Download J Comp Physiol A (1993) 173:143-149

J Comp Physiol A (1993) 173:143-149
Journal of Comparative
Physiology A
© Springer-Verlag 1993
Optical properties of the ocelli of Calliphora erythrocephala and
their role in the dorsal light response
H. Schuppe*, R. Hengstenberg
Max-Planck-Institut für biologische Kybernetik, Spemannstraße 38, D-72076 Tübingen, Germany
Accepted: 8 April 1993
Abstract. The 3 ocelli of the blowfly Calliphora erythrocephala,
grouped close together an the top of the head (Fig. 1), have large,
extensively overlapping visual fields. Together they view the entire
upper hemisphere of the surroundings plus part of the lower
hemisphere (Figs. 5, 7). It is shown for the lateral ocelli that despite
the underfocussing of the ocellar lens large patterns are imaged an the
receptor mosaic. Because of the astigmatism of the lens, patterns in
longitudinal orientations are more accurately represented than in
others (Fig. 3). Nevertheless, an artifical horizon rotated around the
long axis of the animal does not elicit head roll. Likewise, changes of
overall brightness in the visual field of the median and one lateral
ocellus elicit only weak phasic-tonic "dorsal light responses" of the
animal which supplement the tonic dorsal light responses mediated
by the compound eyes (Figs. 9, 10). Our results show that, in
Calliphora, the ocelli have little influence an head orientation during
flight, and must be assumed to serve other functions.
Key words: Blowfly - Ocelli - Astigmatism - Spatial orientation
Introduction
The visual receptors of Calliphora are arranged in 2 large
compound eyes and 3 small ocelli, the latter located on the vertex of
the head (Fig. l a). The compound eyes comprise about 2 x 6000
ommatidia and are responsible for functions that require good
spatial resolution, such
* Present address: Institut für Zoologie, TH Darmstadt, Schnitt-
spahnstraße 3, D-64287 Darmstadt, Germany
Abbreviations: ß, body pitch angle; δ, head-tilt angle; DNOVS,
descending neuron of the ocellar and vertical cell systems; HR, head
roll; λ, spatial wavelength; R, roll angle; SD, standard deviation
Correspondence to: H. Schuppe
as object fixation, movement detection, and possibly pattern
recognition.
Unlike the compound eyes, each ocellus has only one cuticular
lens which produces an underfocussed image an the retina (Homann
1924; Cornwell 1955). Several 100 photoreceptors converge upon a
few large first order interneurons (4 or 6 L-neurons according to
Nässel and Hagberg 1985). This arrangement tends to equalize local
brightness modulations, and allows to measure mean brightness: In
locusts and dragonflies, the visual fields of the ocelli are centered on
the horizon during flight (Cornwell 1955; Wilson 1978; Stange
1981). Changes of flight attitude shift the horizon within the ocellar
visual fields in a directionally specific manner. The resulting
changes in mean brightness, received by the ocelli, elicit and control
compensatory head movements and flight steering actions (Hesse
1908; Wilson 1978; Taylor 1981; Stange 1981; review Wehner
1987).
In addition it may not be ruled out that brightness distributions
are detected within each ocellar visual field: In each ocellar retina of
Drosophilla the large dendritic fields of L-neurons overlap only
partially (Schmidt 1975). This suggests that L-neurons of the same
ocellus gather information from different parts of the visual
surroundings. Furthermore it has been shown for one of the smaller
first order interneurons of the ocellar retina of the blowfly that this
interneuron responds vigorously to flickering light (Hengstenberg
and Hengstenberg 1980), caused by moving gratings of λ = 30° spatial
wavelength.
The arrangement of ocelli in flies, honeybees, and several other
insect orders (revs. Goodman 1981; Toh and Tateda 1991) differs
from that in locusts and dragonflies. Thus in these insects ocelli may
serve different functions as well (Wellington 1953; Cornwell 1955;
Wehrhahn 1984; Kastberger 1990). We have studied the optical
properties of the ocelli of Calliphora to try to establish for them a
specific function, and behavioral experiments have been made to
test the proposed functions. Some of the results have been published
in preliminary form (Hengstenberg 1985).
