Abstract
Different visual features of an object, such as its position and direction of motion, are important elements for animal orientation, but the neural circuits extracting them are generally not well understood. We analyzed this problem in Drosophila, focusing on two well-studied behaviors known as optomotor response and fixation response. In the neural circuit controlling the optomotor response, columnar T4 and T5 cells are thought to be crucial. We found that blocking T4 and T5 cells resulted in a complete loss of the optomotor response. Nevertheless, these flies were still able to fixate a black bar, although at a reduced performance level. Further analysis revealed that flies in which T4 and T5 cells were blocked possess an intact position circuit that is implemented in parallel to the motion circuit; the optomotor response is exclusively controlled by the motion circuit, whereas the fixation response is supported by both the position and the motion circuit.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 12 print issues and online access
$209.00 per year
only $17.42 per issue
Buy this article
- Purchase on SpringerLink
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1038%2Fnn.3386/MediaObjects/41593_2013_Article_BFnn3386_Fig1_HTML.jpg)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1038%2Fnn.3386/MediaObjects/41593_2013_Article_BFnn3386_Fig2_HTML.jpg)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1038%2Fnn.3386/MediaObjects/41593_2013_Article_BFnn3386_Fig3_HTML.jpg)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1038%2Fnn.3386/MediaObjects/41593_2013_Article_BFnn3386_Fig4_HTML.jpg)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1038%2Fnn.3386/MediaObjects/41593_2013_Article_BFnn3386_Fig5_HTML.jpg)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1038%2Fnn.3386/MediaObjects/41593_2013_Article_BFnn3386_Fig6_HTML.jpg)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1038%2Fnn.3386/MediaObjects/41593_2013_Article_BFnn3386_Fig7_HTML.jpg)
Similar content being viewed by others
References
Götz, K.G. Optomotorische Untersuchung des visuellen Systems einiger Augenmutanten der Fruchtfliege Drosophila. Kybernetik 2, 77–92 (1964).
Buchner, E. Elementary movement detectors in an insect visual system. Biol. Cybern. 24, 85–101 (1976).
Blondeau, J. & Heisenberg, M. The three-dimensional optomotor torque system of Drosophila melanogaster. Studies on wild type and the mutant optomotor blind H31. J. Comp. Physiol. A 145, 321–329 (1982).
Tammero, L.F. & Dickinson, M.H. The influence of visual landscape on the free flight behavior of the fruit fly Drosophila melanogaster. J. Exp. Biol. 205, 327–343 (2002).
Mronz, M. & Lehmann, F.-O. The free-flight response of Drosophila to motion of the visual environment. J. Exp. Biol. 211, 2026–2045 (2008).
Reichardt, W. & Wenking, H. Optical detection and fixation of objects by fixed flying flies. Naturwissenschaften 56, 424–425 (1969).
Heisenberg, M. & Wolf, R. Vision in Drosophila: Genetics of Microbehavior (Springer-Verlag, Berlin, 1984).
Reiser, M.B. & Dickinson, M.H. Drosophila fly straight by fixating objects in the face of expanding optic flow. J. Exp. Biol. 213, 1771–1781 (2010).
Rister, J. et al. Dissection of the peripheral motion channel in the visual system of Drosophila melanogaster. Neuron 56, 155–170 (2007).
Götz, K.G. Visual guidance in Drosophila. in Development and Neurobiology of Drosophila (eds. Siddiqi, O., Babu, P., Hall, M.L. & Hall, J.C.) 391–407 (Plenum Press, New York, 1980).
Strauss, R. & Pichler, J. Persistence of orientation toward a temporarily invisible landmark in Drosophila melanogaster. J. Comp. Physiol. A 182, 411–423 (1998).
Maimon, G., Straw, A.D. & Dickinson, M.H. A simple vision-based algorithm for decision making in flying Drosophila. Curr. Biol. 18, 464–470 (2008).
