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First published online November 17, 2006
Journal of Experimental Biology 209, 4597-4606 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.02583
A comparison of visual and haltere-mediated feedback in the control of body saccades in Drosophila melanogaster
Division of Biology, California Institute of Technology, Pasadena, CA 91125, USA
* Author for correspondence (e-mail: jbender{at}caltech.edu)
Accepted 4 October 2006
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Summary |
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Key words: Drosophila, saccade, vision, haltere, feedback
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Introduction |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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). These
behaviors are so rapid that the position of the target is unlikely to change
much during the course of motion. Further, because the dynamics of a
fluid-filled sphere are relatively simple - compared, say, to a multijoint
limb (Fisk and Goodale, 1985)
- it may be reasonable to predict the actuation required to move the eyeball
to the desired orientation without the use of sensors. However, there is
evidence that even for such mechanically simple behaviors as eye saccades,
feedback can nevertheless play a role
(Jürgens et al., 1981;
Soetedjo et al., 2002).
Because of the slow speed of visual processing relative to the duration of the
saccade, this feedback arises from other, faster sensory modalities
(Jürgens et al.,
1981).
Saccadic eye movements are not limited to primates, but are rather
ubiquitous behaviors among animals with image-forming visual systems. They
have been observed across three phyla, even in animals in which the eyes
cannot be moved independently of the head
(Land, 1999). The degree to
which these homologous behaviors employ feedback and, if so, whether such
feedback arises from the visual system itself or from other modalities is not
known. In the fruit fly, Drosophila melanogaster, flight is
characterized by sequences of straight flight interspersed with rapid turns
called `body' saccades (after Land and
Collett, 1974), which are rapid, stereotyped turns during which
the fly changes directions by about 90° in 70 ms
(Tammero and Dickinson,
2002a). Flies in free flight must generate torque to start
rotating and countertorque to stop (Fry et
al., 2003). However, rigidly tethered flies generate torque for
approximately 500 ms, much longer than the duration of a free flight saccade,
and never generate countertorque
(Heisenberg and Wolf, 1979).
This suggests that reafferent feedback does play a role in structuring the
saccade motor program, once a saccade has begun.
Visual expansion can trigger saccades
(Tammero and Dickinson, 2002a;
Tammero and Dickinson, 2002b;
Bender and Dickinson, 2006),
but the time course of saccades in tethered flight is very long even when
flies are allowed to rotate their own visual environment
(Heisenberg and Wolf, 1979;
Tammero and Dickinson, 2002b),
immediately suggesting that the visual system provides little feedback to the
saccade motor program, once a turn is initiated. This lack of influence is
surprising, given that open-loop rotation of large-field visual patterns
elicits strong syndirectional turning responses (after
Götz, 1964). However,
flies also have specialized mechanosensory organs called halteres that are
capable of providing feedback during saccades. The halteres are evolutionarily
modified hindwings that beat antiphase with the wings and function as
gyroscopes (Pringle, 1948).
The haltere system is linearly sensitive to angular velocity
(Dickinson, 1999) and possesses
frequency response properties that are complementary to the low-pass
characteristics of the visual system
(Sherman and Dickinson, 2003).
The halteres also allow feedback into the flight control circuitry to occur
much more rapidly than vision does, as the main pathways operate through mixed
chemical/electrical synapses (Trimarchi
and Murphey, 1997; Fayyazuddin
and Dickinson, 1999). The lack of haltere-mediated feedback to
rigidly tethered animals is a likely explanation for the elongated time course
of saccades relative to free flight. We recently developed a preparation that
allows flies to rotate freely about one axis, thus providing them feedback
from the halteres and other mechanosensory systems
(Bender and Dickinson, 2006).
Flies tethered in this way perform saccades with a time course more closely
resembling that observed in free flight, suggesting that sensory feedback,
possibly from the halteres, plays some role in determining saccade dynamics.
However appealing, this hypothesis is unproven and the relative contribution
of each modality is still uncertain.
In the present study, we tethered Drosophila melanogaster to steel pins and placed them in a magnetic field such that they were free to rotate about their functional yaw axis. We observed the flies with a digital camera and used an electronic panorama to manipulate the visual feedback received by flies during saccades, in combination with alterations of haltere feedback and wing aerodynamics. The results suggest that haltere-mediated feedback is mainly responsible for terminating saccades, but the visual system does play an important role in maintaining straight flight.
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Materials and methods |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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).
