First published online March 27, 2009
Journal of Experimental Biology 212, 1170-1184 (2009)
Published by The Company of Biologists 2009
doi: 10.1242/jeb.027060
Variability of blowfly head optomotor responses
R. Rosner1,2,*,
M. Egelhaaf1,
J. Grewe3 and
A. K. Warzecha1,2
1 Lehrstuhl für Neurobiologie, Universität Bielefeld, Bielefeld,
Germany
2 Psychologisches Institut II, Westfälische Wilhelms-Universität
Münster, Münster, Germany
3 Abteilung Biologie II, Ludwig-Maximilians-Universität München,
München, Germany
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Fig. 1. Scheme of a laterally filmed tethered fly with the legs and wings removed.
Haltere and head were labelled with infrared-light-reflecting markers (here
red dots) to enable evaluation of their movements. For analysis of the image
data, two regions of interest (ROIs), illustrated as orange rectangles, were
positioned upon the haltere and head, respectively. Haltere position was
determined as outlined in the text. In the zoomed ROI, it is indicated how the
head pitch angle was determined. The grid in the upper right corner of the
zoomed ROI illustrates pixel columns (in y-direction) and rows (in
x-direction) in the image. Four straight lines interconnect the
markers.  illustrates the angle subtended by one of these lines with
the horizontal. The mean angle of the four lines with the horizontal
determines the pitch angle of the head in this particular image frame. (Scheme
of fly courtesy of Christian Spalthoff.)
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Fig. 2. A single stimulus sequence (trial) and inter-stimulus pause. Trials (red)
were separated by pauses with a blank screen (black). This sequence was
experienced several hundred times by the fly in each experiment. One trial
consisted of a reset stimulus shown on the monitor, stimulating the fly to
reposition its head in a starting position. Subsequently, a random dot pattern
first remained motionless and then moved downwards, inducing the optomotor
head pitch response analysed in the present study. Image data were acquired
for 378 ms (blue) starting 200 ms prior to pattern motion onset.
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Fig. 3. Bimodal distribution of high-frequency head jitter (above 90 Hz). Frequency
histogram of the strength of head jitter of one fly evaluated within 20 ms
bins. All traces obtained from the fly were used for the histogram. The
bimodal distribution indicates the existence of two distinct states of
behavioural activity of the fly going along with little or no head jitter
(left peak) and conspicuous head jitter (right peak), respectively. Between
the two peaks a threshold value was set (grey vertical line) to classify data
according to these two states.
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Fig. 4. Example traces illustrating head optomotor pitch and head jitter movements.
Four example traces are shown with head jitter throughout the trial (yellow),
no large amplitude jitter at all (black), one trace starting with head jitter
and ending without jitter (green) and one trace starting without large head
jitter but starting jitter within the trial (red). The traces were aligned to
have zero mean in a 50 ms interval starting 42 ms before stimulus motion
onset. When the fly shows conspicuous head jitter, the optomotor response is
stronger than without jitter.
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Fig. 5. Optomotor responses of one fly separated in traces without (A) and with (B)
conspicuous head jitter. All traces of one typical experiment with, B, or
without conspicuous head jitter, A, throughout the trial are shown. Visually
induced head deflections are larger and more variable in amplitude when going
along with conspicuous head jitter than without. Note the different scaling of
the ordinates in A and B.
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Fig. 6. For each fly the mean head deflection is shown for responses with and
without conspicuous head jitter. Dotted lines illustrate the means across
flies in the two states. (A) For each fly, as well as for the mean across
flies, the visually induced head deflections are considerably larger when
going along with large head jitter. Before motion onset, the head position is
not stable but drifts consistently downwards/upwards for mean responses of
trials with/without large head jitter. The upward shift in traces without
conspicuous jitter is hardly visible due to the scaling. (B) Head drift was
compensated for each individual trial before averaging. Head pitch responses
are still larger when accompanied by jitter.
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Fig. 7. Mean amplitude of the head pitch response for each of six flies. Head pitch
was determined at the end of the trial, i.e. 178 ms after stimulus motion
onset. (A) Before and (B) after drift compensation. The numbers below data
points denote number of individual trials without (black) and with (grey) head
jitter. Error bars denote standard deviations. For each fly, head pitch is
larger when going along with conspicuous head jitter irrespective of drift
compensation.
