Motor output reflects the linear superposition of visual and olfactory inputs in Drosophila

Journal of Experimental Biology

Volumn 207, Issue 1, 2004, Pages 123-131

  Frye, Mark A ^a   Dickinson, Michael H ^a  

^a California Institute of Technology   (United States)

Author keywords

Drosophila; Fruit fly; Multimodal integration; Olfaction; Optomotor; Sensorimotor integration; Sensory fusion; Vision

Indexed keywords

ANIMAL; ARTICLE; ASSOCIATION; BIOLOGICAL MODEL; COMPARATIVE STUDY; DROSOPHILA MELANOGASTER; FLYING; MOTOR ACTIVITY; ODOR; PHOTOSTIMULATION; PHYSIOLOGY; PSYCHOMOTOR PERFORMANCE;

ANIMALS; CUES; DROSOPHILA MELANOGASTER; FLIGHT, ANIMAL; MODELS, BIOLOGICAL; MOTOR ACTIVITY; ODORS; PHOTIC STIMULATION; PSYCHOMOTOR PERFORMANCE; SMELL;

ANIMALIA; DROSOPHILA MELANOGASTER; INSECTA; MELANOGASTER;

EID: 0347596885     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.00725     Document Type: Article

References (40)

1. Baader, A., Schafer, M. and Rowell, C. H. F. (1992). The perception of the visual flow field by flying locusts - a behavioral and neuronal analysis. J. Exp. Biol. 165, 137-160.
2. Barth, M., Hirsch, H. V., Meinertzhagen, I. A. and Heisenberg, M. (1997). Experience-dependent developmental plasticity in the optic lobe of Drosophila melanogaster. J. Neurosci. 17, 1493-1504.
3. Borst, A. (1991). Fly visual interneurons responsive to image expansion. Zool. Jb. Physiol. 95, 305-313.
4. Brand, A. and Perrimon, N. (1993). Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118, 401-415.
5. Connolly, J. B., Roberts, I. J. H., Armstrong, K., Kaiser, K., Forte, M., Tully, T. and O'Kane, C. J. (1996). Associative learning disrupted by impaired Gs signaling in Drosophila mushroom bodies. Science 274, 2104-2107.
6. deBelle, J. S. and Heisenberg, M. (1994). Associative odor learning in Drosophila abolished by chemical ablation of mushroom bodies. Science 263, 692-695.
7. Dickinson, M., Lehman, F. and Chan, W. (1998). The control of mechanical power in insect flight. Am. Zool. 38, 718-728.
8. Dickinson, M. H. and Tu, M. S. (1997). The function of Dipteran flight muscle. Comp. Biochem. Physiol. A 116, 223-238.
9. Fry, S. and Dickinson, M. (2003). The aerodynamics of free-flight maneuvers in Drosophila. Science 300, 495-498.
10. Fry, S., Sayaman, R. and Dickinson, M. (2003). The aerodynamics of free-flight maneuvers in Drosophila. Science 300, 495-498.
11. Frye, M. A. and Dickinson, M. H. (2001). Fly flight: a model for the neural control of complex behavior. Neuron 32, 385-388.
12. Frye, M. A., Tarsitano, M. and Dickinson, M. H. (2003). Odor localization requires visual feedback during free flight in Drosophila melanogaster. J. Exp. Biol. 206, 843-855.
13. Gibbs, S. M., Becker, A., Hardy, R. W. and Truman, J. W. (2001). Soluble guanylate cyclase is required during development for visual system function in Drosophila. J. Neurosci. 21, 7705-7714.
14. Gronenberg, W., Milde, J. J. and Strausfeld, N. J. (1995). Oculomotor control in calliphorid flies - organization of descending neurons to neck motor-neurons responding to visual-stimuli. J. Comp. Neurol. 361, 267-284.
15. Gronenberg, W. and Strausfeld, N. J. (1990). Descending neurons supplying the neck and flight motor of Diptera - physiological and anatomical characteristics. J. Comp. Neurol. 302, 973-991.
16. Gronenberg, W. and Strausfeld, N. J. (1992). Premotor descending neurons responding selectively to local visual-stimuli in flies. J. Comp. Neurol. 316, 87-103.
17. Guo, A. and Götz, K. G. (1997). Association of visual objects and olfactory cues in Drosophila. Learn. Mem. 4, 192-204.
18. Heide, G. (1983). Neural mechanisms of flight control in Diptera. In Insect Flight II, vol. Biona Report 2 (ed. W. Nachtigall), pp. 35-52. Stuttgart: G. Fischer.