144
H. Schuppe, R. Hengstenberg: Optical properties and functional role of the dorsal ocelli of Calliphora
Fig. 1. a Dorsal view of part of the head of a female Calliphora; arrows:
ocelli; ce, compound eye; ant., anterior; post., posterior; scale bar,
200 µm. b Schematic drawing of a tangential (horizontal) section of the
ocellar region of the head capsule, showing the retinas (pigmented zones
stippled) and thickened cuticular regions (black) adjacent to the retinas
in the interior of the head; the boundary between thickened cuticle and
retina in the lateral ocelli is at a slight angle to the long axis of the
body; lat., lateral; scale bar 50 µm. c Transverse section through a
lateral ocellus; the retina is below and somewhat medial to the cuticular
lens (l), from which it is separated by a narrow corneageal layer (cl).
The photoreceptor layer is subdivided into a rhabdomere zone (rz), a
pigmented zone (pz) and a basal zone (bz). n, neuropil; cu, cuticle; icu,
internal region of thickened cuticle, within the head capsule; scale bar
20 µm
Fig. 2a, b. Experimental arrangement devised to determine (i) the
resolution of the lenses of the lateral ocelli and (ii) their astigmatism for
patterns in various orientations. A piece of cuticle (C) containing the
lenses of both lateral ocelli was placed in a closed chamber (not shown)
under a microscope (M). The optical axis of one of the lenses (L)
roughly coincided with the optical axis of the microscope. A test pattern
(P) was displayed from below in a plane perpendicular to the optical
axis of the microscope and of the lens. The test pattern consisted of a
sinusoidally modulated grating in various orientations (a and b). The
spatial frequency of the test pattern was variable. The distance between
test pattern and lens of the ocellus was large compared to the focal
length. E , eye of the observer; DV, dorsoventral axis of the
preparation
Materials and methods
corresponding focal plane. The image distance was determined by
means of an electronic dial gauge and corrected for the refractive index
of the physiological saline.
The spatial cut-off frequencies were measured by test patterns of
varying spatial wavelengths displayed on an oscilloscope in front of the
preparation (below the lens in Fig. 2). For each spatial wavelength,
the microscope was focussed an different planes behind the inner lens
surface to determine the distance from the lens at which the contrast
of the test pattern (i.e. maximum and minimum brightness) reversed for
the first time. For this particular distance the spatial frequency of the test
pattern corresponds to the spatial cutoff frequency of the system.
All the experiments employed wild-type female Calliphora erytrocephala
(Meig) taken from a laboratory colony.
Optical measurements. Investigations were performed on lens
preparations using a modification of Homann's (1924) hanging drop
method. A piece of cuticle containing the lenses of both lateral ocelli was
dissected out of the head capsule and transferred to a closed chamber
consisting of a plastic ring between two cover slips. Two small strips of
0.15 mm glass were glued at a distance of 1 mm to the underside of the
upper coverslip, and physiological saline solution (Case 1957; index of
refraction 1.34, adjusted with bovine serum albumin) was placed between
them. The lens preparation was laid on the surface of the saline solution
from below, with the inner surface of the lenses directed upwards, and
covered by the solution. The chamber containing the preparation was
placed under a microscope and the light beam was centered on one of
the lenses aligned with its optical axis (Fig. 2). By using a fluorite
objective (magnification 40 x) with a numerical aperture of 0.75 (which is
large enough to accommodate the whole of the physiological ray bundle)
the imaging of test patterns was studied.
To determine the focal planes of the ocellar lenses, a test pattern in the
form of a cross was positioned at a distance of 132 mm from the lens,
and the microscope optics were focussed onto one of the image planes.
Because the image distance was always small with respect to the object
distance, the image was expected near the
Histology. Heads of flies were fixed in phosphate-buffered formaldehyde-glutaraldehyde solution (Karnovsky 1965), passed through a
graded ethanol series, contrasted en bloc overnight (5% uranyl acetate +
1 % phosphotungstic acid in 70% ethanol) dehydrated and embedded in
Araldite®. The embedded material was cut alternately for light and
electron microscopy. Transverse sections of the ocelli were made from
one preparation and sagittal sections from another. In addition B. Rosser
supplied us with paraffin serial sections of the ocelli. Figure la shows a
scanning electron micrograph of a preparation prefixed by the
method of Karnovsky (1965), dried at the critical point in ethanol/CO2
and sputtered with goldpalladium.
