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The influence of visual landscape on the free flight behavior of the fruit fly Drosophila melanogaster

Lance F. Tammero^1,* and Michael H. Dickinson²

¹ UCB/UCSF Joint Bioengineering Graduate Group, 3060 Valley Life Science Building and
² Department of Integrative Biology, University of California at Berkeley, Berkeley, CA 94720, USA

View larger version (19K): [in a new window]   Fig. 1. Apparatus for measuring free flight trajectories. Stereo video cameras film the flies as they explore a cylindrical arena. Infrared (IR) illumination was used to avoid interference with the fly’s vision. A combination of on-line and post processing generated a three-dimensional flight trajectory. DSP, digital signal processor; LED, light-emitting diode; VCR, video recorder.

View larger version (19K): [in a new window]   Fig. 2. Basic kinematics of free flight trajectories. (A) A sample trajectory lasting 17 s within a textured background demonstrating how a fly explores its environment using a series of straight flight segments separated by saccades. Note that the pattern on the walls was randomly filled, instead of the regular pattern that is shown in the figure. (B) Angular, horizontal and vertical velocity plotted as a time series for the trajectory shown in A. Spikes in the angular velocity trace indicate saccades (B, upper). Horizontal and vertical velocities (B, lower) change in concert with angular velocity. (C) Event-triggered averages of angular velocity and horizontal and vertical velocity over all flies. Traces were aligned using the point of maximum angular velocity. Each plot of horizontal and vertical velocity shows two traces representing the mean ± S.E.M, mean line not plotted. The velocities come from 1523 saccades from 36 flies. All saccades are plotted as if they occurred in the same direction, with the sign of angular velocity reversed for saccades to the right. Horizontal velocity (blue) decreases slowly before each saccade, rises rapidly afterwards and then returns to its pre-saccade level. Vertical velocity (red) increases slightly before the saccade and decreases after the saccade.

View larger version (32K): [in a new window]   Fig. 3. Visual input influences the direction but not the amplitude of a saccade. (A) Approach angle is defined as the angle that a continuation of the trajectory to the wall of the arena would make with the line perpendicular to the tangent at the intersection point. Approach angle is used as a rough measure of the asymmetry of visual motion experienced by the fly prior to the saccade. Positive approach angles indicate that the fly is closer to the arena wall on its left (L) side, and thus that the visual motion perceived on the left side is greater. Negative approach angles indicate that the perception of visual motion is stronger on the fly’s right (R) side. (B) Saccade angle plotted against approach angle for 1579 saccades from trajectories from 36 flies flying within a textured background. The two clusters around ±90° demonstrate that the fly does not alter the amplitude of the saccade on the basis of asymmetries in visual motions. Red lines show linear regressions for each cluster (r2<0.01, P>0.5 for the upper line both regressions, P>0.25 for the lower line). The histogram to the right of the scatterplot shows the distribution of saccade angles pooled over all measurements. (C) The probability of turning left or right depends on approach angle. To generate the probability distributions, saccade angles were binned according to approach angle. Each bin was 5° wide, and bin centers were separated by 5°.

View larger version (38K): [in a new window]   Fig. 4. The fly’s visual environment influences the spatial structure of its flight trajectory. (A) Sample trajectories taken within uniform (left) and textured (right) backgrounds showing the effects of changing the fly’s visual environment. The inter-saccade segments are longer for flight within the uniform background, causing saccades to occur farther from the center of the arena. (B) Histogram of the fly’s position within the arena for uniform and textured backgrounds pooled over multiple flies. The transit probability peaks in the center of the arena with a textured background and is more evenly distributed with the uniform background. (C) Histograms showing the distribution of saccade locations. Within a textured background, flies tend to saccade in the middle of the arena. Position bins are 50 mmx50 mm. Uniform background data represent 58 trajectories totaling 916 s containing 1080 saccades; textured background data represent 36 trajectories totaling 1020 s containing 1579 saccades.

View larger version (23K): [in a new window]   Fig. 5. Histograms of kinematic parameters within uniform (A) and textured (B) backgrounds. The distribution of angular velocity taken from inter-saccade flight segments is similar for flight within a textured or uniform background. The mean horizontal velocity is reduced during flight within a textured background, and the variance of vertical velocity is reduced. In addition, flies tend to fly at a lower altitude within a textured background. The uniform background data come from 58 trajectories totaling 916 s, the textured background data come from 36 trajectories totaling 1020 s.