Briefly, we anesthetized the flies by cooling them to 4°C on a Peltier
stage and then attached a 50 µm diameter stainless steel pin (nominally 0.1
mm minutien, Fine Science Tools, North Vancouver, BC, Canada) to the notum
using UV-activated cement (Duro, Düsseldorf, Germany).
To add weight to the halteres in some experiments, we applied a small
amount of UV-activated cement to the endknob, roughly doubling its volume. For
haltere ablation experiments, we removed the left haltere just above its base
by pulling gently on the stalk with fine forceps. This method left intact the
df2 campaniform sensillum and the large chordotonal organ, which are thought
to be largely responsible for the response to rotations about the yaw axis
(Pringle, 1948;
Fayyazuddin and Dickinson,
1996). Almost all of these flies were capable of remaining
airborne in free flight, if allowed.
In further experiments, we clipped off portions of the wing to reduce the aerodynamic surface. In some flies, we cut away the posterior half of the right wing. In others, we removed the distal third of the left wing. Data from the latter group were collected at a camera speed of 101 frames s-1, and those flies did not receive the experimental visual feedback detailed below. Some of the wing-clipped flies could remain airborne in free flight at least temporarily, but many could not. Flies that did not maintain flight for 10 min while tethered in our arena were excluded from analysis.
An additional set of flies were tethered and observed in neartotal darkness
at a camera speed of 101 frames s-1. Whereas the room lights were
turned off during all recordings, for these sessions we also covered the
entire arena and camera with thick, black fabric to remove as many external
visual cues as possible. Under these conditions, we measured a luminance of
<0.1 lux in the visible spectrum. As previous experiments have shown,
flight duration and performance decrease in the absence of closed-loop visual
feedback (Heisenberg and Wolf,
1988; Dickinson,
1999). Therefore, under dark conditions we included data from
flies that flew continuously for 5 min or more. As an internal control and to
reduce dark adaptation (Bernhard and
Ottoson, 1960), we alternated 1 min periods of darkness with 1 min
periods during which the arena displayed a stationary pattern.
Flight arena and calibration
As detailed in an earlier study (Bender
and Dickinson, 2006), we placed the fly and pin in the magnetic
field of two vertically aligned rare earth (NdFeB) magnets (K&J Magnetics,
Jamison, PA, USA). This configuration allowed the fly to rotate freely about
the long axis of the pin - its functional yaw axis
(Fig. 1B), an approach first
attempted by Heisenberg and Wolf using a long, flexible filament
(Heisenberg and Wolf, 1979).
We recorded the fly's orientation around this axis by illuminating it from
beneath with an array of 940 nm light-emitting diodes (LEDs) and fixing a
mirror below the fly to reflect its image to an infrared-sensitive digital
camera (A602f, Basler, Ahrensburg, Germany). The average frame rate of the
camera was 564 frames s-1, with the exceptions noted above, and the
shutter speed was 1.7 ms for all experiments. We tuned the camera's image
threshold for each fly before each experiment and saved the fly's orientation
in each frame for later analysis. The fly and lighting sat within a
cylindrical arena composed of 32x64 green LEDs
(Fig. 1A), each subtending
approximately 5.6° of azimuth. The individual LEDs were refreshed at 800
Hz, and the pattern displayed on them was updated at about 220 Hz by the
associated control board (M. B. Reiser and M. H. Dickinson, manuscript
submitted for publication). The control board was under the command of a PC
that analyzed the incoming camera images and updated the visual stimulus
accordingly. The 1.8 ms interval between frames, plus a measured average
latency of 3.5 ms between the camera and the PC (including image analysis),
plus the 4.5 ms pattern update rate, totaled an average maximum delay of about
10 ms between a fly's behavior and our ability to alter the visual display in
response to it. This represents roughly two wing strokes or 10-20% of the
duration of a free-flight saccade.
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At the start of each experiment, we first subjected the fly to a
calibration that made it possible to unambiguously determine the fly's heading
with respect to the camera. This calibration period consisted of 1 min of
rotation elicited using a stimulus in which poles of expansion and
contraction, set apart by 180°, were rotated around the fly
(Bender and Dickinson, 2006).
Under these conditions, flies robustly fixate the pole of contraction
(Tammero et al., 2004).
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;
Egelhaaf et al., 1989), and
also matches recent findings using a similar electronic display
(Sherman and Dickinson, 2003).
On top of this background, we displayed a `foreground' stimulus consisting of
a dark, vertical stripe, 45° wide, which was controlled independently of
the background pattern.
