QUICK SEARCH:   [advanced] Author: Keyword(s):
Home     Help     Feedback     Subscriptions     Archive     Search     Table of Contents

First published online November 19, 2007
Journal of Experimental Biology 210, 4092-4103 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.006502

This Article Summary Full Text Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Services Email this article to a friend Related articles in JEB Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Budick, S. A. Articles by Dickinson, M. H. Search for Related Content PubMed PubMed Citation Articles by Budick, S. A. Articles by Dickinson, M. H.

The role of visual and mechanosensory cues in structuring forward flight in Drosophila melanogaster

Seth A. Budick^1,*, Michael B. Reiser^2, and Michael H. Dickinson^1,3,

¹ Division of Biology, California Institute of Technology, Pasadena, CA 91125, USA
² Computational and Neural Systems, California Institute of Technology, Pasadena, CA 91125, USA
³ Bioengineering, California Institute of Technology, Pasadena, CA 91125, USA

View larger version (12K): [in this window] [in a new window]   Fig. 1. A schematic view of the visual arena. The arena had a circumference of 160 rows and a height of 24 rows of LEDs with 24 columns removed at the up- and downwind ends to allow smooth airflow over the fly. Flies were glued to a steel pin, positioned between two magnets, allowing rotation around the functional yaw axis. A camera positioned below the tunnel visualized the fly at 100 Hz through a hole in the center of a set of ring magnets.

View larger version (44K): [in this window] [in a new window]   Fig. 2. Loosely tethered D. melanogaster orient upwind. (A) Flies randomly presented with wind velocities between 0 and 1.0 m s–1 orient progressively more tightly around 0° (upwind) with increasing wind velocity. The heavy black lines indicate the time course of wind velocity. (B) Orientation changes were quantified by an orientation response metric. The mean circular orientation was calculated over the first 100 ms (initial orientation) and the final 2 s (final orientation) of each trial. Orientation response is then given by |initial orientation|–|final orientation|. For example, a fly responded to the onset of a 0.2 m s–1 wind by turning from an initial angle of –150° to a final angle of –12°; an orientation response of 138° (red arrows). In the absence of wind, the same fly turned from –140° to –169°; an orientation response of –29° (blue arrows). (C) Plotting orientation response as a function of the absolute value of the initial orientation provides evidence for orientation to wind (arrowheads indicate the fly whose responses are shown in B). Responses falling along the upper solid line represent perfect upwind orientation, while those along the lower line indicate responses diametric from upwind. (D) A second metric, the response index, quantified responses independently of initial orientation. The response index was calculated as (90° – |final orientation|)/90° where +1 indicates a response with a final orientation of 0°, –1 corresponds to a final orientation of 180° and 0 indicates a response with a final orientation of ±90°. The response index is thus (90°–12°)/90°=0.86 for the fly represented by the red arrows in B (dashed line indicates response index = 0). (E) Response index varied significantly with wind velocity between 0.2 and 1.0 m s–1, with responses at all velocities being significantly greater than in no wind.

View larger version (27K): [in this window] [in a new window]   Fig. 3. A passive aerodynamic response is apparent with increasing wind velocity. Dead flies with their wings intact and, to a lesser extent, dead flies without wings also evinced an orientation response to wind onset.

View larger version (21K): [in this window] [in a new window]   Fig. 4. Orientation responses were much more pronounced in live flies, particularly at low wind velocity. Plotting orientation response as a function of |initial orientation| makes it apparent that responses in dead flies without wings were quite small, even at high wind velocity, while dead flies with intact wings manifested moderately strong orientation, especially at the highest wind velocities.

View larger version (8K): [in this window] [in a new window]   Fig. 5. Response index scores permit a decomposition of the active and passive responses. (A) Response index scores were significantly higher in live flies (asterisks) than in dead, winged flies at velocities below 0.8 m s–1. (B) The percentage of the response attributable to the aerodynamic effects of wings was quantified by subtracting the mean response index for dead wingless flies from the corresponding values for dead, winged flies and dividing by the mean, dead, winged response (filled circles). The effect of the live behavioral response was similarly quantified from the responses of live flies and dead, winged flies (open circles).