View larger version (27K): [in a new window]   Fig. 6. Histograms describing saccade behavior within uniform (A) and textured (B) backgrounds. The time interval between saccades and the distance covered between successive saccades are reduced within a textured background. Removal of the textured background, however, does not affect saccade amplitude. Saccades do, however, occur farther from the center of the arena within a uniform background (see also Fig. 4C). The uniform background data come from 58 trajectories containing 1080 saccades, the textured background data come from 36 trajectories containing 1579 saccades.

View larger version (21K): [in a new window]   Fig. 7. Removing the textured background does not affect saccade amplitude. (A) Plots of approach angle versus saccade angle (see Fig. 3) within a uniform background (black symbols). For comparison, the distributions of saccades in a textured background are replotted from Fig. 3 (gray symbols). In both cases, there are two clusters of saccades centered at ±90°. The r2 values from regression lines fitted to each cluster were again small (r2<0.05, P<0.02 for both). (B) Probabilities of saccading left (blue) and right (red) within uniform and textured backgrounds. Probability distributions were found as described in Fig. 3. The probability of saccading in each direction was similar for flight within the uniform (solid lines) and textured (dashed lines) backgrounds.

View larger version (44K): [in a new window]   Fig. 8. Between saccades, asymmetries in visual motion cause deviation from straight flight, resulting in the fly turning away from the side experiencing the stronger visual motion signal. (A) Each inter-saccade flight segment was rotated and translated such that the initial trajectory, estimated by a regression through the first three points, was aligned downwards along the y-axis. Approach angle (defined in Fig. 3) was used to determine the side of the fly nearest to the wall of the arena, and the straight segments were separated and grouped accordingly. The overlaid plots demonstrate that the flies tend to deviate from straight flight by turning away from the nearest wall, particularly during flight within a textured background. (B) A plot of deviation angle against approach angle demonstrates that asymmetries in perceived visual motion cause flies to deviate from straight flight. Deviation angle is defined as the angle between the best-fitting straight line through the flight segment and the vertical axis. Linear fits yielded a slope of 0.26 (r2=0.11, P<0.001) with the textured background and a slope of 0.13 (r2=0.04, P<0.001) with the uniform background. The difference between the two slopes was significant (P<0.01, F-test). Uniform background data include 959 straight flight segments taken from 58 trajectories, textured data include 1231 straight segments from 36 trajectories.

View larger version (31K): [in a new window]   Fig. 9. Reconstruction of the fly’s visual environment and estimation of optic flow by local motion detection. (A) Reconstruction of the fly’s visual environment is based upon the fly’s position (red circle) and its heading (red arrow) for both the textured (top) and uniform (bottom) backgrounds. Both cases represent the position of a fly 500 ms before a saccade. (B) Calculation of the fly’s visual environment from its position. The projection (in spherical coordinates) of each portion of visual texture onto the fly’s retina was calculated. For example, the regions indicated by the numbers in A map to those in B. A frame representing the mapping of the fly’s visual environment onto its retina at a single point in its flight, similar to that shown in B, was determined for each point along its flight trajectory. (C) Output of local motion detectors. A motion-detection algorithm using delay and correlate motion detectors was applied to this series of frames, resulting in local calculations of horizontal and vertical motion, which are represented by a vector field. Vector fields representing the mean response of the output of the horizontal and vertical motion detectors taken over the 500 ms preceding a saccade are shown in this figure. Note that the spacing of the inputs and outputs of the elementary motion detector was 5°; every second arrow has thus been omitted for clarity. Top, textured background; bottom, uniform background.

