Spatial organization of visuomotor reflexes in Drosophila
1 Bioengineering Graduate Group, University of California, Berkeley, CA
94720, USA
2 Bioengineering, California Institute of Technology, Pasadena, CA 91125,
USA
Author for correspondence (e-mail:
frye{at}caltech.edu)
Accepted 25 September 2003
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Summary |
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Key words: fruit fly, Drosophila, optic flow, vision, sensorimotor integration, wing kinematics, optomotor, motor control, LPTC, behavior, flight
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Introduction |
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Within flies, early evidence for the use of visual motion in flight control
emerged from the identification and analysis of the optomotor response
(Götz, 1968). When placed
within a vertically striped rotating drum, animals turn in the direction of
the moving pattern a response that acts to decrease the optic flow
across the retina. In free flight or in walking, such a reflex is thought to
stabilize locomotion by maintaining yaw velocity close to zero in the face of
either external perturbations or morphological and physiological asymmetries
(Götz, 1975
;
Heisenberg and Wolf, 1988
).
The optomotor response has been used extensively as a behavioral assay to
investigate the relationship between genes and visually mediated behavior in
Drosophila (Blondeau and
Heisenberg, 1982
; Götz,
1985
; Keller et al.,
2002
; Strauss,
2002
). However, the combination of translational and rotational
motion and the structural complexity of the visual world greatly complicate
the pattern of flow seen by a moving animal. Natural optic flow results from
both rotation and translatory self-motion of the animal, as well as the
movements of objects within the environment. The complexity of natural visual
dynamics is probably matched by specialized structurefunction
relationships within the hierarchy of visuomotor processing. By presenting
fruit flies with patterns other than pure image rotation, we show that the
visual system of these animals appears most sensitive not to full-field
optomotor rotation about the vertical axis but rather to patterns of expansion
and contraction generated during lateral translation.
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Materials and methods |
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To track the responses to motion in the display, the stroke amplitude and
frequency of both wings was tracked optically using a wingbeat analyzer
(Götz, 1987). We sampled
the data at 1 kHz using a data acquisition board (National Instruments,
Austin, TX, USA) and custom software written in MATLAB (Mathworks, Natick, MA,
USA). We conditioned and normalized the wingbeat signals off line as described
in a previous study (Tammero and
Dickinson, 2002a
). During each trial, the fly was presented with a
motion stimulus lasting 4 s followed by a 5 s interval with no motion. Each
experiment consisted of between 8 and 15 flies, each completing five sets of
50 trials.
Torque measurements
To measure the yaw torque that a fly generates, the flies were affixed to a
modified tether. A 12 mm-long x 0.15 mm-diameter tungsten rod was placed
inside an 8 mm-longpolished stainless steel tubing (0.36 mm outer diameter,
0.18 mm inner diameter). Both the tubing and tightly nested rod were fixed in
place at one end. The rod extended by 4 mm through the tubing at the free end.
A small 1 mmx1 mmx0.1 mm-thick surface mirror was attached with
cyanoacrylate to the protruding portion of the rod. Flies were tethered to the
free end of the rod as they were with normal tethers. The stiff outer tubing
minimized bending of the rod while permitting torsion generated by the
tethered fly. Thus, as the fly modulated its yaw torque, the rod and mirror
assembly rotated in torsion. Torsion was measured by aiming the beam of an
HeNe laser at the mirror, measuring the deflection of the reflected
beam using a position-sensitive dual photodiode `spot detector' (UDT SL5-2,
capable of detecting displacements as little as 2 µm). The signal from the
photosensor was amplified and low-pass filtered at a cut-off of 1 kHz. The
measured deflection of the beam was calibrated and found to be linear with
respect to applied torque. During turning responses, the torque produced by
the fly was calculated to twist the tether by less than 106
rad.
