FlyingDrosophilamaintain arbitrary but stable headings relative to the angle of polarized light

Abstract

Animals must use external cues to maintain a straight course over long distances. In this study, we investigated how the fruit fly selects and maintains a flight heading relative to the axis of linearly polarized light, a visual cue produced by the atmospheric scattering of sunlight. To track flies' headings over extended periods, we used a flight simulator that coupled the angular velocity of dorsally presented polarized light to the stroke amplitude difference of the animals' wings. In the simulator, most flies actively maintained a stable heading relative to the axis of polarized light for the duration of 15 min flights. We found that individuals selected arbitrary, unpredictable headings relative to the polarization axis, which demonstrates that can perform proportional navigation using a polarized light pattern. When flies flew in two consecutive bouts separated by a 5 min gap, the two flight headings were correlated, suggesting individuals retain a memory of their chosen heading. We found that adding a polarized light pattern to a light intensity gradient enhanced flies' orientation ability, suggesting use a combination of cues to navigate. For both polarized light and intensity cues, flies' capacity to maintain a stable heading gradually increased over several minutes from the onset of flight. Our findings are consistent with a model in which each individual initially orients haphazardly but then settles on a heading which is maintained via a self-reinforcing process. This may be a general dispersal strategy for animals with no target destination.

Heading choices of flyingDrosophilaunder changing angles of polarized light

“…Our experiments show that well-performing flies show a clear tendency to maintain their chosen heading, even when interrupted by a period of unpolarized stimulation. These data again provide independent support for previous studies 18 and reinforce the idea that a generalist fly like Drosophila melanogaster is indeed capable of using skylight polarization for maintaining a chosen course over longer times, which is crucial for achieving more complex navigational tasks [19][20][21] . Like previous studies, we aimed at quantifying the quality of behavioral responses, since we expected Even after tight control of food quality, rearing conditions, temperature, and humidity, the flies' cooperation in these experiments remains unpredictable.…”

“…In addition, the celestial pattern of linearly polarized light serves as an attractive orientation cue that many insects use 2,40,41 . Spontaneous behavioral responses of both walking and flying Drosophila to linearly polarized light ('polarotaxis') have been demonstrated in the past, using both population assays, as well as single fly assays [16][17][18]22,33,42,43 . In all these experiments, much care was given to the control and avoidance of intensity artifacts that can result in behavioral decisions that are in fact independent of the linearly polarized component of the stimulus (reviewed in 15 ).…”

“…Oriented flights of suspended monarch butterflies under a polarized stimulus have been demonstrated, yet its ethological significance remains somewhat controversial, due to conflicting reports [12][13][14] . Probably the most valuable recent progress comes from the fly Drosophila melanogaster: spontaneous responses of flying Drosophila to linearly polarized light using virtual flight arenas have been demonstrated, both under the natural sky, as well as using an artificial stimulus generated in the laboratory using commercially available polarization filters 15 , [16][17][18] . Most importantly, flies were shown to choose arbitrary angular headings with respect to the orientation of the e-vector of the polarized stimulus and showed the tendency to maintain this navigational decision over several minutes, even when the stimulus presentation was perturbed for several minutes 18 .…”

Walking Drosophila aim to maintain a neural heading estimate at an internal goal angle

“…The flies sometimes also changed heading either abruptly or gradually over time (Figure 1B, center and right). Although previous studies have noted that Drosophila tend to fixate vertical stripes directly in front (22)(23)(24)(25), the arbitrary-angle fixation we observed in our setup better resembles previous reports of flies maintaining an arbitrary heading relative to a visual object (menotaxis) (26) or to the angle of polarized light (27,28), and is reminiscent of dispersal behaviors observed in the wild (29,30). We have yet to fully characterize the specific experimental conditions that promote front-fixation vs. arbitrary-angle fixation in walking flies (see Behavioral conditions in Methods), but all genotypes we studied reliably performed arbitrary-angle fixation in our setups, allowing us to examine how this behavior is implemented at the neural level.To quantify the flies' headings over time, we treated each heading measurement in a walking fly as a unit vector, computed the mean of unit vectors over 60 s windows ( Figure 1C), and visualized the distribution of 60-s mean vectors in a polar plot ( Figure 1D, see Methods).…”

Building a heading signal from anatomically defined neuron types in the Drosophila central complex

“…Behavioral experiments have argued that flies can navigate to remembered 2D locations in space [41,49]. Flies can also effectively disperse far from a start location by traveling along a constant, but arbitrary, angular direction for seconds to hours [50–53]. To perform either such task, flies must, at each moment in time, ultimately choose an angle at which to walk or fly, which can be considered the instantaneous goal angle of the fly.…”