Aptekar, J.W., Shoemaker, P.A. & Frye, M.A. Figure tracking by flies is supported by parallel visual streams. Curr. Biol. 22, 482–487 (2012).
Heisenberg, M., Wonneberger, R. & Wolf, R. Optomotor-blind (H31): a Drosophila mutant of the lobula plate giant neurons. J. Comp. Physiol. A 124, 287–296 (1978).
Geiger, G. & Nässel, D.R. Visual orientation behavior of flies after selective laser beam ablation of interneurones. Nature 293, 398–399 (1981).
Hausen, K. & Wehrhahn, C. Neural circuits mediating visual flight control in flies. II. Separation of two control systems by microsurgical brain lesions. J. Neurosci. 10, 351–360 (1990).
Bausenwein, B., Wolf, R. & Heisenberg, M. Genetic dissection of optomotor behavior in Drosophila melanogaster. Studies on wild-type and the mutant optomotor-blind (H31). J. Neurogenet. 3, 87–109 (1986).
Wolf, R. & Heisenberg, M. Visual orientation in motion-blind flies is an operant behavior. Nature 323, 154–156 (1986).
Meinertzhagen, I.A. & O'Neil, S.D. Synaptic organization of columnar elements in the lamina of the wild type in Drosophila melanogaster. J. Comp. Neurol. 305, 232–263 (1991).
Joesch, M., Plett, J., Borst, A. & Reiff, D.F. Response properties of motion-sensitive visual interneurons in the lobula plate of Drosophila melanogaster. Curr. Biol. 18, 368–374 (2008).
Schnell, B. et al. Processing of horizontal optic flow in three visual interneurons of the Drosophila brain. J. Neurophysiol. 103, 1646–1657 (2010).
Joesch, M., Schnell, B., Raghu, S.V., Reiff, D.F. & Borst, A. ON and OFF pathways in Drosophila motion vision. Nature 468, 300–304 (2010).
Eichner, H., Joesch, M., Schnell, B., Reiff, D.F. & Borst, A. Internal structure of the fly elementary motion detector. Neuron 70, 1155–1164 (2011).
Bausenwein, B. & Fischbach, K. Activity labeling patterns in the medulla of Drosophila melanogaster caused by motion stimuli. Cell Tissue Res. 270, 25–35 (1992).
Bausenwein, B., Dittrich, A.P. & Fischbach, K.F. The optic lobe of Drosophila melanogaster. II. Sorting of retinotopic pathways in the medulla. Cell Tissue Res. 267, 17–28 (1992).
Schnell, B., Raghu, S.V., Nern, A. & Borst, A. Columnar cells necessary for motion responses of wide-field visual interneurons in Drosophila. J. Comp. Physiol. A 198, 389–395 (2012).
Seelig, J.D. et al. Two-photon calcium imaging from head-fixed Drosophila during optomotor walking behavior. Nat. Methods 7, 535–540 (2010).
Brand, A.H. & Perrimon, N. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118, 401–415 (1993).
Kitamoto, T. Conditional modification of behavior in Drosophila by targeted expression of a temperature-sensitive shibire allele in defined neurons. J. Neurobiol. 47, 81–92 (2001).
Poggio, T. & Reichardt, W. A theory of the pattern induced flight orientation of the fly Musca domestica. Kybernetik 12, 185–203 (1973).
Wehrhahn, C. Flight torque and lift responses of the housefly (Musca domestica) to a single stripe moving in different parts of the visual field. Biol. Cybern. 29, 237–247 (1978).
Pick, B. Visual flicker induces orientation behavior in the fly Musca. Z. Naturforsch. C 29c, 310–312 (1974).
Wehrhahn, C. Fast and slow flight torque responses in flies and their possible role in visual orientation behavior. Biol. Cybern. 40, 213–221 (1981).
Reichardt, W. Evaluation of optical motion information by movement detectors. J. Comp. Physiol. A 161, 533–547 (1987).
