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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
Context-dependent olfactory enhancement of optomotor flight control in Drosophila
Department of Physiological Science, University of California, Los Angeles, CA 90095-1606, USA
* Author for correspondence (e-mail: dmchow{at}ucla.edu)
Accepted 28 May 2008
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Summary |
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 TOP Summary INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Key words: olfaction, vision, motor control, multisensory, integration, sensory function
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INTRODUCTION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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; Fares et al.,
1980; Vickers,
2000; Vickers et al.,
2001). Furthermore, unlike visual or acoustic stimuli, odors
contain no spatial information. Animals such as moths and flies meet these
challenges by integrating more-reliable visual information to stabilize their
wind-borne heading and plume position
(Gilbert and Keunen,
2008).
Flying creates two general types of optic-flow over the retina: wide-field
image rotation generated during steering maneuvers, and translation generated
during straight flight. Insects turn syn-directionally with a rotating
panorama to minimize the drift of the visual world and thereby correct
unintended deviations in course
(Götz, 1968;
Götz, 1975;
Hassenstein and Reichardt,
1956; Robert,
1988). By contrast, lateral visual expansion generated while
approaching stationary objects triggers rapid evasive turns called
body-saccades – sharp high-velocity turns thought to be functionally
analogous to gaze-stabilizing eye movements in humans
(Tammero and Dickinson,
2002b). Rotational stability and expansion-triggered saccades are
thought to be necessary for straight flight and collision avoidance,
respectively (Collett, 1993; Tammero and
Dickinson, 2002b). The spatial, temporal and contrast-response
properties associated with each type of flow-field suggest that separate
pre-motor control circuits mediate expansion and rotation optomotor flight
behaviors (Duistermars et al.,
2007a), and the expansion control system is further subdivided
into parallel pathways for landing and avoidance of collisions
(Tammero and Dickinson,
2002a).
Despite the sophisticated role of vision in flight control, the visual
resolution of compound eyes is rather poor. Over a century ago, vision
scientists imagined that such eyes "...[give] a picture about as
good as if executed in rather coarse wool-work and viewed at a distance of a
foot" (Mallock,
1894). The spatial resolution of the fly visual system is three
orders of magnitude worse than that of humans
(Land and Nilsson, 2002) and
thus presents a problem for the flying animal: fruit flies cannot visually
discriminate food sources at any appreciable distance.
An odor plume can be fragmented, but it is identifiable at a distance and
triggers robust motor responses. Behavioral studies with Drosophila
have disclosed immediate bilateral increases in wing-beat frequency (WBF) and
wing-beat amplitude (
WBA) upon exposure to attractive odorant, and a
dependence of response kinetics on visual feedback
(Frye and Dickinson, 2004;
Budick, 2007). In free flight
and tethered flight, these visually independent changes in wing kinematics are
integrated with visual feedback to enable a fly to navigate to an odor source
(Duistermars and Frye, 2008;
Frye et al., 2003). As
rotational signals are used to stabilize flight heading, and expansion cues
mediate collision avoidance and landing, we posit that olfactory signals have
a context-dependent influence on these optomotor behaviors. Here, we report
that attractive odorant enhanced the ability of a fly to control visually its
heading by increasing sensitivity to rotational motion but reduced sensitivity
to expansion signals. Finally, flies showed better tracking of experimentally
imposed image motion in the presence of olfactory cues, suggesting an
olfactory-mediated increase in visual salience.
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MATERIALS AND METHODS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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WBA
(Budick and Dickinson, 2006;
Frye and Dickinson, 2004), but
with considerable inter-individual variation characteristic of olfactory
behavioral experiments. Here, we sought to examine the influence of odor on
optomotor behaviors, and thus the crucial prerequisite is active odor
responses. Therefore, data from individual flies were software selected for
the experimental set if, in response to odor, WBF increased by half a standard
deviation during a 5-s test odor pulse at the beginning of each experiment,
and samples were thereafter excluded only if they stopped flying during the
trial. 57% of the animals that successfully completed a trial (167 out of 293
individuals) increased WBF during the test pulse and were included in the data
set.