19. Heide, G. and Götz, K. G. (1996). Optomotor control of course and altitude in Drosophila melanogaster is correlated with distinct activities of at least three pairs of flight steering muscles. J. Exp. Biol. 199, 1711-1726.
20. Ito, K., Suzuki, K., Estes, P., Ramaswami, M., Yamamoto, D. and Strausfeld, N. J. (1998). The organization of extrinsic neurons and their implications in the functional roles of the mushroom bodies in Drosophila melanogaster Meigen. Learn. Mem. 5, 52-77.
21. Juusola, M. and Hardie, R. C. (2001). Light adaptation in Drosophila photoreceptors: I. Response dynamics and signaling efficiency at 25 degrees C. J. Gen. Physiol. 117, 3-25.
22. 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.
23. Lehmann, F. O. and Dickinson, M. H. (1997). The changes in power requirements and muscle efficiency during elevated force production in the fruit fly Drosophila melanogaster. J. Exp. Biol. 200, 1133-1143.
24. Lehmann, F. O. and Dickinson, M. H. (2001). The production of elevated flight force compromises manoeuvrability in the fruit fly Drosophila melanogaster. J. Exp. Biol. 204, 627-635.
25. Lehmann, F. O. and Götz, K. G. (1996). Activation phase ensures kinematic efficacy in flight-steering muscles of Drosophila melanogaster. J. Comp. Physiol. A 179, 311-322.
26. Olberg, R. M. (1981). Parallel encoding of direction of wind, head, abdomen, and visual-pattern movement by single interneurons in the dragonfly. J. Comp. Physiol. 142, 27-41.
27. Olberg, R. M. and Willis, M. A. (1990). Pheromone-modulated optomotor response in male gypsy moths, Lymantria dispar L - Directionally selective visual interneurons in the ventral nerve cord. J. Comp. Physiol. A 167, 707-714.
28. Pascual, A. and Preat, T. (2001). Localization of long-term memory within the Drosophila mushroom body. Science 294, 1115-1117.
29. Rowell, C. H. and Reichert, H. (1986). Three descending interneurons reporting deviation from course in the locust. II. Physiology. J. Comp. Physiol. A 158, 775-794.
30. Sherman, A. and Dickinson, M. H. (2003). A comparison of visual and haltere-mediated equilibrium reflexes in the fruit fly Drosophila melanogaster. J. Exp. Biol. 206, 295-302.
31. Stensmyr, M., Giordano, E., Balloi, A., Angioy, A.-M. and Hansson, B. (2003). Novel natural ligands for Drosophila olfactory receptor neurons. J. Exp. Biol. 206, 715-724.
32. Strauss, R. (2002). The central complex and the genetic dissection of locomotor behavior. Curr. Opin. Neurobiol. 12, 633-638.
33. Tammero, L. F. and Dickinson, M. H. (2002a). Collision-avoidance and landing responses are mediated by separate pathways in the fruit fly, Drosophila melanogaster. J. Exp. Biol. 205, 2785-2798.
34. Tammero, L. F. and Dickinson, M. H. (2002b). The influence of visual landscape on the free flight behavior of the fruit fly Drosophila melanogaster. J. Exp. Biol. 205, 327-343.
35. Tammero, L. F., Frye, M. A. and Dickinson, M. H. (2004). Spatial organization of visuomotor reflexes in Drosophila. J. Exp. Biol. 207, 113-122.
36. Tannouye, M. A. and Wyman, R. J. (1980). Motor outputs of giant nerve fiber in Drosophila. J. Neurophysiol. 44, 405-421.
37. Trimarchi, J. R. and Schneiderman, A. M. (1995a). Different neural pathways coordinate Drosophila flight initiations evoked by visual and olfactory stimuli. J. Exp. Biol. 198, 1099-1104.
38. Trimarchi, J. R. and Schneiderman, A. M. (1995b). Initiation of flight in the unrestrained fly, Drosophila melanogaster. J. Zool. 235, 211-222.
39. Vosshall, L. B. (2000). Olfaction in Drosophila. Curr. Opin. Neurobiol. 10, 498-503.
40. Wolf, R. and Heisenberg, M. (1990). Visual control of straight flight in Drosophila melanogaster. J. Comp. Physiol. A 167, 269-283.