Each experimental trial was conducted during a spontaneous saccade made by
the fly. The trial type was selected randomly ad hoc, with the
constraints that each trial begin at least 1 s after the previous trial and
that two consecutive trials be of different types. To determine in real time
when a saccade was made, we approximated the fly's angular velocity by
averaging its instantaneous velocity between each unique pair drawn from three
consecutive camera images (e.g. the average of the instantaneous velocity
measured between frames 1 and 2, frames 2 and 3, and frames 1 and 3; a total
of 3.5 ms of flight). The instantaneous angular velocity between two frames
was calculated by measuring the difference between the fly's orientation in
each frame and dividing by the elapsed time between those two frames. When
this estimate exceeded 650 deg. s-1, our software automatically
initiated a rotation of either the foreground, background, both, or neither by
40° in 80 ms at a constant angular velocity of 500 deg. s-1.
These values were chosen because they corresponded roughly to rotations
generated by the fly's own motion during a typical saccade in this preparation
(Bender and Dickinson, 2006).
The visual rotation was either with or against the direction of the saccade,
and the foreground could be rotated in the opposite direction from the
background. Our real-time velocity thresholding technique resulted in many
more false positives than false negatives; however, only trials during which
the fly both performed a saccade (as determined post hoc; see below)
and met the real-time saccade criterion were used in further analysis. The
discrepancies between the timing of the two (real-time and post hoc)
thresholds is shown in Fig. 2B
and can be seen for a single trial in Fig.
1C as the difference between the beginning of the `saccade
duration' period and the gray box indicating the time course of the
experimental feedback. Trials where the real-time threshold was reached before
or more than 15 ms after the post hoc threshold were discarded,
leaving only saccades with a distribution of total detection latencies ranging
from 10 to 25 ms, including delays due to both the hardware and software. By
way of comparison, the latency of vision-to-motor responses in a flying
housefly is 30 ms (Land and Collett,
1974).
After the experiments were over, we identified and quantified saccadic
flight sequences as in our prior analysis
(Bender and Dickinson, 2006).
We filtered the orientation data (140 Hz, low-pass) and applied the central
difference formula to estimate angular velocity. We used the post hoc
velocity threshold of 350 deg. s-1 calculated during our previous
study to separate saccadic events from straight flight and slow turning. We
defined the duration of each saccade as the time during which the fly's
angular velocity exceeded one-quarter of its maximum value for that event. We
then quantified the amplitude of each saccade as the difference between the
fly's median orientations across two 50 ms windows: one window before and one
after the period defining saccade duration
(Fig. 1C,D). Only saccades with
amplitudes between 15° and 150° were analyzed.
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Results |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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To address the issue of visual control in a more extreme setting, we observed several flies in a visual setting alternating between a static display and total darkness (Fig. 4). These suggested significant differences (P<0.05) in the duration, amplitude and peak angular velocity of saccades performed in the dark compared with saccades performed in the light. However, the P-values calculated by ANOVA statistics directly depend on the number of degrees of freedom in the model, with increasing degrees of freedom tending to decrease P-values. Therefore, because of the relatively large number of saccades analyzed in these experiments compared to our other analyses, the threshold for statistical significance must be more stringent. Taking all these factors into consideration, we interpret these results to indicate that saccade dynamics are mostly independent of the visual environment, with the possible exception of saccade duration (Fig. 4).
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), which are a
function of the endknobs' inertia (Fig.
5B). Thus, since the Coriolis forces scale with mass, increasing
the mass of the endknobs should act to increase the gain of the haltere
feedback. On the other hand, unilateral haltere ablation should decrease the
total haltere-mediated feedback. In the absence of any manipulation of visual
feedback, we found that weighting the halteres significantly decreased the
median amplitude and peak velocity of saccades
(Fig. 5C, second row) compared
to control (P<0.001) and also tended to decrease saccade duration,
but not significantly. Ablating one haltere statistically increased saccade
amplitude, duration and peak angular velocity, an effect that is laterally
symmetric, in the sense that an ablation of the left haltere equally
influences saccades to the left and right (amplitude shown in
Fig. 8A; P>0.05).
The results of these experiments suggest that feedback from the halteres plays
a role in terminating the saccade motor pattern, and may be integrated
centrally rather than via simple ipsilateral projections. This is
plausible, given what is known about the projections of haltere afferent
neurons (Chan and Dickinson,
1996).