Flight arena and olfactory delivery
We used an electronic LED flight simulator equipped with a video camera to
present visual cues, track wing motions and detect landing responses. The
arena was outfitted with a mass-flow-regulated odor-delivery system. The LED
arena geometry, visual display technology, camera system and odor control have
been described previously (Duistermars and
Frye, 2008; Frye and
Dickinson, 2004; Reiser and
Dickinson, 2008). Briefly, visual stimuli were computer controlled
on 48 individual 8x8 LED panel arrays arranged in a cylinder. A fly was
tethered in the center of the cylinder, and a diode cast a shadow of the
beating wings onto an optical sensor, which encoded amplitude and frequency
for each individual wing stroke (Fig.
1A). These values were digitized at 500 Hz (National Instruments
data acquisition PCI card, Austin, TX, USA) and stored on a computer using
Matlab (Mathworks, Natick, MA, USA).
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Experimental protocol
We examined visuo-olfactory integration in Drosophila melanogaster
with a two-part approach. First, the left-minus-right wing-beat amplitude
(
WBA) signal was coupled to the movement of the digital display,
allowing flies active `closed-loop' control over the visual panorama in a
manner consistent with free flight. Flies were challenged with `open-loop'
stimuli, over which they had no control. Open-loop test trials were
interspersed with closed-loop inter-test segments to ensure that the animals
remained actively engaged in optomotor control. Second, we combined the two
approaches in a `biased closed-loop' experiment. Under closed-loop control, a
periodic signal was added such that the flies had to compensate actively for
the imposed bias by steering (varying WBA) to stabilize image motion
(Frye and Dickinson, 2004;
Tammero et al., 2004).
We primarily used two types of experimental visual stimuli: wide-field
(panoramic) rotating and expanding motion. Expansion simulates a lateral body
translation, with the focus of expansion at 90° to the left of the fly and
the focus of contraction at 90° to the right of the fly, whereas
rotational motion simulates nontranslatory turning about the vertical axis.
Each wide-field pattern was generated using random checkerboards of nonuniform
spatial wavelength. Several studies show that multisensory enhancement is
greater when some of the component unimodal stimuli are weak
(Guo and Guo, 2005;
Meredith and Stein, 1986).
Thus, we used patterns of varying contrast in the closed-loop experiments in
order to assess responses to different stimulus strengths [for calculation and
calibration of contrast, see Reiser and Dickinson
(Reiser and Dickinson, 2008)].
In addition to wide-field patterns, we also presented several other visual
stimuli, including a dark bar on a bright background, 15° in width and
120° tall (subtended at the eye), which simulates a desired perch and thus
was actively fixated in the frontal field of view
(Maimon et al., 2008). A
flickering display rapidly reversed spatial contrast and thus formed a
no-motion control stimulus.
The first open-loop experiment consisted of an actively controlled
small-field stripe interspersed with wide-field open-loop expansion or
rotation. Contrast was set to an intermediate value (67%) for the wide-field
patterns. The expansion stimulus is an approximation of a translational flow
field, but angular velocity is constant across the azimuth in order to
maintain maximal similarity to the rotational stimulus. Thus, the expansion
and rotation stimuli were identical, except that, for expansion, the direction
of motion across the rear field of view was reversed. To examine landing
responses, flies were presented with a 7.5° dark square that expanded to
120° within 0.48 s, giving a rate of expansion of 250 deg.
s–1. The trajectory of object expansion followed a constant
velocity to maintain similarity to the expanding wide-field stimulus and
therefore did not represent the accelerating trajectory of a true looming
stimulus. Nevertheless, a prior study showed that constant-velocity expansion
elicits strong landing responses (Tammero
and Dickinson, 2002a), and the influence of spatio-temporal
variations in visual expansion on saccades has been examined by Bender and
Dickinson (Bender and Dickinson,
2006). The landing stimulus was presented at –120°,
–60°, 0°, 60° and 120° azimuthal position, where 0°
corresponded to the fixed heading of the fly. For the biased closed-loop
experiment, the flies were presented with either a wide-field expansion or
rotational pattern under closed-loop control with an added frequency-modulated
bias signal. The stimulus waveform was constructed from sine waves of fixed
amplitude and varying in frequency (1, 2, 4 and 8 Hz, each lasting 4, 4, 1.5
and 1 s, respectively). Therefore, the patterns were swept back and forth
along a sinusoid that increased in frequency, then decreased in frequency
along the same steps.