View larger version (24K): [in this window] [in a new window]   Fig. 6. Saccades play a role in the active behavioral response. Saccades were quantified as turns with magnitudes greater than 15° and angular velocities exceeding 300° s–1. (A) An orientation trace from a fly orienting in a 0.6 m s–1 wind manifests two rapid turns. (B) An angular velocity trace of the same data as in A, illustrating the spikes in angular velocity that characterize saccades. (C) In live flies, spontaneous saccades (i.e. those exhibited in the absence of wind) were distributed throughout the trial (note that the histograms are stacked). Furthermore, those that improved the flies' orientation relative to upwind (blue bars) did not predominate compared with those that turned the flies away from upwind (red bars). In the presence of wind, saccades tended to cluster near the onset of the wind stimulus and also tended to improve the orientation relative to upwind. In dead flies, saccades were very rare under all conditions.

View larger version (50K): [in this window] [in a new window]   Fig. 7. Antennal immobilization greatly reduces the orientation response. (A) Orientation traces from flies that had their antennae glued, either unilaterally or bilaterally, indicate a decrement in orientation ability. (B) At 0.2 m s–1, orientation was not significantly different from baseline in bilaterally glued flies (t=0.24, d.f.=31, P=0.49), or in flies with the right (t=–2.77, d.f.=25, P=0.055) or left (t=–0.35, d.f.=28, P=0.37) antennae unilaterally glued. Control flies, however, did orient significantly better than baseline at the lower velocity (t=–4.84, d.f.=26, P<0.001). At 1.0 m s–1, all groups oriented significantly better than baseline (non-glued: t=–5.26, d.f.=26, P<0.001; right antenna glued: t=–4.04, d.f.=25, P<0.001; left antenna glued: t=–3.61, d.f.=28, P<0.001; both antennae glued: t=–3.65, d.f.=31, P<0.001). (C) The percentage of the response attributable to a single JO was quantified by subtracting the mean response index for bilaterally glued flies from the corresponding mean values for flies with one antenna glued and dividing by the unilaterally glued response (filled circles). The effect of the second JO was similarly calculated from the responses of non-glued flies and the mean unilaterally glued responses (open circles).

View larger version (26K): [in this window] [in a new window]   Fig. 8. Flight orientation was quantified in response to competing wind and visual stimuli. Flies were presented with 39 different combinations of wind velocity, expansion rate and orientation of the expansion pattern. (A) Exemplar responses are shown to a striped pattern expanding at a temporal frequency of 1.0·Hz, from a focus of expansion (FOE) at ±90°, in the absence and presence of a 0.6 m s–1 wind [location of the focus of contraction (FOC) is indicated by the red bar, orientation favored by wind is indicated by the blue bar]. (B) To quantify the preference for the visual or wind stimulus, the number of instantaneous heading vectors in each trial that fell within ±45° of 0° (blue shaded area) was divided by the total number falling within ±45° of 0° and ±45° of the FOC (red shaded area). This yielded a preference index between 1 (wind preferred) and 0 (FOC preferred). In B, the arrows represent the mean orientation vectors of each fly in A over the full 5 s trial.

View larger version (142K): [in this window] [in a new window]   Fig. 9. Both the visual and wind stimuli shaped fly orientation. The orientation predicted by a preference for wind is indicated by the blue bars and that predicted by FOC orientation is indicated by the red bars. Each row represents a change in the location of the FOC with the bottom row corresponding to the orientation behavior measured while the visual arena was dark. Numerical values above and to the right of the labeled panels are mean preference indices ±s.d. Orientation could, in general, be described as a compromise between the two competing stimuli with orientation being increasingly biased towards the wind with increasing wind velocity, and increasingly favoring the FOC with increasing expansion velocity.

View larger version (9K): [in this window] [in a new window]   Fig. 10. Saccades were employed, as with the wind stimuli (Fig. 6) to orient flies towards an attractive visual stimulus. A visual pattern expanding at 5 Hz in the absence of a wind stimulus tended to elicit saccades that oriented flies towards (blue bars) rather than away from the FOC (red bars), particularly at the beginning of the trial (note that histograms are stacked). Flies also exhibited a large number of saccades towards the end of trials with expansion rates of 5 Hz, particularly when the FOC was at either the up- or the downwind ends of the arena.