Mushroom bodies modulate salience-based selective fixation behavior in Drosophila

European Journal of Neuroscience

Volumn 27, Issue 6, 2008, Pages 1441-1451

  Xi, Wang ^a,b   Peng, Yueqing ^a,b   Guo, Jianzeng ^a   Ye, Yizhou ^a   Zhang, Ke ^a,b   Yu, Feng ^a,b   Guo, Aike ^a,c  

^a Shanghai Jiao Tong University Affiliated Sixth People s Hospital   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^c INSTITUTE OF BIOPHYSICS   (China)

Author keywords

Behavioral neuroscience; Drosophila melanogaster; Fixation; Flight simulator; Mushroom bodies

Indexed keywords

ARTICLE; DROSOPHILA; MUSHROOM BODY; NOISE; NONHUMAN; PRIORITY JOURNAL; SENSORY STIMULATION; SMELLING; VISUAL ORIENTATION;

ANIMALS; DROSOPHILA MELANOGASTER; FEMALE; FLIGHT, ANIMAL; MUSHROOM BODIES; PHOTIC STIMULATION; VISUAL PERCEPTION;

EID: 40949141956     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2008.06114.x     Document Type: Article

References (64)

1. Armstrong, J.D., de Belle, J.S., Wang, Z. Kaiser, K. (1998) Metamorphosis of the mushroom bodies; large-scale rearrangements of the neural substrates for associative learning and memory in Drosophila. Learn. Mem, 5, 102 114.
2. de Belle, J.S. Heisenberg, M. (1994) Associative odor learning in Drosophila abolished by chemical ablation of mushroom bodies. Science, 263, 692 695.
3. de Belle, J.S. Heisenberg, M. (1996) Expression of Drosophila mushroom body mutations in alternative genetic backgrounds: a case study of the mushroom body miniature gene (mbm). Proc. Natl Acad. Sci. USA, 93, 9875 9880.
4. Chen, M.S., Obar, R.A., Schroeder, C.C., Austin, T.W., Poodry, C.A., Wadsworth, S.C. Vallee, R.B. (1991) Multiple forms of dynamin are encoded by shibire, a Drosophila gene involved in endocytosis. Nature, 351, 583 586.
5. Davis, R.L. (1993) Mushroom bodies and Drosophila learning. Neuron, 11, 1 14.
6. Desimone, R. Duncan, J. (1995) Neural mechanisms of selective visual attention. Annu. Rev. Neurosci., 18, 193 222.
7. Ehmer, B. Gronenberg, W. (2002) Segregation of visual input to the mushroom bodies in the honeybee (Apis mellifera). J. Comp. Neurol., 451, 362 373.
8. Everling, S., Tinsley, C.J., Gaffan, D. Duncan, J. (2002) Filtering of neural signals by focused attention in the monkey prefrontal cortex. Nat. Neurosci., 5, 671 676.
9. Goetz, K.G. (1964) Optomotorische Untersuchung des visuellen Systems einiger Augenmutanten der Fruchtfliege Drosophila. Kybernetik, 2, 77 92.
10. Goetz, K.G. (1994) Exploratory strategies in Drosophila. In Schildberger, K. Elsner, N. (Eds), Neural Basis of Behavioral Adaptations. International Symposium. Tuzing, Germany, pp. 47 59.
11. Gottfried, J.A. Dolan, R.J. (2003) The nose smells what the eye sees: crossmodal visual facilitation of human olfactory perception. Neuron, 39, 375 386.
12. Greenspan, R.J. van Swinderen, B. (2004) Cognitive consonance: complex brain functions in the fruit fly and its relatives. Trends Neurosci., 27, 707 711.
13. Guo, J. Guo, A. (2005) Crossmodal interactions between olfactory and visual learning in Drosophila. Science, 309, 307 310.
14. Guo, A., Li, L., Xia, S.Z., Feng, C.H., Wolf, R. Heisenberg, M. (1996) Conditioned visual flight orientation in Drosophila: dependence on age, practice, and diet. Learn. Mem., 3, 49 59.
15. Heisenberg, M. (1998) What do the mushroom bodies for the insect brain? Learn. Mem., 5, 1 10.
16. Heisenberg, M. (2003) Mushroom body memoir: from maps to models. Nat. Rev. Neurosci., 4, 266 275.