View larger version (47K): [in a new window]   Fig. 10. Large-field, unidirectional visual motion does not trigger saccades. (A) Large-field rotation calculation. A vector field representing the output of the local motion at a single instant of time is shown. The horizontal components of the visual motion perceived through the local motion detectors were spatially summed over each of the two frontal quadrants (together comprising 180° of azimuth) of the fly’s field of view (regions 2 and 3 in Fig. 9). For each saccade, the side away from which the fly turns is termed ipsilateral and the side towards which the fly turns is termed contralateral. Front-to-back rotation is plotted as positive for each side. Red arrows indicate the direction of large-field summation. (B) Event-triggered averages suggest that large-field horizontal motion does not trigger saccades. Each individual trace (gray lines) represents the time course of large-field horizontal motion (HIps and HCont) before and after each saccade. The y-axis of this and subsequent figures is a dimensionless quantity that represents the amplitude of the spatially summed output of the motion detectors without any sort of normalization (see Appendix for details). Each trace is aligned at the initiation of the saccade, referred to as time zero. The mean value is shown by the red lines; blue lines represent ±S.D. The gray regions of each plot indicate time after the initiation of each saccade. Large-field front-to-back rotation on both sides precedes each saccade during flight within a textured background (top traces), but is absent during flight within a uniform background (bottom traces). The time resolution of each of these traces was 6.67 ms. Individual traces were taken from 123 saccades from three flies within a textured background and 99 saccades from three flies within a uniform background. (C) Large-field vertical motion, calculated by spatially summing the output of the vertical elementary motion detectors. Upward motion is denoted as positive. (D) Event-triggered averages indicate that saccades are not triggered by vertical motion. Large-field downward motion (VIps and VCont) precedes saccades during flight within a textured background but not within a uniform background. The scaling of the y-axis is identical to that in B.

View larger version (46K): [in a new window]   Fig. 11. Large-field expansion may serve as a trigger for saccades. (A) The outputs of the horizontal motion detectors were spatially summed over each half of the two quadrants making up the frontal 180° of the fly’s field of view (regions 2 and 3 in Fig. 9). The difference between these two spatial sums represents the gross horizontal expansion within the region experienced by the fly (see Appendix for details). The dashed red lines indicate the focus of expansion, while the red arrows schematically represent large-field expansion. (B) Horizontal expansion (HExp,Ips and HExp,Cont) cannot alone serve as a saccade trigger. Gray lines indicate individual expansion traces, aligned at the initiation of the saccade; red lines indicate the mean value, and blue lines represent ±S.D., as in Fig. 10. The y-axis scaling is the same as in Fig. 10B, and the calculation of HExp,Ips and HExp,Cont is as described in the Appendix; there has been no normalization. During flight within a textured background, the fly experiences significant horizontal expansion on its ipsilateral side, but not on its contralateral side (upper). However, this horizontal expansion is absent during flight within the uniform background (lower). The traces come from the same set of saccades as those in Fig. 10. (C) Calculation of the vertical expansion (VExp,Ips and VExp,Cont) from the output of the local motion detectors. To determine vertical expansion, the outputs of the elementary motion detectors sensitive to vertical motion were summed over the top and bottom halves of each frontal quadrant (see Appendix). The difference between these two spatial sums represents the gross vertical expansion experienced by the fly. (D) Prominent vertical expansion preceded saccades during flight within both the textured (upper traces) and uniform (lower traces) backgrounds and was greater on the ipsilateral side. The y-axis scaling is the same as in B; there has been no normalization.

View larger version (22K): [in a new window]   Fig. 12. The sum of the vertical and horizontal expansions (VExp+HExp; see Appendix) is similar prior to saccades in both the textured and the uniform background. The sum of the average vertical and horizontal expansions (from Fig. 11) is shown for both the textured (red) and the uniform (blue) backgrounds. Mean ± standard deviations are shown by the solid and dashed lines, respectively. The total expansion signals correspond well for the textured and the uniform backgrounds despite the differences in velocities and distance from the walls in the two conditions. The data were collected over the same set of saccades as Figs 10 and 11. The y-axis has the same scaling as in Figs 10 and 11.

View larger version (20K): [in a new window]   Fig. 13. Model for visual control of free flight behavior in Drosophila melanogaster. As a fly moves through its environment, a two-dimensional array of motion detectors estimates optic flow (top). The local measurements of optic flow are summed as a rough measure of the image expansion on each side of the fly. The estimates of image expansion are then integrated with respect to time, t. When the time-integrated expansion signal on one side exceeds a threshold, a saccade away from that side is initiated. The time-integrated expansion signal inhibits saccades on the ipsilateral side, preventing a saccade in the opposite direction from quickly following the initial saccade. See Discussion for further details.