Saccadic body turns in walking Drosophila

Abstract

Drosophila melanogaster structures its optic flow during flight by interspersing translational movements with abrupt body rotations. Whether these "body saccades" are accompanied by steering movements of the head is a matter of debate. By tracking single flies moving freely in an arena, we now discovered that walking Drosophila also perform saccades. Movement analysis revealed that the flies separate rotational from translational movements by quickly turning their bodies by 15 degrees within a tenth of a second. Although walking flies moved their heads by up to 20 degrees about their bodies, their heads moved with the bodies during saccadic turns. This saccadic strategy contrasts with the head saccades reported for e.g., blowflies and honeybees, presumably reflecting optical constraints: modeling revealed that head saccades as described for these latter insects would hardly affect the retinal input in Drosophila because of the lower acuity of its compound eye. The absence of head saccades in Drosophila was associated with the absence of haltere oscillations, which seem to guide head movements in other flies. In addition to adding new twists to Drosophila walking behavior, our analysis shows that Drosophila does not turn its head relative to its body when turning during walking.

Keywords: Drosophila; halteres; head body coordination; optic flow; saccades; visual acuity; walking.

Figure 1

Body trajectories of walking Drosophila. (A) Prototypical movement patterns (PMs) of adult Drosophila walking freely in a circular arena (56 male 57 female flies, recorded @ 500 fps). Colored arrows highlight the velocity combination that characterizes each PM, and gray arrows indicate the maximum speeds. The color code is given by the legend to the left. For each PM, its respective abundance in the data set is presented in percent, along with its average duration. (B) Distributions of the three velocities (thrust, slip, yaw) during translational movements and saccadic turns. Yaw velocities cluster around zero during translations but not during rotations. (C) Example of a single trajectory. Circles mark the center of mass of the animal and lines depict the long axis of its body. To facilitate following the trajectory, gray scales indicate time. Dashed boxes highlight three saccades. (D) Yaw angles and velocities of the trajectory in (B) plotted against time. Orange rectangles mark the three saccades that are highlighted in panel B. (E) Mean velocity of 1885 individual saccades, identified by using a yaw velocity of 200 deg^*s⁻¹ as the threshold criterion and arranged so that their peak velocity is at 0 ms. Leftward and rightward turns were separated prior to the analysis, yielding velocity profiles for each of them that are virtually mirror-symmetric. (F) Corresponding yaw angles documenting that, within the 100 ms time window, the flies turned by on average 15°. (G) Distribution of saccade durations in milliseconds.

Figure 2

Head movements during saccadic turns. (A) Snapshots of a fly turning around the right angle in the labyrinth (top) and fitted head and thorax templates (bottom) used to deduce their respective orientations. (B) Example trace of the yaw velocities (top) and yaw angles (bottom) of the head (solid blue lines) and body (dashed blue lines) of a fly walking through the labyrinth. Head and body were traced separately by two different investigators (head: B.G., thorax: P.J.). (C) Average yaw velocities (top) and yaw angles (bottom) obtained for 114 saccades observed in the labyrinth. Colored areas depict the 95% confidence intervals. (D) Histogram of yaw angle amplitudes during saccades (dark blue: body, light blue: head). (E) Distribution of the peak yaw velocities during saccades (color code as in D). (F) Distribution of the time lapse between the velocity peak of head and body during the saccades.

Figure 3

Comparison of the head and body movements of walking Drosophila, walking blowflies (“Calliphora”), and flying honey bees (“Apis”). (A) Respective average yaw velocities during saccades. Note that for bees only the probability density is shown. (B) Average yaw angles (top) of the head and body and the difference between them (bottom) during saccadic body rotations. (C) Distributions of the angles between head and body (the ϕ-angles) observed during the entire trajectories, including saccades, and the trajectories between them. (D) Correlation coefficients between the yaw angles of the head and the body during the saccades. Calliphora is not included in this panel since no such data is available for this species. Data for Apis was taken from Boeddeker (2010) and data for Calliphora from Blaj and van Hateren (2004).

Figure 4

Retinal inputs and image shifts. (A) Voronoi cells computed for the eyes of Drosophila, Apis, and Calliphora (top row), and respective retinal images (subsequent rows) deduced for three different images (left). The image in the lower row was taken by Janne Voutilainen (for a complete list of the images used, see Supplemental Materials). Note that for Calliphora, only the central field of view is covered (for data sources, see Materials and Methods). (B) Mean ommatidial luminescence difference, caused by shifting sinusoidal stripe patterns with different sine periods by half a sine period. The differences were normalized to the maximal pixel wise difference of the original images and plotted against the sine period. (C) Mean ommatidial luminescence difference caused by shifting images depicting a naturalistic scenes in steps of 0.1° around the animal from −180 to +180° (for images, see Supplementary Figure 1). The differences were normalized to the corresponding pixel wise difference of the image and plotted against the rotation angles. Lines: means; transparent areas: 95% confidence intervals. A zoomed in version of the data in the dashed box is plotted in Figure 4D. For respective data obtained with artificial images with an 1/f spatial distribution, see Supplementary Figure 2). (D) Close-up from panel C. Note that Drosophila generates a smaller ommatidial luminescence difference by turning by more than 15° (as seen during the body saccades) than Calliphora generates by turning about 4° (as seen during a Calliphora head saccade).

Figure 5

Absence of haltere oscillations. (A) Percentage of flies oscillating their halteres under different conditions (free walking, N = 9; tethered walking, N = 6; tethered flying, N = 6; after landing, N = 3; after take-off, N = 3). (B) Time delay between the last tarsus leaving the ball (“take off on ball”) or the first tarsus touching the ball (“landing on ball”) and the respective on- and offsets of haltere oscillations (N = 3 each, means ± 1 SD).