17. Heisenberg, M. Wolf, R. (1984) Vision in Drosophila. Springer, Berlin.
18. Heisenberg, M., Wolf, R. Brembs, B. (2001) Flexibility in a single behavioral variable of Drosophila. Learn. Mem., 8, 1 10.
19. Horn, E. (1978) The mechanism of object fixation and its relation to spontaneous pattern preferences in Drosophila melanogaster. Biol. Cybern., 31, 145 158.
20. Huber, F. (1963) The role of the central nervous system in Orthoptera during the co-ordination and control of stridulation. In Busnel, R.G. (Ed.), Acoustic Behavior of Animals. Elsevier, Amsterdam, pp. 440 488.
21. Huber, F. (1965) Brain controlled behavior in orthopterans. In Treherne, J.E. Beament, J.W.L. (Eds), The Physiology of the Insect Central Nervous System. Academic Press, London, pp. 233 246.
22. Joiner, W.J., Crocker, A., White, B.H. Sehgal, A. (2006) Sleep in Drosophila is regulated by adult mushroom bodies. Nature, 441, 757 760.
23. Kanwisher, N. Wojciulik, E. (2000) Visual attention: insights from brain imaging. Nat. Rev. Neurosci., 1, 91 100.
24. 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.
25. Koenig, J.H., Saito, K. Ikeda, K. (1983) Reversible control of synaptic transmission in a single gene mutant of Drosophila melanogaster. J. Cell Biol., 96, 1517 1522.
26. Land, M.F. (1997) Visual acuity in insects. Annu. Rev. Entomol., 42, 147 177.
27. Laurent, G. (1996) Dynamical representation of odors by oscillating and evolving neural assemblies. Trends Neurosci., 19, 489 496.
28. Laurent, G. Davidowitz, H. (1994) Encoding of olfactory information with oscillating neural assemblies. Science, 265, 1872 1875.
29. Laurent, G. Naraghi, M. (1994) Odorant-induced oscillations in the mushroom bodies of the locust. J. Neurosci., 14, 2993 3004.
30. Li, Y. Strausfeld, N.J. (1997) Morphology and sensory modality of mushroom body extrinsic neurons in the brain of the cockroach, Periplaneta americana. J. Comp. Neurol., 387, 631 650.
31. Liu, X., Krause, W.C. Davis, R.L. (2007) GABA(A) receptor RDL inhibits Drosophila olfactory associative learning. Neuron, 56, 1090 1102.
32. Liu, L., Wolf, R., Ernst, R. Heisenberg, M. (1999) Context generalization in Drosophila visual learning requires the mushroom bodies. Nature, 400, 753 756.
33. Martin, J.R., Ernst, R. Heisenberg, M. (1998) Mushroom bodies suppress locomotor activity in Drosophila melanogaster. Learn. Mem., 5, 179 191.
34. Martinez-Trujillo, J. Treue, S. (2002) Attentional modulation strength in cortical area MT depends on stimulus contrast. Neuron, 35, 365 370.
35. McDonald, J.J., Teder-Salejarvi, W.A. Hillyard, S.A. (2000) Involuntary orienting to sound improves visual perception. Nature, 407, 906 908.
36. McGuire, S.E., Deshazer, M. Davis, R.L. (2005) Thirty years of olfactory learning and memory research in Drosophila melanogaster. Prog. Neurobiol., 76, 328 347.
37. Nitz, D.A., van Swinderen, B., Tononi, G. Greenspan, R.J. (2002) Electrophysiological correlates of rest and activity in Drosophila melanogaster. Curr. Biol., 12, 1934 1940.
38. Otto, D. (1971) Untersuchugen zur zentralnervosen kontrolle der lauterzeugung von grillen. Z. Vergl. Physiol., 74, 227 271.
39. Peng, Y., Xi, W., Zhang, W., Zhang, K. Guo, A. (2007) Experience improves feature extraction in Drosophila. J. Neurosci., 27, 5139 5145.
40. Pitman, J.L., McGill, J.J., Keegan, K.P. Allada, R. (2006) A dynamic role for the mushroom bodies in promoting sleep in Drosophila. Nature, 441, 753 756.
