Theta Motion Processing in Fruit Flies

The tiny brains of insects presumably impose significant computational limitations on algorithms controlling their behavior. Nevertheless, they perform fast and sophisticated visual maneuvers. This includes tracking features composed of second-order motion, in which the feature is defined by higher-order image statistics, but not simple correlations in luminance. Flies can track the true direction of even theta motions, in which the first-order (luminance) motion is directed opposite the second-order moving feature. We exploited this paradoxical feature tracking response to dissect the particular image properties that flies use to track moving objects. We find that theta motion detection is not simply a result of steering toward any spatially restricted flicker. Rather, our results show that fly high-order feature tracking responses can be broken down into positional and velocity components – in other words, the responses can be modeled as a superposition of two independent steering efforts. We isolate these elements to show that each has differing influence on phase and amplitude of steering responses, and together they explain the time course of second-order motion tracking responses during flight. These observations are relevant to natural scenes, where moving features can be much more complex.

[1]  F. A. Miles,et al.  Visual Motion and Its Role in the Stabilization of Gaze , 1992 .

[2]  J. M. Zanker,et al.  Visual detection of paradoxical motion in flies , 1991, Journal of Comparative Physiology A.

[3]  Martin Egelhaaf,et al.  Visual course control in flies relies on neuronal computation of object and background motion , 1988, Trends in Neurosciences.

[4]  Michael H. Dickinson,et al.  A modular display system for insect behavioral neuroscience , 2008, Journal of Neuroscience Methods.

[5]  M. Heisenberg,et al.  Vision in Drosophila , 1984 .

[6]  W. Reichardt,et al.  Computational structure of a biological motion-detection system as revealed by local detector analysis in the fly's nervous system. , 1989, Journal of the Optical Society of America. A, Optics and image science.

[7]  Michael H Dickinson,et al.  Motor output reflects the linear superposition of visual and olfactory inputs in Drosophila , 2004, Journal of Experimental Biology.

[8]  Yan Zhu,et al.  Peripheral Visual Circuits Functionally Segregate Motion and Phototaxis Behaviors in the Fly , 2009, Current Biology.

[9]  B. Kimmerle,et al.  Object detection by relative motion in freely flying flies , 1996, Naturwissenschaften.

[10]  Johannes M. Zanker,et al.  Theta motion: a paradoxical stimulus to explore higher order motion extraction , 1993, Vision Research.

[11]  W. Reichardt,et al.  Properties of individual movement detectors as derived from behavioural experiments on the visual system of the fly , 1988, Biological Cybernetics.

[12]  K. Hausen Motion sensitive interneurons in the optomotor system of the fly , 1982, Biological Cybernetics.

[13]  A. Borst,et al.  A look into the cockpit of the fly: visual orientation, algorithms, and identified neurons , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[14]  Michael H Dickinson,et al.  Spatial organization of visuomotor reflexes in Drosophila , 2004, Journal of Experimental Biology.

[15]  Dario L. Ringach,et al.  Flies see second-order motion , 2008, Current Biology.

[16]  Andreas S. Thum,et al.  The Neural Substrate of Spectral Preference in Drosophila , 2008, Neuron.

[17]  K. Götz Course-control, metabolism and wing interference during ultralong tethered flight in Drosophila melanogaster , 1987 .

[18]  Karl Georg Götz,et al.  Flight control in Drosophila by visual perception of motion , 1968, Kybernetik.

[19]  R. Wolf,et al.  On the fine structure of yaw torque in visual flight orientation ofDrosophila melanogaster , 2004, Journal of comparative physiology.

[20]  Mark A Frye,et al.  Dynamics of optomotor responses in Drosophila to perturbations in optic flow , 2010, Journal of Experimental Biology.

[21]  N. Strausfeld,et al.  Dissection of the Peripheral Motion Channel in the Visual System of Drosophila melanogaster , 2007, Neuron.

[22]  J. Zanker On the elementary mechanism underlying secondary motion processing. , 1996, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[23]  Michael B. Reiser,et al.  Dynamic properties of large-field and small-field optomotor flight responses in Drosophila , 2007, Journal of Comparative Physiology A.

[24]  M. Egelhaaf,et al.  Processing of figure and background motion in the visual system of the fly , 1989, Biological Cybernetics.

[25]  G. Sperling,et al.  Drift-balanced random stimuli: a general basis for studying non-Fourier motion perception. , 1988, Journal of the Optical Society of America. A, Optics and image science.

[26]  R. Wolf,et al.  On the fine structure of yaw torque in visual flight orientation ofDrosophila melanogaster , 1979, Journal of comparative physiology.

[27]  J. M. Zanker,et al.  Theta motion: A new psychophysical paradigm indicating two levels of visual motion perception , 1990, Naturwissenschaften.

[28]  B. Hassenstein,et al.  Systemtheoretische Analyse der Zeit-, Reihenfolgen- und Vorzeichenauswertung bei der Bewegungsperzeption des Rüsselkäfers Chlorophanus , 1956 .

[29]  Martin Egelhaaf,et al.  Dynamic properties of two control systems underlying visually guided turning in house-flies , 1987, Journal of Comparative Physiology A.

[30]  C. Wehrhahn,et al.  Neural circuits mediating visual flight control in flies. II. Separation of two control systems by microsurgical brain lesions , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[31]  Werner Reichardt,et al.  Optical detection and fixation of objects by fixed flying flies , 1969, Naturwissenschaften.

[32]  Alexander Borst,et al.  Principles of visual motion detection , 1989, Trends in Neurosciences.