Undiluted commercial apple-cider vinegar served as the appetitive odorant. Air was either bubbled through aqueous vinegar or passed over a piece of filter paper saturated with vinegar. The two methods revealed no detectable response differences. Aliquots of vinegar were stored frozen; a new aliquot was used for each experiment. The odor stimulus was interspersed with the water vapor control such that the single plume port released a continuous mass-flow regulated stream of vapor onto the antennae. Odor was typically switched on at least two seconds before the onset of any visual stimuli and off at the end of each stimulus presentation. For each fly, each visual stimulus condition was presented before adding odor to prevent carry-over effects of odor on vision-only treatments. After each visual stimulus in open-loop experiments, flies were allowed at least 5 s of closed-loop control of the small-field stripe without the odor. Experiments were conducted in a random-block repeated-measures design, such that each fly received each stimulus in random order and only once.
Visual control signals, including azimuthal pattern-position, WBF,
WBA and WBA, along with the odor control sync signals, were
digitized at 500 samples s–1 and stored on a computer using
standard data-acquisition hardware. Visual stimuli, odor delivery, data
acquisition and video acquisition were controlled using custom Matlab
scripts.
Data analysis
Means were taken for each trial of duration 10 s in the closed-loop
experiment, and then these were grouped by odor treatment. WBA
responses were processed with a fifth-order zero-phase 200 Hz low-pass digital
Butterworth filter. To derive a mean value for each individual fly, five
WBA responses were averaged, and then the maximum response was taken
from the first 0.3 s of the response mean. Subsequently, the response means
(R) from each fly were normalized against the maximum response mean
(Rmax) for that fly, giving
R/Rmax. Statistical significance was assessed
using a paired t-test on the normalized data. To derive a value for
each open-loop visual stimulus, the maximum response within the first 0.3 s of
each individual WBA response was normalized against the maximum
individual response for that fly across all treatments. Statistical
significance was assessed using two-factor repeated measures ANOVA.
In order to calculate the peak-to-peak amplitude of the WBA response
at each frequency epoch, a sine wave was fitted to the WBA trace of
each fly using an optimization algorithm. Sine waves were fitted using a
sum-of-squares minimization routine. Once a fit was defined, peak-to-peak
amplitude was found from the maximum and minimum fly responses within 100
samples (0.2 s) of the corresponding minimum and maximum values of the fit.
r-squared goodness of fit was calculated with the following equation:
r2=1–(observed
WBA–fit)2/(observed WBA–mean
WBA)2. Data analysis was conducted with custom-scripts
written in Matlab.
Digitized pictures during the landing experiment were acquired at 30Hz. A custom algorithm detected the increase in average image brightness caused by lateral extension of the legs during the landing reflex. Digital filtering of the image eliminated variance in luminance caused by the beating wings, and subtraction of the first frame enhanced the image contrast. Analysis performed by hand on three sample flies indicated a zero false-positive rate and a false-negative rate of 7.14%. The algorithm generally only detected responses involving all six legs, although sometimes very brief responses involving only one or two legs were seen, which were not included. The landing probability was defined as the percentage of landing responses detected by the algorithm out of all stimulus presentations at that position for all flies.
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RESULTS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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).
WBA is a quantitative proxy for yaw torque, and thus the variability
in this signal is a direct measure of steering activity. Upon odor exposure,
WBA variance decreased in wide-field expansion and rotation. Data
collected using low-contrast and high-contrast wide-field stimuli were
qualitatively similar and thus were pooled
(Fig. 2A, paired
t-test, expansion P<0.001, rotation P<0.05).
Upon exposure to odor, there were no significant changes in variance during
the presentation of flicker or during object tracking, indicating that the
odor-mediated decrease in WBA variance was dependent on the context of
active visual control (Fig.