Closed-loop experiments
The methods for the closed loop experiments were identical to those used in
the open loop, except that the difference between the left and right wingbeat
amplitude was fed back to control the angular velocity of the display. The
visual pattern placed in closed loop with the fly was either a full-field
rotary pattern or a lateral expansion pattern, both of which extend over the
full flight arena. In these experiments, a 3.5 V peak-to-peak 0.5 Hz
sinusoidal bias was added to the feedback signal to challenge the fly's
ability to control the display. Each trial lasted 180 s with the bias applied
being switched on and off every 30 s. An individual experiment consisted of
three trials with the rotary stimulus and three trials with the expansion
stimulus.
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Results |
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Combining identical pattern motion in the front visual hemisphere with motion in the opposite direction in the rear field approximates the pattern of optic flow during sideways translation (side-slip) with a coherent focus of expansion on one side of the animal and a focus of contraction on the other. The amplitude of the response to this lateral expansion/contraction pattern is larger than that elicited by either full- or frontal-field motion. Unlike full-field rotation, the response to the expansion/contraction stimulus does not represent a simple linear sum of separate front and rear responses (Fig. 1D, dotted red lines). Instead, the response reaches a lower plateau and does not decay, as one would expect from the sum of separate front and rear field responses. This may result from morphological limits on the maximum wingbeat amplitude that the animal can exhibit during turns.
To further examine this interaction between motion in the rear and front visual hemispheres, we systematically varied the sign and magnitude of motion displayed behind the fly while keeping the motion in front of the fly constant (Fig. 1E). For each contrast frequency displayed to the rear field, the flies' responses showed little change as long as the rear field pattern rotated in the same direction as the front field. When the rear field was stationary, the turning response increased by a factor of 2.4 times over the full-field rotation response. When the direction of motion in the rear visual field was in the direction opposite that of the front field, creating lateral foci of expansion and contraction, response magnitude increased to three times the full-field rotatory optomotor response. Thus, the response to front field motion is greatly elevated by any small counterdirectional motion behind the fly, whereas a small concurrent rotation causes a large decrease in the turning response. The effect shows a non-linear saturation, such that variation in the contrast frequency of the rear hemisphere has little influence on the magnitude of the turning response, as long as it is in the opposite direction as the front hemisphere.
To test whether responses to the expansion/contraction stimulus vary
spatially, we measured the turning response while systematically changing the
azimuth of the foci of expansion and contraction. For foci of expansion
ranging from 100° to 100° azimuth, the relationship between the
turning response and stimulus position is sigmoidal
(Fig. 1F). Thus, any time the
focus of image expansion is displaced by more than 20° to one side, the
fly generates a robust turning response away from the pole of expansion.
Qualitatively, spatial variation in turning responses to a pattern of
large-field (i.e. panoramic) expansion is similar to that measured for a
small-field expanding object (Tammero and
Dickinson, 2002a).
Responses to image motion in insects are thought to result from the spatial
integration of directionally sensitive local elementary motion detectors
(EMDs; Buchner, 1976;
Buchner et al., 1978
;
Hassenstein and Reichardt,
1956
). Due to their underlying architecture, EMDs are subject to
aliasing due to the spatial separation of the detector elements
(Buchner, 1976
;
Götz, 1964b
), an effect
that might explain the reversal of the optomotor response in the rear field of
view. If, for example, the spacing of the rear field EMDs were substantially
different from those in the front field, they might exhibit aliasing for image
velocities that elicit a non-aliased response from front field EMDs. We tested
this possibility by examining the dependence of both the front and rear
responses on image velocity. Holding the spatial wavelength of the pattern at
30°, we found no evidence for a change in the sign of either the front or
rear field responses at elevated image velocities
(Fig. 2). Although the rear
field response was more broadly tuned than the front field response, both
showed a similar unimodal dependence on contrast frequency (the image velocity
divided by the spatial wavelength). To further ensure that the sign of the
turning response did not result from this spatial aliasing, we repeated the
experiments with a 60° grating pattern, twice the initial spatial period.