Reichardt, W. & Poggio, T.A. Figure-ground discrimination by relative movement in the visual system of the fly. Part I: Experimental Results. Biol. Cybern. 35, 81–100 (1979).
Egelhaaf, M. On the neuronal basis of figure-ground discrimination by relative motion in the visual system of the fly. I. Behavioral constraints imposed on the neuronal network and the role of the optomotor system. Biol. Cybern. 52, 123–140 (1985).
Egelhaaf, M. On the neuronal basis of figure-ground discrimination by relative motion in the visual system of the fly. II. Figure-detection cells, a new class of visual interneurones. Biol. Cybern. 52, 195–209 (1985).
Liang, P., Heitwerth, J., Kern, R., Kurtz, R. & Egelhaaf, M. Object representation and distance encoding in three-dimensional environments by a neural circuit in the visual system of the blowfly. J. Neurophysiol. 107, 3446–3457 (2012).
Egelhaaf, M. On the neuronal basis of figure-ground discrimination by relative motion in the visual system of the fly. III. Possible input circuitries and behavioral significance of the FD cells. Biol. Cybern. 52, 267–280 (1985).
Warzecha, A.K., Borst, A. & Egelhaaf, M. Photo-ablation of single neurons in the fly visual system reveals neural circuit for the detection of small moving objects. Neurosci. Lett. 141, 119–122 (1992).
Cuntz, H., Haag, J. & Borst, A. Neural image processing by dendritic networks. Proc. Natl. Acad. Sci. USA 100, 11082–11085 (2003).
Borst, A. Drosophila's view on insect vision. Curr. Biol. 19, R36–R47 (2009).
Pfeiffer, B.D. et al. Tools for neuroanatomy and neurogenetics in Drosophila. Proc. Natl. Acad. Sci. USA 105, 9715–9720 (2008).
Acknowledgements
We wish to thank G. Rubin and A. Nern for providing the T4/T5 cell–specific driver line R42F06-Gal4 and V. Jayaraman for advice on setting up the locomotion recorder. We are also grateful to J. Haag, A. Mauss, A. Arenz and A. Leonhardt for many helpful discussions and critically reading the manuscript, S. Prech for help with the design of the Peltier temperature control system, C. Theile for fly work, and F. Foerstner for reconstructing the three horizontal system cells shown in Figure 1a. A. Bahl and A. Borst are members of the Bernstein Center for Computational Neuroscience and the Graduate School of Systemic Neurosciences.
Author information
Authors and Affiliations
Contributions
A. Bahl set up the locomotion recorder and the stimulus display, and wrote the software for reading the behavioral output and displaying the stimulus. A. Bahl and T.S. performed all of the behavioral experiments and evaluated the data. G.A. performed the electrophysiological recordings and analyzed the data. A. Bahl and A. Borst designed the study. A. Borst carried out the modeling work. A. Borst and A. Bahl wrote the manuscript with the help of the other authors.
Corresponding authors
Ethics declarations
Competing interests
The authors declare no competing financial interests.
Supplementary information
Supplementary Text and Figures
Supplementary Figures 1–4 and Supplementary Statistics (PDF 1508 kb)
Rights and permissions
About this article
Cite this article
Bahl, A., Ammer, G., Schilling, T. et al. Object tracking in motion-blind flies. Nat Neurosci 16, 730–738 (2013). https://doi.org/10.1038/nn.3386
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/nn.3386
This article is cited by
-
Direction Selectivity of TmY Neurites in Drosophila
Neuroscience Bulletin (2023)
-
A biophysical account of multiplication by a single neuron
Nature (2022)
-
How fly neurons compute the direction of visual motion
Journal of Comparative Physiology A (2020)
-
A neural heading estimate is compared with an internal goal to guide oriented navigation
Nature Neuroscience (2019)
-
Generation of stable heading representations in diverse visual scenes
Nature (2019)