2A). These results suggest that, upon encountering an attractive
odor, flies use wide-field cues, but not small-field cues, to stabilize their
flight heading better (Fig. 2B,
paired t-test, expansion P<0.001, rotation,
P<0.001).
|
).
The odor-evoked increases in total wing-beat amplitude (WBA) and WBF
are reflected in increased aerodynamic power output as the cubed product of
WBF and WBA is proportional to total aerodynamic power output
(Lehmann and Dickinson, 1998;
Lehmann and Dickinson, 1997).
Therefore, the odor-mediated changes in power output could effectively limit
WBA variance. To test this hypothesis, we plotted WBA against
(WBAxWBF)3, a proxy for aerodynamic power output
(Duistermars et al., 2007b) and
confirmed that WBA variance indeed tends towards zero at high power
output (Fig. 2C). However, over
the full range of power values, the distribution of points associated with
odor clusters more tightly around zero than that of responses without odor
(Fig. 2C), and thus the
steering variance during odor presentation is lower than for the no-odor
control (Fig. 2C, inset). This
result confirms two separate motor responses to attractive odors: a bilateral
increase in WBA and WBF that results in increased aerodynamic power
output, and an increase in active visual stabilization that results in a
straight flight heading.
Visual-context-dependent influence of olfactory input on flight control
In order to test the hypothesis that odor differentially influences
rotation and expansion optomotor responses, we tracked wing steering
kinematics in response to open-loop presentations of expansion and rotation
optic flow in the presence and absence of an attractive odor. Aversive odors
are irrelevant to active tracking behavior and thus were not investigated.
Flies were presented with a sequence of five visual stimuli of duration 1 s in
which the visual panorama rotated clockwise or expanded from left to right,
interspersed with segments of duration 1s in which the fly had active
closed-loop control of a vertical stripe (ensuring that the animal was
actively engaged in visual flight control throughout the experiment). Flies
responded strongly to both treatments with an increase in WBA,
representing a rightward turn. An example raw data trace is shown in
Fig. 3A. The effect of odor is
subtle, yet clearly evident as an increase in WBA for rotation and a
decrease for expansion (Fig.
3A,B). There was no difference in WBA arising from
olfactory treatment in expansion, although WBA decreased significantly
in odor for rotation (data not shown). Odor-mediated suppression of mean
expansion responses and enhancement of mean rotation responses were
independent of the time course of stimulus presentation (two-factor repeated
measures ANOVA, odor P<0.05, time P>0.05). Although we
designed the expansion and rotation stimuli to produce steering responses of
similar magnitude, we note here that the rotation responses are nevertheless
smaller than the expansion responses, which is consistent with previous
findings (Tammero et al.,
2004; Duistermars et al.,
2007a; Duistermars et al.,
2007b).
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Odor interacts with the expansion optomotor pathway `upstream' of the landing pathway
Because it decreased sensitivity to expanding cues
(Fig. 3), we hypothesized that
odor might facilitate landing by increasing visual tolerance of a stimulus
expanding on the retina. In response to a small square expanding at 250
deg.s–1, flies rapidly extend their legs in a stereotypical
landing reflex (Fig. 4A)
(Borst, 1990;
Tammero and Dickinson, 2002a).
We presented landing stimuli in random order at several positions around the
arena. The probability of eliciting a landing reflex (see Materials and
methods) increases as the stimulus is presented progressively towards the
front of the fly (Tammero and Dickinson,
2002a). At each azimuthal stimulus position, except at that of the
heading of the fly, odor slightly decreased landing response probability
(Fig. 4B, two-factor repeated
measures ANOVA P<0.01).
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The interaction of olfactory-mediated flight control and heading stability
An increase in sensitivity to open-loop rotational motion
(Fig. 3) is consistent with the
increased flight stability observed when the fly has active control over
retinal image motion (Fig. 2).
