Olfactory trace conditioning in Drosophila

Journal of Neuroscience

Volumn 31, Issue 20, 2011, Pages 7240-7248

  Galili, Dana Shani ^a   Lüdke, Alja ^b   Galizia, C Giovanni ^b   Szyszka, Paul ^b   Tanimoto, Hiromu ^a  

^a MAX PLANCK INSTITUTE OF NEUROBIOLOGY   (Germany)

^b UNIVERSITY OF KONSTANZ   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL BEHAVIOR; ARTICLE; CONDITIONING; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; NERVE CELL; NONHUMAN; ODOR; OLFACTORY DISCRIMINATION; OLFACTORY MEMORY; OLFACTORY RECEPTOR; OLFACTORY TRACE CONDITIONING; PRIORITY JOURNAL; SENSORY STIMULATION; STATE DEPENDENT LEARNING; STIMULUS RESPONSE; TASK PERFORMANCE;

ANIMALS; ASSOCIATION LEARNING; CONDITIONING, CLASSICAL; DROSOPHILA MELANOGASTER; ODORS; OLFACTORY RECEPTOR NEURONS; REACTION TIME; SMELL;

EID: 79956327027     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.6667-10.2011     Document Type: Article

References (59)

1. Bathellier B, Buhl DL, Accolla R, Carleton A (2008) Dynamic ensemble odor coding in the mammalian olfactory bulb: sensory information at different timescales. Neuron 57:586-598.
2. Bellmann D, Richardt A, Freyberger R, Nuwal N, Schwärzel M, Fiala A, Störtkuhl KF (2010) Optogenetically induced olfactory stimulation in Drosophila larvae reveals the neuronal basis of odor-aversion behavior. Front Behav Neurosci 4:27.
3. Beylin AV, Gandhi CC, Wood GE, Talk AC, Matzel LD, Shors TJ (2001) The role of the hippocampus in trace conditioning: temporal discontinuity or task difficulty? Neurobiol Learn Mem 76:447-461.
4. Bhandawat V, Olsen SR, Gouwens NW, Schlief ML, Wilson RI (2007) Sensory processing in the Drosophila antennal lobe increases reliability and separability of ensemble odor representations. Nat Neurosci 10:1474-1482.
5. Carter RM, Hofstotter C, Tsuchiya N, Koch C (2003) Working memory and fear conditioning. Proc Natl Acad Sci U S A 100:1399-1404.
6. Clark RE, Squire LR (1998) Classical conditioning and brain systems: the role of awareness. Science 280:77-81.
7. Clark RE, Manns JR, Squire LR (2002) Classical conditioning, awareness, and brain systems. Trends Cogn Sci 6:524-531.
8. Daly KC, Christensen TA, Lei H, Smith BH, Hildebrand JG (2004) Learning modulates the ensemble representations for odors in primary olfactory networks. Proc Natl Acad Sci U S A 101:10476-10481.
9. Davis RL (2005) Olfactory memory formation in Drosophila: from molecular to systems neuroscience. Annu Rev Neurosci 28:275-302.
10. Galán RF, Weidert M, Menzel R, Herz AV, Galizia CG (2006) Sensory memory for odors is encoded in spontaneous correlated activity between olfactory glomeruli. Neural Comput 18:10-25.
11. Galizia CG, Szyszka P (2008) Olfactory coding in the insect brain: molecular receptive ranges, spatial and temporal coding. Entomol Exp Appl 128: 81-92.
12. Galizia CG, Vetter R (2004) Optical methods for analyzing odor-evoked activity in the insect brain. In: Advances in insect sensory neuroscience (Christensen T, ed), pp 349-392. Boca Raton, FL: CRC.
13. Gerber B, Tanimoto H, Heisenberg M (2004) An engram found? Evaluating the evidence from fruit flies. Curr Opin Neurobiol 14:737-744.
14. Gervasi N, Tchénio 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.
15. Gil M, De Marco RJ, Menzel R (2007) Learning reward expectations in honeybees. Learn Mem 14:491-496.
