaic analysis with a repressible neurotechnique cell marker for studies of gene function in neuronal morphogenesis. Neuron 22: 451-461.
21. 2+/calmodulin-responsive adenylyl cyclase. Cell 68: 479-489.
22. Liu G, Seiler H, Wen A, Zars T, Ito K, Wolf R, Heisenberg M, Liu L (2006) Distinct memory traces for two visual features in the Drosophila brain. Nature 439: 551-556.
23. Martin JR, Ernst R, Heisenberg M (1999) Temporal pattern of locomotor activity in Drosophila melanogaster. J Comp Physiol [A] 184: 73-84.
24. 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.
25. Monastirioti M, Linn CE Jr, White K (1996) Characterization of Drosophila tyramine beta-hydroxylase gene and isolation of mutant flies lacking octopamine. J Neurosci 16: 3900-3911.
26. Putz G (2002) Characterization of memories and ignorant (S6KII) mutants in operant conditioning in the heat-box. Department of Genetics and Neurobiology, Wuerzburg, Julius Maximillians Universitaet Wuerzburg, p 115.
27. Putz G, Heisenberg M (2002) Memories in Drosophila heat-box learning. Learn Mem 9: 349-359.
28. Putz G, Bertolucci F, Raabe T, Zars T, Heisenberg M (2004) The S6KII (rsk) gene of Drosophila melanogaster differentially affects an operant and a classical learning task. J Neurosci 24: 9745-9751.
29. Rein K, Zockler M, Heisenberg M (1999) A quantitative three-dimensional model of the Drosophila optic lobes. Curr Biol 9: 93-96.
30. Riemensperger T, Voller T, Stock P, Buchner E, Fiala A (2005) Punishment prediction by dopaminergic neurons in Drosophila. Curr Biol 15: 1953-1960.
31. Rodriguez-Valentin R, Lopez-Gonzalez I, Jorquera R, Labarca P, Zurita M, Reynaud E (2006) Oviduct contraction in Drosophila is modulated by a neural network that is both octopaminergic and glutamatergic. J Cell Physiol 209: 183-198.
32. Saraswati S, Fox LE, Soll DR, Wu CF (2004) Tyramine and octopamine have opposite effects on the locomotion of Drosophila larvae. J Neurobiol 58: 425-441.
33. Sayeed O, Benzer S (1996) Behavioral genetics of thermosensation and hygrosensation in Drosophila. Proc Natl Acad Sci USA 93: 6079-6084.
34. Scholz H, Ramond J, Singh CM, Heberlein U (2000) Functional ethanol tolerance in Drosophila. Neuron 28: 261-271.
35. Schroll C, Riemensperger T, Bucher D, Ehmer J, Voller T, Erbguth K, Gerber B, Hendel T, Nagel G, Buchner E, Fiala A (2006) Light-induced activation of distinct modulatory neurons triggers appetitive or aversive learning in Drosophila larvae. Curr Biol 16: 1741-1747.
36. Schwaerzel M, Monastirioti M, Scholz H, Friggi-Grelin F, Birman S, Heisenberg M (2003) Dopamine and octopamine differentiate between aversive and appetitive olfactory memories in Drosophila. J Neurosci 23: 10495-10502.
37. Seymour B, O'Doherty JP, Koltzenburg M, Wiech K, Frackowiak R, Friston K, Dolan R (2005) Opponent appetitive-aversive neural processes underlie predictive learning of pain relief. Nat Neurosci 8: 1234-1240.
38. Sinakevitch I, Strausfeld NJ (2006) Comparison of octopamine-like immunoreactivity in the brains of the fruit fly and blow fly. J Comp Neurol 494: 460-475.
39. Sitaraman D, Zars M, Zars T (2007) Reinforcement pre-exposure enhances spatial memory formation in Drosophila. J Comp Physiol [A] 193: 903-908.
40. Sitaraman D, Zars M, Laferriere H, Chen YC, Sable-Smith A, Kitamoto T, Rottinghaus GE, Zars T (2008) Serotonin is necessary for place memory in Drosophila. Proc Natl Acad Sci USA 105: 5579-5584.
41. Sweeney ST, Broadie K, Keane J, Niemann H, O'Kane CJ (1995) Targeted expression of tetanus toxin light chain in Drosophila specifically eliminates synaptic transmission and causes behavioral defects. Neuron 14: 341-351.
42. 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.
43. Tomchik SM, Davis RL (2009) Dynamics of learning-related cAMP signaling and stimulus integration in the Drosophila olfactory pathway. Neuron 64: 510-521.
44. Tully T, Quinn WG (1985) Classical conditioning and retention in normal and mutant Drosophila melanogaster. J Comp Physiol [A] 157: 263-277.
45. Unoki S, Matsumoto Y, Mizunami M (2005) Participation of octopaminergic reward system and dopaminergic punishment system in insect olfactory learning revealed by pharmacological study. Eur J Neurosci 22: 1409-1416.
46. Unoki S, Matsumoto Y, Mizunami M (2006) Roles of octopaminergic and dopaminergic neurons in mediating reward and punishment signals in insect visual learning. Eur J Neurosci 24: 2031-2038.
47. Wustmann G, Heisenberg M (1997) Behavioral manipulation of retrieval in a spatial memory task for Drosophila melanogaster. Learn Mem 4: 328-336.
48. Wustmann G, Rein K, Wolf R, Heisenberg M (1996) A new paradigm for operant conditioning of Drosophila melanogaster. J Comp Physiol [A] 179: 429-436.
49. Zars T (2001) Two thermosensors in Drosophila have different behavioral functions. J Comp Physiol [A] 187: 235-242.
50. Zars T (2009) Spatial orientation in Drosophila. J Neurogenet 23: 104-110.
51. Zars T (2010a) Short-term memories in Drosophila are governed by general and specific genetic systems. Learn Mem (in press).
52. Zars T (2010b) Visualizing PKA activity in a learning center. Neuron 65: 442-444.
53. Zars M, Zars T (2006) High and low temperatures have unequal reinforcing properties in Drosophila spatial learning. J Comp Physiol [A] 192: 727-735.
54. Zars M, Zars T (2009) Rapid matching in Drosophila place learning. Naturwissenschaften 96: 927-931.
55. Zars T, Fischer M, Schulz R, Heisenberg M (2000a) Localization of a short-term memory in Drosophila. Science 288: 672-675.
56. Zars T, Wolf R, Davis R, Heisenberg M (2000b) 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.