However, how does reduced sensitivity to open-loop expansion allow the animal
to fly straighter while actively controlling an expanding panorama
(Fig. 3)? It would seem
reasonable to posit that, under fully closed-loop conditions, the performance
should be `sloppier' with an expanding panorama because the fly tolerates more
image expansion before exhibiting steering maneuvers. However, for all
combinations of spatial, temporal and contrast properties yet tested,
wide-field expansion evokes stronger steering responses than equivalent
wide-field rotation (Duistermars et al.,
2007a; Duistermars et al.,
2007b; Tammero et al.,
2004). Without a deeper understanding of the maximum operational
gain that is possible, it is very difficult to predict what the influence of a
change in gain might be. For a system operating under nearly
saturated conditions, a decrease in gain could damp feedback oscillations and
improve stability. By contrast, if the system is operating below maximum gain,
then an increase could push the system closer to oscillation instability.
Similarly, the temporal delay between visual motion detection and resultant
corrections from the motor circuits greatly impact the influence of varying
the stimulus conditions.
To resolve the apparent inconsistency between the open-loop and closed-loop
conditions presented, we presented the fly with a combination of both. Thus,
we imposed a bias on the ability of the fly to control the visual panorama
actively and then tested how odor influences optomotor sensitivity. Under
these conditions, if the fly were to ignore the bias signal completely, then
the wing kinematics would be independent of the bias signal, and the visual
panorama would follow the motion trajectory defined by the bias. Conversely,
if the fly fully compensated for the bias, then the wing kinematics of the
animal would follow the bias, and the visual display would move in a manner
indistinguishable from the normal closed-loop conditions.
(Frye and Dickinson, 2004;
Tammero et al., 2004). We used
a sinusoidally varying frequency waveform that ranged from 1–8 Hz. An
example trace is shown in Fig.
5A. Under biased closed-loop conditions, flies attempted to
correct for the sinusoidal stimulus by varying their WBA sinusoidally
in phase with the stimulus velocity (Fig.
5B).
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WBA was reduced
in expansion and increased in rotation
(Fig. 5B). To test this
difference quantitatively, we fitted a sine function to the WBA
response of each frequency epoch for each fly. Wide-field expansion generally
showed a lower average peak-to-peak amplitude response in odor (except at 1
Hz), whereas the average amplitude was increased for rotation at all
frequencies (Fig. 5C,
two-factor repeated measures ANOVA, expansion P<0.05, rotation
P<0.001). Consistent with the previous results, the effect of
expansion suppression, although statistically significant, was subtler than
that of rotation enhancement.
Olfactory enhanced salience of visual input
Although the differences are repeatable and significant, we were impressed
by the rather subtle influence that odor has on optomotor steering kinematics.
We reasoned that any influence of olfactory cues might arise from increased
perceptual salience of visual input regardless of the specific visual context
and that increased salience would mediate the differences between optomotor
reactions, which might be subtle `by design' so as not to compromise optomotor
flight control. We found that, during both the expansion- and rotation-biased
closed-loop treatments, the experimental trials with odor had higher average
r-squared values than trials without odor when fit to sine functions
(Fig. 6). This suggests that
the flies are tracking the imposed visual bias more closely when exposed to
odor, resulting in a more sinusoidal, less variable, WBA waveform. This
recapitulates our closed-loop findings
(Fig. 2) and, taken together,
implies that odor increases the salience of visual signals.
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DISCUSSION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Ethological implications for plume tracking behavior
Male moths display upwind anemotaxis during flight, interspersed with
cross-wind casting to track pheromone plumes emitted by female conspecifics
(Preiss and Kramer, 1986;
Vickers, 2000). Recently,
Drosophila melanogaster has been shown to use a similar
plume-tracking strategy (Budick and
Dickinson, 2006). As flying insects cannot differentiate
self-motion from wind cues using mechanosensory input alone, reliance on
visual side-slip cues has been shown to play an important role in anemotaxis
(Kennedy and Marsh, 1974;
Vickers, 2000). An
odor-activated increase in rotational optomotor gain might help maintain a
straight heading in a plume, whereas enhanced tracking of wide-field expansion
cues might facilitate optomotor anemotaxis. Concomitantly, suppressed
expansion avoidance enables closer approach to smelly objects. Therefore,
context-dependent olfactory-enhanced optomotor reflexes might underlie the
visual dependence of airborne odor localization across taxa.