Although the lower spatial frequency resulted in larger amplitude responses,
both the sign and magnitude of turning responses showed a similar dependence
on contrast frequency. Taken together, these results suggest that both front
and rear responses are mediated by EMDs with roughly similar spatial
properties and that the reversed sign of the rear field response cannot be
explained by spatial aliasing.
|
Optic flow fields generated during translation contain diametrically opposed poles of expansion and contraction. To determine if the full-field response could be explained by particularly salient individual components of the flow (Fig. 3A), we presented animals with a series of visual patterns approximating only parts of a translatory optic flow field; i.e. the focus of expansion, the focus of contraction and the area in between those parts of the flow field (Fig. 3BD). A stimulus in which the moving grating was eliminated over the lateral 90° azimuth on both sides of the fly (Fig. 3B) provided a pattern in which there were translational cues but no motion at the poles. The responses to this translating stimulus are similar to those elicited by a full-field expansion/contraction (Fig. 3A) or an isolated focus of expansion (Fig. 3C). By contrast, the response to an isolated focus of contraction is qualitatively different from the lateral expansion/contraction response. The turning response is smaller, never reaches steady state and changes sign after approximately 1.5 s (Fig. 3D). The responses to motion across the entire rear field followed a similar time course (Fig. 3D inset). The mathematical sum of responses to expansion and contraction presented individually slightly underestimates the response to both presented together (Fig. 3A, dotted red line). Together, these results demonstrate that whereas either translational motion or a clear focus of expansion is sufficient to initiate a strong turning response, an isolated focus of contraction is not.
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We further examined these phenomena by comparing responses to image motion restricted to individual quadrants of the fly's visual field. Like the response to image motion over an entire front half-field (Fig. 4A), the fly turns syndirectionally with motion over either quarter of the frontal visual field (Fig. 4B,C). Although the individual quarter-field turning responses are smaller in amplitude than the half-field response, the arithmetic sum of the two quarter-field responses exhibits a faster onset and larger amplitude than the half-field response, suggesting that the front field response is saturated (Fig. 4A, dotted red line). As expected, the responses to motion restricted to individual quarter-fields have the same polarity as image motion (Fig. 4D).
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The responses to image motion over the rear-quarter fields, however, follow a different pattern. Whereas clockwise motion across the rear half-field generated counterclockwise turns (Fig. 4E), clockwise motion restricted to the right rear quarter-field generated clockwise turns (Fig. 4F). Due to this difference in polarity, the arithmetic sum of the rear quarter-field responses is much smaller in magnitude than the response to motion over the entire rear half-field (Fig. 4E, dotted red line). Remarkably, the initial polarity of rear quarter-field responses is independent of the direction of image motion. Motion presented to the left rear quarter-field triggered clockwise turns, regardless of the direction of motion (Fig. 4G,H). Thus, only progressive (front-to-back) motion in the rear field of view elicits responses against the direction of motion, opposite the polarity expected of the optomotor reflex (compare panels B, C, F and G in Fig. 4). Inaddition, the temporal properties of rear field responses vary with stimulus direction. Whereas the response to progressive motion over a rear quarter-field steadily decays, the response to regressive motion over the same sector is sustained for the duration of the motion stimulus.
Steady-state responses to translatory optic flow in sensorimotor
closed loop
How are open-loop expansion/contraction responses incorporated into a
functional organization of the flight control system? We examined this
question by allowing flies to control pattern velocity under closed-loop
conditions. In these experiments, animals could control the sign and magnitude
of either rotational velocity (i.e. optomotor closed loop) or
expansion/contraction velocity by adjusting the difference between left and
right wing stroke amplitude. We periodically challenged the fly's capacity to
control pattern motion by adding a sinusoidal bias to the feedback signal.