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In some circumstances, manipulations of the halteres can cause them to
adopt a different stroke frequency than that of the wings
(Sellke, 1936;
Pringle, 1948). Because the
halteres provide sensory feedback to the wing control circuitry on a
stroke-by-stroke basis even in the absence of body rotation
(Heide, 1983;
Fayyazuddin and Dickinson,
1999), the observed effects of haltere alteration might be due not
to a modulation of rotation sensitivity but to a disruption of
wingbeat-synchronous afferents on the haltere that are required for normal
steering muscle function. To determine whether our flies had an altered
haltere stroke frequency, we analyzed sequences of high-speed video (6000
frames s-1) for any indication of a phase shift relative to the
wingbeats but detected no such change.
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We applied a detailed mathematical model of the forces produced during
flapping flight (Dickson et al.,
2006) to simulate the aerodynamics of flies with one wing surface
altered to match our experiments. In this model, both of the wing alterations
we made induced a significant yaw moment relative to flies with intact wings,
assuming flies did not change their wing motion in response to the alteration
in wing area. However, high-speed video analysis of real flies indicates that,
when maintaining straight flight, the clipped-wing flies were continuously
compensating by differentially altering wing flip timing in a manner similar
to that seen during turns in intact flies (H. Sugiura and M. H. Dickinson,
manuscript in preparation). These compensatory changes were particularly large
in the distal-clipped flies, and more subtle in the posterior-clipped flies.
There are limits to the compensation, however, such that when we inadvertantly
cut away too much of the wing surface in some flies in each group (which we
could not further analyze), they spun continuously like a propeller on our
magnetic tether. This implies that our manipulations did have effects on
aerodynamic force production, in agreement with the model, and that flies must
have been compensating in order to sustain straight flight. However, in
clipped flies flying stably, we found no differences between saccades to the
right and left in terms of amplitude (Fig.
8B,C), duration, or peak velocity (data not shown)
(P>0.05). It is also worth noting that because wing motion is due
in part to complex, but subtle, effects of translational and rotational
inertia, some of the changes in wing motion observed in clipped flies may have
been caused not by active compensation, but by passive effects as a result of
the change in wing mass and shape.
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Discussion |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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Haltere-mediated feedback and saccade termination
Our data indicate that increased haltere feedback leads to smaller
saccades, presumably by premature triggering of the counterturn phase
necessary to overcome the animal's inertia and stop rotation
(Fry et al., 2003). This is
consistent with the hypothesis that a major reason for the differences between
the saccade behavior as observed in free and rigidly tethered flies is the
lack of haltere feedback under tethered conditions (e.g.
Heisenberg and Wolf, 1979;
Bender and Dickinson, 2006).
Electrophysiological studies in rigidly tethered flies suggested that saccades
are caused by changes in steering muscle activity, including a burst of action
potentials in the second basalar muscle (b2) and a phase advance of the first
basalar muscle (b1) (Heide and Götz,
1996). However, these transient changes in activity last much
longer than in the free flight or magnetically tethered cases, and probably
represent feed-forward components of the underlying motor program that play
out in the absence of haltere-mediated rotational feedback. Presumably, such
feedback somehow terminates these changes and initiates others responsible for
generating the countertorque that stops the turn.
It is difficult to make strong claims based only on our ablation
experiments, because such manipulations might compromise the function of the
haltere in other ways. In particular, ablation disrupts the feedback from all
the mechanosensory organs on the haltere, only two of which (the df2
campaniform field and the chordotonal organ) are thought to encode Coriolis
forces (Pringle, 1948;
Fayyazuddin and Dickinson,
1996). Even in the absence of body rotation, the other campaniform
fields provide wingbeat-synchronous input that is necessary for proper phase
tuning of wing steering muscles (Heide,
1983; Fayyazuddin and
Dickinson, 1996). In fact, flies with both halteres removed will
not maintain flight on a magnetic tether for more than a few minutes at most,
although they will fly for several minutes in total darkness; however, their
saccades and general flight dynamics are extremely disturbed. Thus, removal of
the phasically active campaniform inputs that do not encode Coriolis forces
could cloud the interpretation of experiments addressing the haltere's role as
an equilibrium organ. The experiments with weighted halteres are less
ambiguous, because the manipulation is unlikely to severely alter the function
of the phasically active, Coriolis-insensitive campaniform fields. Indeed, our
observation that increasing haltere mass decreased saccade size is difficult
to explain except by the predicted increase in haltere sensitivity.
Collectively, the results of our experimental manipulations support the
hypothesis that saccade dynamics are tuned by the amount of rotational
feedback provided by the halteres, but not the eyes. The minimal role of
vision is further corroborated by the finding that saccade dynamics are fairly
constant even in total darkness (Fig.
