First published online November 24, 2003
Journal of Experimental Biology 207, 113-122 (2004)
Published by The Company of Biologists 2004
doi: 10.1242/jeb.00724
Spatial organization of visuomotor reflexes in Drosophila
Lance F. Tammero1,*,
Mark A. Frye2,*,
and
Michael H. Dickinson2
1 Bioengineering Graduate Group, University of California, Berkeley, CA
94720, USA
2 Bioengineering, California Institute of Technology, Pasadena, CA 91125,
USA
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Fig. 1. Responses to large-field motion stimuli presented in open-loop conditions.
At the onset of image motion, the fly generates a bilateral change in wing
stroke amplitude that is highly correlated with yaw torque. (A) Uniform
rotation across the entire visual field elicits a turning response in the same
direction as the stimulus. (B) Motion confined to the front half of the visual
field elicits a larger response compared with the full-field stimulus. (C)
Motion across the rear visual field elicits a turning response in the opposite
direction. The sum of separate front and rear field responses (dotted red
lines in A) closely approximates the full-field response. (D) A lateral
expansion/contraction stimulus with motion in opposite directions in the front
and rear visual fields elicits the largest turning response. The dotted red
line shows the sum of the responses to individual stimuli indicated in B and
C. Each trace represents mean ± S.D. (shaded area)
(N=10). In all cases, contrast frequency changed from 0
s–1 to 10 s–1 according to the motion
stimulus trace. The scale bars indicate 1 V for the wingbeat amplitude and
10–8 N m for torque. Wingbeat amplitude signals were
normalized (see Materials and methods). (E) Effect of rear field contrast
frequency on turning response, measured from changes in wing stroke amplitude.
Contrast frequency in the front field was held constant at 10
s–1 while the value in the rear field varied from –10
s–1 to 10 s–1. Negative values indicate
motion in the same direction as the front field. Data points represent the
mean values of the response ± S.D. (N=10). (F)
Turning response amplitude varies with the azimuth of the focus of expansion
(N=5). From –100 deg. s–1 to 100 deg.
s–1, the turning response varies sigmoidally with the
location of the focus of expansion. The response attenuates as the focus of
expansion moves into the animal's rear field of view.
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Fig. 2. The effect of contrast frequency on the front and rear field turning
responses. The mean response amplitudes ± S.E.M. for front
(open symbols; N=12) and rear (black symbols; N=13) field
motion reach a maximum at a contrast of 10 s–1 and 6.7
s–1, respectively. Doubling the spatial period of the pattern
(gray symbols; N=8) results in a shift in the contrast frequency
optimum. No response reversal indicative of aliasing was found within the
tested range of spatial and temporal frequencies.
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Fig. 3. Flies show similar responses to individual elements of the
expansion/contraction pattern. Data (including scale bar) presented as in
Fig. 1. (A) Mean responses to
full-field expansion/contraction. (B) Responses to a pattern of translation
without motion in the lateral fields of view produce expansion avoidance
responses similar to the full-field pattern. (C) Responses to the focus of
expansion and (D) contraction. For comparison, assuming bilateral symmetry,
data from Fig. 1C are inverted
and re-plotted here (inset). The sum of the responses shown in C and D (dotted
red line in A) approximates full-field expansion/contraction responses
(N=10).
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Fig. 4. Turning responses to motion in the rear quarter-fields are
non-directionally selective. Motion across the front half-field (A) or the
constituent quarter-fields (B,C) generates turning responses that follow the
sign of image motion (D). Front quarter-field motion produces saturated
responses, thus the sum of responses (dotted red line in A) exceeds responses
to half-field motion. (E) Motion across the rear half-field generates
counterdirectional turning responses. However, responses to motion restricted
to constituent quarter-fields show a sign inversion (F,G). Both clockwise and
counterclockwise motion centered in a rear quarter-field triggers clockwise
turns (G,H). Assuming bilateral symmetry, data from F are inverted and
re-plotted here. As a consequence, the sum of rear quarter-field responses
(dotted red line in E) does not approximate the response to half-field motion.
This indicates non-linear processing of binocular motion information in the
rear part of the visual field.
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Fig. 5. Flies maintain better closed-loop control of an expansion/contraction
pattern than a full-field rotatory pattern. The fly controls the direction and
velocity of either a full-field rotational (A) or a lateral
expansion/contraction pattern (B) by adjusting the difference between left and
right wing stroke amplitude. (C) The fly's ability to hold the pattern steady
is reflected by the variance in the position over a series of 1 s windows. (D)
A sinusoidal bias is added to the feedback signal to challenge the fly's
ability to control the pattern. The variance in position is much larger when
the fly controls the position of a rotational pattern when compared to the
expansion/contraction pattern.
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Fig. 6. In closed-loop conditions, flies show a powerful steady-state expansion
avoidance reflex. By adjusting the difference between the right and left wing
stroke amplitude, flies control the azimuth of (A) a random checkerboard
pattern (N=27), (B) a single vertical stripe (N=27) and (C)
the poles of a constantly expanding/contracting pattern of vertical stripes
(N=13). For each experimental treatment, example responses are
plotted in the left column (i), time series averages are plotted in the center
column (ii; indicated in grayscale) and total probability distributions are
plotted in the right column (iii). For the grayscale plots, the white area
indicates that flies maintained the rotating pattern in that particular
position. On average, flies do not show preference for any single element of
the random checkerboard pattern, whereas they tend to fixate the vertical
stripe in front (0°). Flies show even more robust fixation of the poles of
expansion/contraction. There is less variability in the fly's tendency to
stabilize the poles of the expanding pattern in the rear field of view, thus
the pole of contraction is fixed frontally.
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Fig. 7. Delay and steady-state balance of the expansion avoidance reflex depend
upon the contrast frequency of large-field image motion. Flies had closed-loop
control over the yaw position of the poles of expansion/contraction, while a
pattern of stripes drifted at constant velocity. We periodically challenged
the fly's closed loop responses to image expansion/contraction by reversing
the drift direction, therefore exchanging the position of the two poles. (A)
At each direction reversal, flies rapidly turn away from the pole of expansion
to fixate the pole of contraction frontally. In this figure, drift direction
is indicated by the polarity of the stimulus waveform. Dashed lines indicate
pole positions along the y-axis. (B) Either doubling the drift
velocity or (C) halving the functional wavelength of the pattern on one half
of the arena resulted in a 20° shift in fixation towards the side of the
arena showing the slower drift speed. (D) Increasing the drift velocity
results in shorter delay to the onset of steady-state responses
(N=13; ANOVA, F=14.7, P<0.01).
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Fig. 8. Schematic model for the spatial organization of visuomotor reflexes in
Drosophila. Image motion within individual quarter-fields is
temporally filtered and spatially summed (see text for details). Motion across
the frontal visual hemisphere results in a syndirectional turn, whereas motion
in the rear results in a counterdirectional turn. By summation, full-field
rotation results in a weak syndirectional turn. However, a pattern of
expansion centered laterally produces a stronger turn away from the focus of
expansion. Note that the polarity of turning responses to motion within the
rear quarter-fields is independent of the direction of image motion.
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© The Company of Biologists Ltd 2004
