Central complex neurons exhibit behaviorally gated responses to visual motion in Drosophila

Journal of Neurophysiology

Volumn 111, Issue 1, 2014, Pages 62-71

  Weir, Peter T ^a   Schnell, Bettina ^a   Dickinson, Michael H ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

Author keywords

Context; Fan shaped body; Flight; Optic flow; Task dependent

Indexed keywords

ARTICLE; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; IMAGING AND DISPLAY; NERVE CELL; NERVOUS SYSTEM; NONHUMAN; OPTIC FLOW; PRIORITY JOURNAL; VISUOMOTOR COORDINATION;

CONTEXT; FAN-SHAPED BODY; FLIGHT; OPTIC FLOW; TASK DEPENDENT;

ACTION POTENTIALS; ANIMALS; CALCIUM; DROSOPHILA MELANOGASTER; EVOKED POTENTIALS, VISUAL; GANGLIA, INVERTEBRATE; LOCOMOTION; NEURONS; OPTIC FLOW; RETINA; SENSORY GATING;

EID: 84891532363     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00593.2013     Document Type: Article

References (46)

1. Akerboom J, Chen TW, Wardill TJ, Tian L, Marvin JS, Mutlu S, Calderón NC, Esposti F, Borghuis BG, Sun XR, Gordus A, Orger MB, Portugues R, Engert F, Macklin JJ, Filosa A, Aggarwal A, Kerra R, Takagi R, Kracun S, Shigetomi E, Khakh BS, Baier H, Lagnado L, Wang SS, Bargmann CI, Kimmel BE, Jayaraman V, Svoboda K, Kim DS, Schreiter ER, Looger LL. Optimization of a GCaMP calcium indicator for neural activity imaging. J Neurosci 32: 13819-13840, 2012.
2. Bahl A, Ammer G, Schilling T, Borst A. Object tracking in motion-blind flies. Nat Neurosci 16: 730-738, 2013.
3. Baird E, Srinivasan MV, Zhang S, Cowling A. Visual control of flight speed in honeybees. J Exp Biol 208: 3895-3905, 2005.
4. Bender JA, Dickinson MH. Visual stimulation of saccades in magnetically tethered Drosophila. J Exp Biol 209: 3170-3182, 2006.
5. Bender JA, Pollack AJ, Ritzmann RE. Neural activity in the central complex of the insect brain is linked to locomotor changes. Curr Biol 20: 921-926, 2010.
6. Card G, Dickinson MH. Visually mediated motor planning in the escape response of Drosophila. Curr Biol 18: 1300-1307, 2008.
7. Cherry EC. Some further experiments upon the recognition of speech, with one and with two ears. J Acoust Soc Am 26: 554, 1954.
8. Chiappe ME, Seelig JD, Reiser MB, Jayaraman V. Walking modulates speed sensitivity in Drosophila motion vision. Curr Biol 20: 1470-1475, 2010.
9. Clark DA, Bursztyn L, Horowitz MA, Schnitzer MJ, Clandinin TR. Defining the computational structure of the motion detector in Drosophila. Neuron 70: 1165-1177, 2011.
10. El Jundi B, Heinze S, Lenschow C, Kurylas A, Rohlfing T, Homberg U. The locust standard brain: a 3D standard of the central complex as a platform for neural network analysis. Front Syst Neurosci 3: 21, 2009.
11. Fry SN, Rohrseitz N, Straw AD, Dickinson MH. Visual control of flight speed in Drosophila melanogaster. J Exp Biol 212: 1120-1130, 2009.
12. Gibson JJ. Visually controlled locomotion and visual orientation in animals. Br J Psychol 49: 182-194, 1958.
13. Götz K. Course-control, metabolism and wing interference during ultralong tethered flight in Drosophila melanogaster. J Exp Biol 128: 35-46, 1987.
14. Guo P, Ritzmann RE. Neural activity in the central complex of the cockroach brain is linked to turning behaviors. J Exp Biol 216: 992-1002, 2013.
15. Hammond S, O'Shea M. Escape flight initiation in the fly. J Comp Physiol A 193: 471-476, 2007.
16. Hanesch U, Fischbach K, Heisenberg M. Neuronal architecture of the central complex in Drosophila melanogaster. Cell Tissue Res 257: 343-366, 1989.
17. Heinze S, Homberg U. Linking the input to the output: new sets of neurons complement the polarization vision network in the locust central complex. J Neurosci 29: 4911-4921, 2009.
18. Heinze S, Homberg U. Neuroarchitecture of the central complex of the desert locust: intrinsic and columnar neurons. J Comp Neurol 511: 454-478, 2008.
19. Homberg U. Flight-correlated activity changes in neurons of the lateral accessory lobes in the brain of the locust Schistocerca gregaria. J Comp Physiol A 175: 597-610, 1994.
20. Homberg U. In search of the sky compass in the insect brain. Naturwissenschaften 91: 199-208, 2004.