16. Gil M, Menzel R, De Marco RJ (2008) Does an insect's unconditioned response to sucrose reveal expectations of reward? PLoS One 3:e2810.
17. Guerrieri F, Lachnit H, Gerber B, Giurfa M (2005) Olfactory blocking and odorant similarity in the honeybee. Learn Mem 12:86-95.
18. Hallem EA, Ho MG, Carlson JR (2004) The molecular basis of odor coding in the Drosophila antenna. Cell 117:965-979.
19. Ito I, Ong RC, Raman B, Stopfer M (2008) Sparse odor representation and olfactory learning. Nat Neurosci 11:1177-1184.
20. Jortner RA, Farivar SS, Laurent G (2007) A simple connectivity scheme for sparse coding in an olfactory system. J Neurosci 27:1659-1669.
21. Kehoe EJ, Ludvig EA, Sutton RS (2009) Magnitude and timing of conditioned responses in delay and trace classical conditioning of the nictitating membrane response of the rabbit (Oryctolagus cuniculus). Behav Neurosci 123:1095-1101.
22. LaBar KS, Disterhoft JF (1998) Conditioning, awareness, and the hippocampus. Hippocampus 8:620-626.
23. Larsson MC, Domingos AI, Jones WD, Chiappe ME, Amrein H, Vosshall LB (2004) Or83b encodes a broadly expressed odorant receptor essential for Drosophila olfaction. Neuron 43:703-714.
24. Masek P, Heisenberg M (2008) Distinct memories of odor intensity and quality in Drosophila. Proc Natl Acad Sci U S A 105:15985-15990.
25. Masse NY, Turner GC, Jefferis GS (2009) Olfactory information processing in Drosophila. Curr Biol 19:R700-R713.
26. Mazor O, Laurent G (2005) Transient dynamics versus fixed points in odor representations by locust antennal lobe projection neurons. Neuron 48:661-673.
27. McEchron MD, Bouwmeester H, Tseng W, Weiss C, Disterhoft JF (1998) Hippocampectomy disrupts auditory trace fear conditioning and contextual fear conditioning in the rat. Hippocampus 8:638-646.
28. Mishra D, Louis M, Gerber B (2010) Adaptive adjustment of the generalization-discrimination balance in larval Drosophila. J Neurogenet 24:168-175.
29. 2+ probe composed of a single green fluorescent protein. Nat Biotechnol 19:137-141.
30. Neuser K, Triphan T, Mronz M, Poeck B, Strauss R (2008) Analysis of a spatial orientation memory in Drosophila. Nature 453:1244-1247.
31. Olsen SR, Bhandawat V, Wilson RI (2007) Excitatory interactions between olfactory processing channels in the Drosophila antennal lobe. Neuron 54:89-103.
32. Pavlov I (1911) Lectures on conditioned reflexes. In: Transactions of the Society of Russian Physicians, Chap 27, pp 190-191. St. Petersburg: Society of Russian Physicians.
33. Pelz C, Gerber B, Menzel R (1997) Odorant intensity as a determinant for olfactory conditioning in honeybees: roles in discrimination, overshadowing and memory consolidation. J Exp Biol 200:837-847.
34. Perez-Orive J, Mazor O, Turner GC, Cassenaer S, Wilson RI, Laurent G (2002) Oscillations and sparsening of odor representations in the mushroom body. Science 297:359-365.
35. Rescorla RA, Wagner AR (1972) A theory of Pavlovian conditioning: variations in the effectiveness of reinforcement an nonreinforcement. In: Classical conditioning II: current research and theory (Black AH, Prokasy WF, eds), pp 64-99. New York: Appleton-Century-Crofts.
36. Riemensperger T, Völler T, Stock P, Buchner E, Fiala A (2005) Punishment prediction by dopaminergic neurons in Drosophila. Curr Biol 15: 1953-1960.