When flies controlled a full-field rotatory pattern, introduction of the
sinusoidal bias causes them to lose control of pattern velocity, subjecting
them to rapid shifts in image position
(Fig. 5A). Flies were better
able to reduce visual motion for a translating expansion/contraction pattern
(Fig. 5B). To quantify a fly's
ability to control image motion, we measured the variance in pattern velocity
during consecutive 1 s windows throughout the flight sequence. Position
variance was substantially smaller when flies controlled the lateral
expansion/contraction pattern than when they controlled the rotary pattern at
identical gain (Fig. 5C). Thus,
within the confines of the flight simulator, flies can better stabilize
translatory flow than they can rotatory flow.
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The magnitude, time course and polarity of open-loop turning responses to patterns of expansion/contraction indicate that flies robustly and continuously turn away from an expanding stimulus. Therefore, for a steadily translating flow field, bilaterally symmetrical collision avoidance reflexes should equilibrate only when the focus of expansion is centered directly behind the fly. To determine if flies stabilize a pole of expansion, we allowed flies to control the yaw velocity of an expansion pole under closed loop conditions. The strength of the fixation of pole of contraction is best seen in comparison with other closed-loop configurations. If permitted to control the yaw velocity of a rotating checkerboard, flies tend to generate rapid rotations of the pattern that are thought to be analogous to the saccadic turns executed in free flight (Fig. 6Ai). Although they may transiently orient towards a particular feature of the display, on average the flies do not stabilize, or fixate, any preferred position within the random pattern (Fig. 6Aii). By contrast, flies presented with a single vertical stripe in closed-loop tend to smoothly track the object and maintain its position frontally (Fig. 6B). However, the positional variation of object fixation is significantly larger than for fixation of a contraction pole at identical feedback gain (Fig. 6C). We further challenged the fly's ability to control the position of the expanding/contracting flow field by periodically reversing the direction of pattern motion on either side of the animal, thereby instantaneously switching the positions of the expansion and contraction poles. Flies respond by rapidly turning away from the new pole of expansion, fixating the new pole of contraction (Fig. 7A).
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What are the salient visual cues that flies use to locate the position of the foci of expansion and contraction? Flies execute steady-state collision avoidance responses to patterns of image translation without motion at the poles (Fig. 3B), suggesting that the fixation of the contraction pole results from balancing the spatial integral of image flow in the left and right hemispheres. Alternatively, flies might be tracking the apparent `seams' of the flow field the poles themselves. We tested these competing hypotheses by varying the spatial and temporal composition of image motion on one side of a drifting expansion/contraction pattern. The two treatments produced similar results. By either doubling the image velocity (Fig. 7B) or halving the spatial wavelength (Fig. 7C) on one side, the steady-state fixation responses were biased approximately 20° toward the side of the arena containing the lower contrast frequency. Therefore, flies appear to be balancing contrast frequency bilaterally rather than tracking the apparent position of the poles. This integration model also predicts that the time course of the response should vary with contrast frequency. For a bilaterally symmetric drifting pattern of expansion/contraction, increasing contrast frequency from 1.1 Hz to 6.6 Hz results in a 3-fold decrease in the delay to steady-state expansion avoidance (Fig. 7D). Therefore, both the spatial tuning and temporal dynamics of steady-state expansion responses depend upon the contrast frequency of the moving image.
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Discussion |
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Importance of distinguishing translational and rotational flow for
flight control
Flies use patterns of rotational and translational optic flow to maintain
stable flight within visually textured environments. The relative
contributions of rotation and translation to the retinal optic flow field
depend upon the fly's motions, the spatial organization of the visual world,
as well as the respective geometrical constraints on optic flow. For example,
body rotation in the absence of translation generates a flow pattern
consisting of equal local velocity vectors along each meridian of the axis of
rotation. Translation, by contrast, produces a field in which optic flow
radiates outward along meridians from the focus of expansion towards the focus
of contraction.