Opto-olfactory control systems
The spatial and temporal dynamics of visually mediated flight behavior
indicate that the optomotor reactions to wide-field rotation and expansion are
mediated by separate neural pathways
(Duistermars et al., 2007a;
Duistermars et al., 2007b).
Similarly, expansion-triggered behaviors are further subdivided into collision
avoidance and landing and are probably mediated by separate neural circuits
(Tammero and Dickinson,
2002a). The latter analysis posits a three-way local circuit of
elementary motion detectors comprising frontal and lateral inputs such that
collision-avoidance pools from the lateral arrays, and landing pools from the
frontal array (Tammero and Dickinson,
2002a). This tripartite model forms a conceptual framework for the
olfactory results presented here such that olfactory cues both amplify
rotational optomotor responses and selectively diminish the sensitivity of the
peripheral collision-avoidance circuits. This idea is supported by two lines
of evidence. First, olfactory stimuli suppress both collision-avoidance turns
evoked by lateral expansion (Figs
3 and
5) and landing responses to
lateral expansion (Fig. 4B).
Second, the probability of landing responses is not influenced by frontal
expansion (Fig. 4B). Similar
olfactory-mediated enhancement of visual circuits is observed within
descending pre-motor neurons in moths, which are visually specific yet exhibit
amplified spiking activity when the moth is exposed to pheromone
(Olberg and Willis, 1990).
Olfactory-mediated increase in visual salience
It was intriguing to find that optomotor responses more closely reflect an
imposed visual stimulus under the influence of odor, by contrast to no odor,
in which the steering responses are significantly less dependent on the visual
stimulus. Under closed-loop feedback conditions, the mean goodness of fit
between a fitted sine function and the resultant wing kinematics of the fly
during flight improves under both rotation and expansion at all tested
frequencies when the fly was presented with attractive odor
(Fig. 6). This suggests to us
that odor enhances the salience of ambient visual cues. Casually speaking,
flies seem to be `paying attention' to the visual panorama within an odor
plume more so than within the water vapor control. These results are
consistent with other findings in Drosophila, such as a
frequency-specific increase in brain activity attributed to olfactory-enhanced
salience of a visual object (van Swinderen
and Greenspan, 2003), and olfactory-enhanced memory retrieval
associated with a weakly detectable visual stimulus
(Guo and Guo, 2005); however,
to our knowledge, this is the first behavioral evidence that the perceptual
salience of visual stimuli is enhanced by olfactory input specifically to
improve active optomotor control during flight.
An adjustable cross-modal search algorithm
During free-flight, visual feedback is required for odor localization, but
the behavioral effects are subtle and highly variable. Simulations confirm
that small modifications to flight heading and collision cues are at least
sufficient to enable odor localization when the search algorithm is iterated
over hundreds of saccades, as occurs in free flight
(Frye et al., 2003;
Reynolds and Frye, 2007). A
subtle effect of odor on the flight-control algorithm might be preferable,
however, as a robust influence could potentially leave the animal vulnerable
to course perturbations imposed by gusts of wind and pursuit from predators.
By contrast, small, yet consistent, modifications to flight behavior take
advantage of sensory reflexes to bias merely the heading of the animal towards
the odor source without compromising adaptive reflexes.
Animals seeking widely dispersed chemical signals search actively even when they are not actually experiencing an odor plume. The improved sine fits for both expansion and rotation suggest that odor might tip the balance from sensory-independent exploratory search behavior towards a sensory-dependent active tracking algorithm. It therefore stands to reason that the course correction to rotation and expansion are implemented as a result of increased visual salience. As a working hypothesis, we suggest that odor triggers rotational optomotor responses that enhance straight flight; simultaneously, expansion responses are suppressed to enable an animal to approach more closely an appropriately smelly visual feature. Odor-enhanced visual salience tips the balance from variable sensory-independent exploratory behavior towards more-stereotyped sensory-dependent local search behavior to steer a fly to its goal. The modulation of optomotor control by olfactory input represents a relatively simple, yet robust, mechanism by which an animal might track a fragmented odor plume within varied visual landscapes without the need for high-order object-recognition computations.
LIST OF ABBREVIATIONS
WBA
WBA
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Acknowledgments |
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