4). Confirmation of this working hypothesis will require
electrophysiological records under conditions in which haltere feedback can be
experimentally induced. In addition, genetic methods offer a potential means
of selectively disturbing the input from the Coriolis-sensitive haltere
fields. The gene shaking-B2 is required for the function
of a subset of gap junctions in the fly, including those between the halteres
and wing motor neurons (Thomas and Wyman,
1984; Trimarchi and Murphey,
1997). Flies with a null allele of this gene flew poorly in our
apparatus, preventing a direct comparison with our other results. However,
this strain did appear to perform saccade-like behaviors and is worthy of
future attention.
On the role of visual feedback during flight
It is known that flies can discriminate prominent foreground objects from
the visual background (Reichardt and
Poggio, 1979; Egelhaaf,
1985; Reichardt et al.,
1989) and tend to fixate large, vertical stripes in the foreground
(Götz, 1980;
Götz, 1987). For this
reason, we tested our flies with combinations of foreground and background
rotations during saccades, and found that none of these manipulations had any
significant effect. However, the P-values obtained when rotating the
foreground stripe against the direction of the saccade were more nearly
significant than those measured during the other rotation conditions
(P=0.15 for duration; P=0.07 for velocity). Testing the
figure-ground distinction was not a major goal of this analysis, however, and
we do not have sufficient data to test for effects of the relative orientation
of the fly and the large stripe.
Although vision appears have a potent role in maintaining overall flight
stability (Fig. 9), our results
do not support a role for visual feedback in terminating body saccades. This
is noteworthy, given the large quantity of studies showing its importance in
other flight behaviors (e.g. Reichardt,
1969; Collett and Land,
1975; Götz,
1975; Reichardt and Poggio,
1976; Wolf and Heisenberg,
1990; Tammero and Dickinson,
2002a; Egelhaaf et al.,
2002; Higgins,
2004; Frye and Dickinson,
2004). However, most previous studies have focused on the role of
vision as an equilibrium system to maintain straight flight or a detection
system to initiate maneuvers, not its use during active turns. The strength of
optomotor responses under open-loop conditions
(Götz, 1964) raises
questions about the influence of vision during selfgenerated motion. In
particular, there must be a mechanism by which strong compensatory reflexes do
not continually counteract voluntary turns. One possibility is that some form
of internal efference copy (Sperry,
1950; von Holst and
Mittelstaedt, 1950) is used to counteract reafference generated by
motion. Another possibility is that the visual system is simply too slow, such
that an internally generated motion command results in substantial body
rotation before optomotor reflexes can act to attenuate it.
The visual system has bandpass filter characteristics that largely suppress
its response to rotations above 600 deg. s-1
(Sherman and Dickinson, 2003;
Hengstenberg, 1991); however,
the majority of the saccades we observed in the magnetically tethered
preparation have peak velocities below this value
(Bender and Dickinson, 2006),
and our experimental visual rotations were of a constant 500 deg.
s-1. Heisenberg and Wolf, working on rigidly tethered preparations,
performed a set of experiments related to the ones we present here
(Heisenberg and Wolf, 1979).
They reported a response to rotations of a full-field visual pattern by
30° in 200 ms (150 deg. s-1) in the same direction as the
saccade, but due to technical limitations at that time, they show only the
results of a few trials. They found no response to visual rotation opposite
the direction of the saccade, either with single-stripe or checkerboard
patterns, but did note a syndirectional turning response to an open-loop
rotation of the visual field. Therefore, we analyzed the flies' responses to
our `false positive' trials, in which the visual rotation was initiated but a
post hoc analysis did not indicate a saccade, to determine the
open-loop responses to the visual rotation shown during saccades. Flies made
small (2-3°) course corrections in response to these stimuli, which were
comparable in magnitude to the statistically insignificant changes in saccade
amplitude we measured when presenting the flies with the same rotating visual
stimuli. These observations suggest that the visual feedback during saccades
may be too brief to elicit a substantial response, but that ongoing feedback
from the haltere system acts to terminate the saccade motor program. This also
supports a previous study concluding that haltere-mediated and visual feedback
are combined by the fly's flight control system as a weighted sum, with
greater emphasis placed on the mechanosensory feedback
(Sherman and Dickinson,
2004).
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Acknowledgments |
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) and
the halteres' mass (m) and velocity (v). The deflections
caused by the Coriolis forces are sensed by haltere mechanoreceptors. (C)
Changing the amount of haltere feedback affects saccade dynamics. Top to
bottom: control (same data as top row of