In response to panoramic image rotation, freely flying hoverflies
(Syritta pipiens) turn in the same direction (syndirectionally) to
minimize retinal slip (Collett,
1980). Counteracting rotational retinal slip, an example of the
optomotor response, is thought to mediate stable forward flight in flies
(Götz, 1975
). During
linear translation, image expansion triggers collision avoidance maneuvers
during free flight in which Drosophila turn away from the pole of
expansion (Tammero and Dickinson,
2002b
). This reflex cannot be based solely on optomotor feedback
because it requires that the animal turns against the direction of image
motion seen within a large portion of its visual field. Our results show that,
when presented with horizontal motion restricted to either the front or rear
hemisphere, Drosophila always turn in the direction of apparent
translation (Fig. 1). Thus, for
ambiguous patterns of optic flow, flies default to translation responses.
Open-loop responses to translational expansion/contraction stimuli are three
times larger than those generated by full-field rotation at an identical
contrast frequency (Fig. 1E).
This amplification of operational gain results in more robust closed-loop
control over the velocity of expansion/contraction than to that of full-field
rotation (Fig. 5). As a result
of the spatial organization of visuomotor responses, when given a choice, the
fly frontally fixates a steadily contracting flow field, a strange situation
that illustrates a very low tolerance for image expansion
(Fig. 6). As soon as an
expansion pole is displaced laterally on the retina, the fly turns away. Thus,
the only stable condition the expansion pole positioned directly
behind the fly results in frontal fixation of the contraction pole.
The positional variance during closed loop is substantially less for a pole of
contraction than for a vertical stripe
(Götz, 1968
;
Heisenberg and Wolf, 1979
;
Wolf and Heisenberg, 1990
). To
our knowledge, expansion avoidance generated by linear image translation is
the most robust visual reflex yet recorded in Drosophila and is
therefore likely to be a fundamental component of the animal's flight control
system.
Model for the spatial summation of translational flow fields
We propose the following model to summarize our findings
(Fig. 8). The progressive (blue
pathway) and regressive (red pathway) motion over each quarter of visual space
is processed via an appropriate temporal filter. For example,
progressive motion over the frontal visual field is processed by a filter
(ffp) with both tonic and phasic step response
characteristics (Fig. 4C). Similarly, the response of the filter sensitive to regressive motion in the
front visual field (ffr) has transient and sustained
components, although the sustained component is somewhat smaller than for that
of progressive motion (Fig.
4B). The polarity of the response to frontal motion always matches
the direction of image motion (Fig.
4BD).
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The processing of motion over the rear visual field is carried out in a similar fashion, with some distinct differences. The filter sensitive to progressive motion over the rear visual field (frp) is dominated by the transient component, whereas the sustained component dominates the filter sensitive to regressive motion (frr). The polarity of the turning responses does not, however, reverse when the direction of motion is reversed. Thus, both progressive and regressive motion over a rear quarter-field causes a turning response of the same polarity. The response to motion over the rear half-field does not result from the summation of the two rear quarter-fields (Fig. 4E, dotted red line). Rather, the response to progressive motion in one quarter-field appears to inhibit the response to regressive motion in the adjacent quarter-field when motion is presented across the rear half-field (Fig. 4). Finally, the output of each temporal filter is spatially summed, integrating motion over the fly's entire field of view. The final sum is then subject to saturation due to the mechanical and temporal limits on the control of wing kinematics. The model predicts that the sum of antagonistic translation commands results in a weak tendency of the fly to turn in the direction of full-field rotation the classic optomotor response. By contrast, for a pattern of lateral translation producing opposing poles of expansion and contraction, similar rightward motion in the front field of view coupled with leftward motion in the rear field of view results in a stronger tendency to turn to the right a collision avoidance response.
New implications for the neural mechanisms of visuomotor
reflexes
For decades, visually mediated reflexes in insects have been used as
behavioral assays to predict and examine structurefunction
relationships within the nervous system at both the cellular
(Bishop and Keehn, 1967;
Hassenstein and Reichardt,
1956
) and molecular-genetic levels
(Fischbach and Heisenberg,
1984
; Götz,
1964a
). The power of this integrative approach emerges from
comparing the dynamics of intact behaviors with the physiological properties
of individual neurons. The new interpretation of visuomotor reflexes presented
here therefore initializes both a search for new physiological mechanisms and
a reinterpretation of current advances.