37. Root CM, Masuyama K, Green DS, Enell LE, Nässel DR, Lee CH, Wang JW (2008) A presynaptic gain control mechanism fine-tunes olfactory behavior. Neuron 59:311-321.
38. Schaefer AT, Margrie TW (2007) Spatiotemporal representations in the olfactory system. Trends Neurosci 30:92-100.
39. Schultz W (2006) Behavioral theories and the neurophysiology of reward. Annu Rev Psychol 57:87-115.
40. Schwaerzel M, Heisenberg M, Zars T (2002) Extinction antagonizes olfactory memory at the subcellular level. Neuron 35:951-960.
41. Silbering AF, Galizia CG (2007) Processing of odor mixtures in the Drosophila antennal lobe reveals both global inhibition and glomerulus-specific interactions. J Neurosci 27:11966-11977.
42. Silbering AF, Okada R, Ito K, Galizia CG (2008) Olfactory information processing in the Drosophila antennal lobe: anything goes? J Neurosci 28:13075-13087.
43. Solomon PR, Groccia-Ellison ME (1996) Classic conditioning in aged rabbits: delay, trace, and long-delay conditioning. Behav Neurosci 110:427-435.
44. Solomon PR, Vander Schaaf ER, Thompson RF, Weisz DJ (1986) Hippocampus and trace conditioning of the rabbit's classically conditioned nictitating membrane response. Behav Neurosci 100:729-744.
45. Szyszka P, Ditzen M, Galkin A, Galizia CG, Menzel R (2005) Sparsening and temporal sharpening of olfactory representations in the honeybee mushroom bodies. J Neurophysiol 94:3303-3313.
46. Szyszka P, Galkin A, Menzel R (2008) Associative and non-associative plasticity in kenyon cells of the honeybee mushroom body. Front Syst Neurosci 2:3.
47. Szyszka P, Demmler C, Oemisch M, Sommer L, Biergans S, Birnbach B, Silbering AF, Galizia CG (2011) Mind the gap: olfactory trace conditioning in honeybees. J Neurosci 31:7229-7239.
48. Tanimoto H, Heisenberg M, Gerber B (2004) Experimental psychology: event timing turns punishment to reward. Nature 430:983.
49. Thompson RF, Krupa DJ (1994) Organization of memory traces in the mammalian brain. Annu Rev Neurosci 17:519-549.
50. Tomchik SM, Davis RL (2009) Dynamics of learning-related cAMP signaling and stimulus integration in the Drosophila olfactory pathway. Neuron 64:510-521.
51. Tully T, Quinn WG (1985) Classical conditioning and retention in normal and mutant Drosophila melanogaster. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 157:263-277.
52. Turner GC, Bazhenov M, Laurent G (2008) Olfactory representations by Drosophila mushroom body neurons. J Neurophysiol 99:734-746.
53. Wang JW, Wong AM, Flores J, Vosshall LB, Axel R (2003) Two-photon calcium imaging reveals an odor-evoked map of activity in the fly brain. Cell 112:271-282.
54. 2+ imaging. J Neurosci 24:6507-6514.
55. Weiss C, Bouwmeester H, Power JM, Disterhoft JF (1999) Hippocampal lesions prevent trace eyeblink conditioning in the freely moving rat. Behav Brain Res 99:123-132.
56. Wilson RI, Turner GC, Laurent G (2004) Transformation of olfactory representations in the Drosophila antennal lobe. Science 303:366-370.
57. Woodruff-Pak DS, Disterhoft JF (2008) Where is the trace in trace conditioning? Trends Neurosci 31:105-112.
58. Yarali A, Ehser S, Hapil FZ, Huang J, Gerber B (2009) Odour intensity learning in fruit flies. Proc Biol Sci 276:3413-3420.
59. Yu D, Ponomarev A, Davis RL (2004) Altered representation of the spatial code for odors after olfactory classical conditioning; memory trace formation by synaptic recruitment. Neuron 42:437-449.