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First published online July 14, 2008
Journal of Experimental Biology 211, 2478-2485 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.018879
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Context-dependent olfactory enhancement of optomotor flight control in Drosophila

Dawnis M. Chow* and Mark A. Frye

Department of Physiological Science, University of California, Los Angeles, CA 90095-1606, USA


Figure 1
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Fig. 1. Visual and olfactory stimuli were delivered to a fly tethered within a computer-controlled flight-simulator modified with odor delivery. (A) The tethered fly was suspended in the center of a cylindrical array of LEDs. Mass-flow-regulated water or apple-cider vinegar vapor was delivered to the antennae and removed continuously with a gentle vacuum to produce a continuous plume. (B) Flies were presented with wide-field patterns of rotation and expansion stimuli. Space-time plots indicate the movement in time of one representative horizontal row of the visual display. FOE, focus of expansion; FOC, focus of contraction.

 

Figure 2
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Fig. 2. Attractive odorant decreases steering variance and increases visual stability under closed-loop control. (A) Flies showed a decrease in mean {Delta}WBA variance under the influence of odor (expansion P<0.001, rotation P<0.05, paired t-test) and (B) a corresponding decrease in mean image velocity (P<0.001, paired t-test), indicating increased visual stabilization. (Flicker, N=64; SF stripe, N=64; WF expansion, N=100; WF rotation, N=106). (*P<0.05, ***P<0.001). (C) {Delta}WBA responses were binned and sorted by increasing ({Sigma}WBAxWBF)3. The inset shows the variance calculated from {Delta}WBA responses plotted against power.

 

Figure 3
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Fig. 3. Rotational optomotor responses are enhanced and expansion-avoidance optomotor responses are suppressed under the influence of attractive odor. (A) Example raw {Delta}WBA responses evoked by five rotation and expansion stimuli either in the presence of odor (red) or without odor (blue). (B) Odor increased the mean amplitude of rotational optomotor responses but decreased the mean expansion amplitude (N=46, *P<0.05, **P<0.01, paired t-test). (C) This is the same as (B) but separated by each one-second visual-stimulus presentation. There was no significant time-course effect (two-factor repeated measures ANOVA, odor P<0.05, time P>0.05). Note: within-subjects design eliminates the need for error bars. R/Rmax is the normalized response magnitude (see text for details).

 

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Fig. 4. Attractive odorant influences the probability of a reflexive landing response. (A) Image sequence depicts the leg extension of a typical landing response evoked by a rapidly expanding visual object. (B) The probability of landing was decreased by attractive odorant at all azimuthal positions except directly in front of the fly (N=14, P<0.01, two-factor repeated measures ANOVA).

 

Figure 5
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Fig. 5. The combination of enhanced rotation responses and suppressed expansion responses persists under conditions in which the fly has active control of image motion. (A) An example position trace shows the small remnant of a sinusoidal bias added to the control of the fly over the arena heading. (B) Top, mean {Delta}WBA responses with odor (red) and without odor (blue) (N=43). Bottom, the frequency-modulated stimulus position waveform of the imposed bias. (C) Mean peak-to-peak response amplitude for each consecutive stimulus epoch. The response amplitude was quantified and tested statistically using fitted sine functions. {Delta}WBA response amplitudes were significantly enhanced by odor at all frequencies for rotation (two-factor repeated measures ANOVA, P<0.001) but were only suppressed significantly between 2 Hz and 8 Hz for expansion (two-factor repeated measures ANOVA, P<0.05).

 

Figure 6
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Fig. 6. Olfactory cues increase the salience of visual stimuli. (A) The example optomotor response trace (black) and optimized sine-fit for each frequency epoch (pink). (B) Mean r-squared values for each stimulus epoch with and without odor.

 

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© The Company of Biologists Ltd 2008