41. Poggio, T. Reichardt, W. (1976) Visual control of orientation behaviour in the fly. Part II. Towards the underlying neural interactions. Q. Rev. Biophys., 9, 377 438.
42. Rensink, R.A., O'Regan, J.K. Clark, J.J. (1997) To see or not to see: the need for attention to perceive in scenes. Psychol. Sci., 8, 368 373.
43. Reynolds, J.H. Chelazzi, L. (2004) Attentional modulation of visual processing. Annu. Rev. Neurosci., 27, 611 647.
44. Reynolds, J.H., Chelazzi, L. Desimone, R. (1999) Competitive mechanisms subserve attention in macaque areas V2 and V4. J. Neurosci., 19, 1736 1753.
45. Reynolds, J.H., Pasternak, T. Desimone, R. (2000) Attention increases sensitivity of V4 neurons. Neuron, 26, 703 714.
46. Schildberger, K. (1984) Multimodal interneurons in the cricket brain: properties of identified extrinsic mushroom body cells. J. Comp. Physiol. A, 154, 71 79.
47. Strausfeld, N.J., Hansen, L., Li, Y., Gomez, R.S. Ito, K. (1998) Evolution, discovery, and interpretations of arthropod mushroom bodies. Learn. Mem., 5, 11 37.
48. Strausfeld, N.J., Sinakevitch, I. Vilinsky, I. (2003) The mushroom bodies of Drosophila melanogaster: an immunocytological and golgi study of Kenyon cell organization in the calyces and lobes. Microsc. Res. Tech., 62, 151 169.
49. Strauss, R. Heisenberg, M. (1993) A higher control center of locomotor behavior in the Drosophila brain. J. Neurosci., 13, 1852 1861.
50. Strayer, D.L., Drews, F.A. Johnston, W.A. (2003) Cell phone-induced failures of visual attention during simulated driving. J. Exp. Psychol. Appl., 9, 23 32.
51. Swinderen, B. (2005) The remote roots of consciousness in fruit-fly selective attention? Bioessays, 27, 321 330.
52. van Swinderen, B. (2007) Attention-like processes in Drosophila require short-term memory genes. Science, 315, 1590 1593.
53. van Swinderen, B. Flores, K.A. (2007) Attention-like processes underlying optomotor performance in a Drosophila choice maze. Dev. Neurobiol., 67, 129 145.
54. van Swinderen, B. Greenspan, R.J. (2003) Salience modulates 20-30 Hz brain activity in Drosophila. Nat. Neurosci., 6, 579 586.
55. van Swinderen, B., Nitz, D.A. Greenspan, R.J. (2004) Uncoupling of brain activity from movement defines arousal states in Drosophila. Curr. Biol., 14, 81 87.
56. Tang, S. Guo, A. (2001) Choice behavior of Drosophila facing contradictory visual cues. Science, 294, 1543 1547.
57. Treue, S. (2001) Neural correlates of attention in primate visual cortex. Trends Neurosci., 24, 295 300.
58. Wahdepuhl, M. (1983) Control of grasshopper singing behavior by the brain responses to electrical stimulation. Z. Tierpsychol., 63, 173 200.
59. Wolf, R., Wittig, T., Liu, L., Wustmann, G., Eyding, D. Heisenberg, M. (1998) Drosophila mushroom bodies are dispensable for visual, tactile, and motor learning. Learn. Mem., 5, 166 178.
60. Wu, Z., Gong, Z., Feng, C. Guo, A. (2000) An emergent mechanism of selective visual attention in Drosophila. Biol. Cybern., 82, 61 68.
61. Ye, Y., Xi, W., Peng, Y., Wang, Y. Guo, A. (2004) Long-term but not short-term blockade of dopamine release in Drosophila impairs orientation during flight in a visual attention paradigm. Eur. J. Neurosci., 20, 1001 1007.
62. Zars, T. (2000) Behavioral functions of the insect mushroom bodies. Curr. Opin. Neurobiol., 10, 790 795.
63. Zeman, A. (2001) Consciousness. Brain, 124, 1263 1289.
64. Zhang, K., Guo, J.Z., Peng, Y., Xi, W. Guo, A. (2007) Dopamine-mushroom body circuit regulates saliency-based decision-making in Drosophila. Science, 316, 1901 1904.