Most electrophysiological studies of visual processing in flies have
focused on a group of 60 or so motion-sensitive cells in the lobula plate
(Hausen, 1984,
1993
). Some of the lobula
plate tangential cells (LPTCs) show local directional specificity for global
patterns of optic flow (Krapp and
Hengstenberg, 1996
; Krapp et
al., 2001
). As yet, there have been few descriptions of LPTCs
sensitive to expanding flow fields in flies. The Hx neuron responds strongly
to patterns of translatory optic flow emanating from the caudo-lateral visual
field (Krapp et al., 2001
).
Also, Hausen postulated that HS neurons probably participate in encoding self
translation (Hausen, 1984
,
1993
). Furthermore, output
regions in the central brain visit descending neurons that convey visual
signals to the flight motor circuits within the thoracic ganglion
(Strausfeld, 1976
). Several
neurons descending through the cervical connective of the blowfly
(Calliphora erythrocephalia) are sensitive to frontally positioned
image expansion (Borst, 1991
).
In the locust Schistocerca americana, identified descending
contralateral motion detector cells (DCMDs) may play a roll in collision
avoidance or escape behavior by firing in response to looming objects
(Gabbiani et al., 1999
;
Gray et al., 2001
;
Judge and Rind, 1997
). In the
lobula plate of the hawk moth Manduca sexta, `class 2 cells' respond
to an expanding optic flow field (Wicklein
and Strausfeld, 2000
). It may be within similar premotor networks
that the patterns of linear translation and expansion are encoded in
flies.
Why should minimizing lateral translation or avoiding lateral expansion
play such a dominant role in flight control? In both free-flight and
tethered-flight conditions, fruit flies respond to a laterally positioned
focus of expansion by turning away from the focus of expansion (Tammero and
Dickinson,
2002a,b
).
This explains the tendency of Drosophila to saccade away from
approaching walls in free flight, avoiding collisions. Consistent with
free-flight behavior, tethered flies in visual closed loop show
counterdirectional saccades that send an expanding object to the rear field of
view. In the experiments described here, Drosophila appear to be
treating the focus of expansion of a large field pattern as it does an
expanding object, by turning away from the expanding flow field. By contrast,
walking blowflies in which one eye has been occluded show a weak tendency to
turn in the direction of the non-occluded eye, thus turning towards the focus
of expansion (Kern and Egelhaaf,
2000
). However, in flight, monocular animals do not show
trajectories significantly different from their binocular counterparts. Strong
differences in the temporal dynamics of image motion may contribute to varying
behavioral strategies to stabilize gaze during locomotion in walking
vs flying animals.
The most common source of lateral image motion and its associated expansion
is side-slip during free flight, a situation that may occur if an animal is
blown off course by a gust of wind. In response to such lateral translation,
our results suggest that a fly would turn away from the laterally positioned
focus of expansion, reflexively directing it away from any impending
collision. Thus, this reflex and its underlying circuitry might be analogous
to the centering response observed in bees
(Srinivasan et al., 1991). A
specific application of this reflex might be the maintenance of upwind flight,
an essential component of long-distance odor tracking
(Vickers, 2000
).
Mechanosensory structures such as filiform hairs or antennae cannot by
themselves localize the upwind direction, because without an independent
measure of ground speed a flying animal cannot easily distinguish an external
wind from a self-generated component of airflow. Within the natural
environment, the most likely source of side-slip is the drag that results from
yaw relative to wind direction, an effect analogous to leeway on a boat. By
turning to minimize lateral translation and fixate the focus of expansion in
the rear field of view, an animal would tend to steer into the wind. The
expansion avoidance reflex is thus a simple and robust means by which the
animal might avoid obstacles and also maintain an upwind direction.
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Acknowledgments |
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Footnotes |
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