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Fig. 9. Power spectra of haltere oscillation and head jitter. Power spectrum of a
50 Hz high-pass filtered head orientation trace (grey, right ordinate) and of
haltere oscillations (black, left ordinate). The fly was filmed from the side
to resolve the haltere oscillation frequency. The peak head jitter frequency
of about 125 Hz corresponds well with the haltere oscillation frequency.
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Fig. 10. Head pitch and thorax movements in the two activity states (high and low).
The fly was filmed ventrally. (A) When the halteres did not oscillate, neither
the head position (upper trace) nor the thorax position (lower trace)
fluctuated with amplitudes resolvable by our technical equipment. (B) When the
halteres oscillated, the head (upper trace) showed peculiar head jitter but
the thorax (lower trace) did not.
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Fig. 11. Bimodal distributions of concurrently filmed high-frequency haltere
movements and head jitter of one fly. (A) Frequency histogram of the strength
of haltere movements for one of the two ventrally filmed halteres evaluated
within 20 ms bins. All traces obtained from the fly were used for the
histogram. The distribution of haltere movements is bimodal. Two activity
states can be distinguished; large haltere oscillations (right peak) and small
or no haltere oscillations (left peak). (B) Same as in A but for ventrally
filmed head jitter movements. The bimodal distribution indicates the existence
of two distinct activity states of the head with no head jitter and
conspicuous head jitter, respectively. Between the two peaks, threshold values
were set (grey vertical lines) for haltere movements and head jitter,
respectively, to classify data according to the two activity states.
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Fig. 12. Concurrency of head jitter and haltere movements. Percentages of 20 ms time
bins with the four combinations of occurrence and non-occurrence of haltere
oscillations and head jitter for four experiments on different flies. All bins
in which at least one haltere oscillated were classified as `haltere
oscillation'. (A) Percentages of time bins relative to all bins of one
experiment. In (B) these time bins were not taken into account during which
neither halteres oscillated nor the head jittered. The total number of bins
taken into account is shown on top of each column.
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Fig. 13. Activity state transitions in a ventrally filmed fly. (A) Transition from
low-to-high activity state within one trial. Speed of both halteres (grey
lines, left ordinate) and head speed (black line, right ordinate) as a
function of time. The head starts accelerating and thus undergoes a state
transition before the halteres do (see also inset for finer temporal
resolution). Therefore, haltere oscillations cannot account for the
accelerated head movement. (B) Transition from high-to-low activity state. The
head stops jittering before the halteres stop oscillating, indicating that
haltere oscillation is not sufficient for head jitter.
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Fig. 14. Changes in head movements after ablation of both halteres. The fly was
filmed laterally. Before (A) and after (B) ablation of both halteres. Left:
the measured head orientation traces of all trials are displayed, irrespective
of whether there was an activity state transition within a trial or not. These
transitions explain why the separation into high and low activity state
responses appears less clear than in Fig.
5. The traces were aligned to have zero mean in a 50 ms interval
starting 42 ms before stimulus motion onset. Right: histograms of
high-frequency head jitter strength. (C) Two example traces with high
optomotor gain and two example traces with small optomotor gain. Both high
gain traces, the one before (grey) and the one after (black) haltere ablation,
show head jitter. But B (right) indicates a reduction in head jitter
strength.
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Fig. 15. Diagram illustrating our current hypothesis about the mechanisms that
modify the gain of visually induced head pitch and the origin of the head
jitter. A motor command from the central nervous system initiates the fly to
walk or fly. Additionally the central nervous system elevates the gain of head
optomotor responses (red arrow). Movements associated with locomotor
behaviour, namely haltere oscillations, are sensed by the mechanosensory
system and cause head jitter movements (green arrow). On the basis of our
experiments, it remains open whether the signal from the halteres contributes
to modifying the gain of optomotor head pitch responses. Note, that this
diagram is not meant to capture the entire complexity of the sensory motor
interface controlling head pitch movements. It only shows the relation between
those parts of the system that are the focus of the present study. Sens. mot.
trans., sensory-motor transformation.
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© The Company of Biologists Ltd 2009
