First published online November 24, 2003
Journal of Experimental Biology 207, 123-131 (2004)
Published by The Company of Biologists 2004
doi: 10.1242/jeb.00725
Motor output reflects the linear superposition of visual and olfactory inputs in Drosophila
Mark A. Frye* and
Michael H. Dickinson
Bioengineering, California Institute of Technology, Pasadena, CA
91125, USA
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Fig. 1. Experimental apparatus to examine sensorimotor interactions in
Drosophila. (A) A fly is tethered beneath an infrared diode that
casts a shadow of the beating wings onto an optoelectronic wingbeat analyzer
(red). The output of the analyzer is coupled with the rotational velocity of
the pattern displayed on the wraparound LED screen (green) such that the fly
has closed-loop control of the visual panorama. (B) System to deliver a
continuous stream of saturated vapor onto the antennae. A computer-controlled
solenoid valve shunts a mass-flow-regulated air supply to either a vial of
distilled water (experimental control) or a vial of dilute vinegar solution.
(C) A pattern of vertical stripes appears to expand from the right and
contract to the left of the fly. The velocity of expansion/contraction is in
closed-loop such that if the expansion appeared from the right, a turn to the
left would reduce the velocity of expansion and vice versa. To
examine the strength of visual reflexes, with and without odor, we perturbed
the fly's closed-loop control of the expansion/contraction stimulus by adding
a 1.25-s bias to the feedback loop (see Materials and methods).
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Fig. 2. Visual and olfactory stimuli evoke robust, repeatable, motor responses. (A)
Sample responses to a regime of 1.25-s visual bias, 10-s odor and both stimuli
presented simultaneously. Onset of stimuli is indicated in last two rows. (B)
Time series averages to multisensory stimulus patterns. Gray fill shows the
envelope of S.D. (C) Time-expanded responses. The shaded regions in
the last two rows of A and B correspond to the data presented in C and D.
Sample responses from A (indicated by thin black lines) are overlaid with mean
responses from B (indicated by thick red lines). The arrow in column (i)
indicates phasic modulation of image velocity (see text). The arrow in column
(ii) highlights a transient decrease in WBA at the onset of the odor pulse
(see text). (D) Odor did not alter the mean responses to imposed bias during
closed-loop control of a single vertical stripe (i; N=10), a rotating
random checkerboard pattern (ii; N=10) or an expanding flow field
centered laterally (iii; N=10). Rv, response to
visual stimulus; Ro, response to olfactory stimulus;
Rv+o, response to visual and olfactory stimuli
simultaneously.
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Fig. 3. Odor does not alter the magnitude or time course of steady-state collision
avoidance reflexes in closed-loop conditions. Flies were presented with a
2.5-s bias in expansion, with and without concomitant presentation of 30-s
odor pulses. Each trace represents a time series average. Each fly received
three visual trials within each of nine consecutive odor trials (N=16
flies).
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Fig. 4. During the duration of an odor pulse, motor responses to visual and
olfactory cues represent the linear superposition of responses to each
stimulus presented alone. Data sets are segregated into responses to visual
bias during control water vapor delivery (i; Rv), odor in
the absence of visual bias (ii; Ro), both stimuli
simultaneously (Rv+o; indicated by black lines, iii), and
the sum of responses to each stimulus presented alone (Rv
+ Ro; indicated by red lines, iii). N=22.
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Fig. 5. Visual feedback alters the time course of the odor-off response. (A) Time
series average of closed-loop control without either visual bias or odor. (B)
Average odor responses without visual bias (black lines) decay along a slower
time course compared with odor responses coupled with impulsive visual bias
(red lines). N=22. Rb, response to baseline;
Roo, response to odor-off; Roo+v,
response to odor-off and visual bias.
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Fig. 6. Unbiased closed-loop visual feedback is sufficient to alter the time course
odor-off responses. Flies were presented with 30-s odor pulses. Time series
averaged responses to odor presented during visual closed-loop conditions (red
lines) decay more rapidly between odor pulses (example highlighted with
arrows) than odor responses in the absence of any visual motion (black
lines).
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Fig. 7. A schematic model to describe neural mechanisms by which multisensory input
is linked to motor output. Visual (blue) and olfactory (red) feedback projects
along separate neural pathways to the flight motoneurons of the thorax.
Olfactory feedback is selectively targeted to the motoneurons of both the
indirect power muscles and constitutively active steering muscles –
resulting in tonic elevation in wingbeat frequency (WBF) and sum of wingbeat
amplitude ( WBA) in response to odor. Visual feedback activates steering
muscles that initiate rapid, phasic changes in wingbeat amplitude resulting in
collision avoidance maneuvers. The superposition of both motor responses could
alter body posture or heading to bias flies' overall flight trajectory towards
visual features associated with attractive odorants.
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© The Company of Biologists Ltd 2004