21. Jayaraman V, Laurent G. Evaluating a genetically encoded optical sensor of neural activity using electrophysiology in intact adult fruit flies. Front Neural Circuits 1: 3, 2007.
22. Joesch M, Schnell B, Raghu SV, Reiff DF, Borst A. ON and OFF pathways in Drosophila motion vision. Nature 468: 300-304, 2010.
23. Jung SN, Borst A, Haag J. Flight activity alters velocity tuning of fly motion-sensitive neurons. J Neurosci 31: 9231-9237, 2011.
24. Kahsai L, Martin JR, Winther AM. Neuropeptides in the Drosophila central complex in modulation of locomotor behavior. J Exp Biol 213: 2256-2265, 2010.
25. Knudsen EI. Fundamental components of attention. Annu Rev Neurosci 30: 57-78, 2007.
26. Koenderink JJ. Optic flow. Vision Res 26: 161-179, 1986.
27. Li W, Pan Y, Wang Z, Gong H, Gong Z, Liu L. Morphological characterization of single fan-shaped body neurons in Drosophila melanogaster. Cell Tissue Res 336: 509-519, 2009.
28. Liu G, Seiler H, Wen A, Zars T, Ito K, Wolf R, Heisenberg M, Liu L. Distinct memory traces for two visual features in the Drosophila brain. Nature 439: 551-556, 2006.
29. Loesel R, Nässel DR, Strausfeld NJ. Common design in a unique midline neuropil in the brains of arthropods. Arthropod Struct Dev 31: 77-91, 2002.
30. Maimon G, Straw AD, Dickinson MH. Active flight increases the gain ofvisual motion processing in Drosophila. Nat Neurosci 13: 393-399, 2010.
31. Martin JR, Raabe T, Heisenberg M. Central complex substructures are required for the maintenance of locomotor activity in Drosophila melanogaster. J Comp Physiol A 185: 277-288, 1999.
32. Paulk A, Millard SS, van Swinderen B. Vision in Drosophila: seeing the world through a model's eyes. Annu Rev Entomol 58: 313-332, 2013.
33. Phillips-Portillo J, Strausfeld NJ. Representation of the brain's superior protocerebrum of the flesh fly, Neobellieria bullata, in the central body. J Comp Neurol 520: 3070-3087, 2012.
34. Phillips-Portillo J. The central complex of the flesh fly, Neobellieria bullata: recordings and morphologies of protocerebral inputs and small-field neurons. J Comp Neurol 520: 3088-3104, 2012.
35. Reichardt W, Poggio T. Visual control of orientation behaviour in the fly. Q Rev Biophys 9: 311-375, 1976.
36. Rosner R, Homberg U. Widespread sensitivity to looming stimuli and small moving objects in the central complex of an insect brain. J Neurosci 33: 8122-8133, 2013.
37. Schnell B, Joesch M, Forstner F, Raghu SV, Otsuna H, Ito K, Borst A, Reiff DF. Processing of horizontal optic flow in three visual interneurons of the Drosophila brain. J Neurophysiol 103: 1646-1657, 2010.
38. Seelig J, Chiappe M, Lott G, Dutta A. Two-photon calcium imaging from head-fixed Drosophila during optomotor walking behavior. Nature 7: 535-540, 2010.
39. Srinivasan M, Zhang S, Bidwell N. Visually mediated odometry in honey-bees. J Exp Biol 200: 2513-2522, 1997.
40. Strausfeld NJ, Hirth F. Deep homology of arthropod central complex and vertebrate basal ganglia. Science 340: 157-161, 2013.
41. Strauss R, Heisenberg M. A higher control center of locomotor behavior in the Drosophila brain. J Neurosci 13: 1852-1861, 1993.
42. Suver MP, Mamiya A, Dickinson MH. Octopamine neurons mediate flight-induced modulation of visual processing in Drosophila. Curr Biol 22: 2294-2302, 2012.
43. Tian L, Hires SA, Mao T, Huber D, Chiappe ME, Chalasani SH, Petreanu L, Akerboom J, McKinney a S, Schreiter ER, Bargmann CI, Jayaraman V, Svoboda K, Looger LL. Imaging neural activity in worms, flies and mice with improved GCaMP calcium indicators. Nat Methods 6: 875-881, 2009.
44. Vitzthum H, Muller M, Homberg U. Neurons of the central complex of the locust Schistocerca gregaria are sensitive to polarized light. J Neurosci 22: 1114-1125, 2002.
45. Wang Z, Pan Y, Li W, Jiang H, Chatzimanolis L, Chang J, Gong Z, Liu L. Visual pattern memory requires foraging function in the central complex of Drosophila. Learn Mem 15: 133-142, 2008.
46. Young JM, Armstrong JD. Structure of the adult central complex in Drosophila: organization of distinct neuronal subsets. J Comp Neurol 518: 1500-1524, 2010.