Electroretinograms (ERGs). The ocellar ERG in an isolated fly head
was recorded in order to measure the visual fields of the ocelli.
H. Schuppe, R. Hengstenberg: Optical properties and functional role of the dorsal ocelli of Calliphora
To prevent interference from the ERGs of the compound eyes, these
structures were removed together with a major part of the optic
lobes; the cut surfaces were occluded. Using the method described by
Metschl (1963), a glass capillary electrode (1 M KCl; ca. 20-30 MΩ)
was inserted near the transition from ocellar neuropil to the ocellar nerve.
The reference electrode was placed in the occipital foramen of the fly's
head.
During the experiment the head preparation was mounted in a
perimeter where it could be illuminated from various directions by a
light guide, 1 mm in diameter, that was rotated at a distance of 9 mm
about a point midways between the 3 ocelli. The stimulus was white light
from a xenon XBO 150-W-lamp; the irradiance at the ocelli was ca.
10 mW/cm while the background brightness contributed no more than
0.02 µW/cm2. Before a test series was begun, the preparation was darkadapted for 5 min. A series consisted of the computer-controlled
presentation of 10 light pulses of 30 ms duration, presented at intervals
of 1 s. After each sequence of 10 pulses, the position of the light guide
was changed in steps of 30° and, after 1 min, a new sequence was
presented. In averaged ERGs the amplitude of the first positive
transient (base to peak) was measured.
Behavioral studies. The visually induced head-rolling response was
studied by analyzing video recordings of the frontal aspect of animals
flying while tethered in a wind tunnel (for details see Hengstenberg et al.
1986). The wind tunnel held a pattern cylinder, coaxial with the body
axis of the fly, and the pattern consisting of a bright "sky" and a dark
"ground" could be rotated about the fly by a servomotor.
In another experiment the interior of the wind tunnel was illuminated
homogeneously. One of the lateral eyes was blinded with black paint
and the ambient brightness was changed in a single step. Again, the head
rolling reaction was recorded on video tape.
Fig. 3. Imaging characteristics of preparations of the lenses of the lateral
ocelli of Calliphora determined with the experimental arrangement
shown in Fig. 2. To find the distance from the lens at which the
image of the test pattern reversed its contrast the microscope was
focussed onto various planes behind the ocellar lens. The spatial
frequency of the pattern at this distance indicates the cutoff frequency.
The figure shows a relationship between cutoff frequency (spatial
wavelength) and distance from the back surface of the lens. The two
curves in the figure were obtained with two orthogonal orientations
of the test pattern, as illustrated by the insets. Here the
145
Head tilt was studied in free flight. In each test, 50-100 intact
Calliphora females were placed in a cage measuring 50 cm on each edge.
The animals were startled into flight and photographed shortly later.
Head tilt angle S (the angle between the posterior plane of
the head and the vertical) and pitch angle ß (orientation of the long axis)
of the body were extracted from the photographs.
Results
Ocellar optics. In lateral ocelli the focal planes of the lenses
were clearly behind the microvillar zones which began 7-19
µm behind the inner surface of the lens, the microvillar zone
being about 8 µm high (Fig. 3). These values were derived
from 6 ocelli (maximum diameter 53-63 µm) measured in a
direction perpendicular to the center of the lens surface
(the "optical axis"). Focal planes were measured in 5 lenses
of lateral ocelli. They were found to have two focal planes
along the optical axis : one at an average distance of 58 ±
21 µm SD and a second one at 96±29 µm SD from the inner
lens surface. All lenses had an oval shape with the major axis
roughly parallel to the long axis of the body. The mean
diameters of the 5 lenses were 76 ± 13 µm SD parallel to the
long axis of the body and 64 ± 8 µm SD parallel to the
transverse axis.
The oval shape of the lenses and the presence of two
focal planes indicate a pronounced astigmatism. This was
tested in two additional measurements which showed that
astigmatism is also noticeable in image transmission.
head of the fly is shown from above, the dorsoventral axis slightly tilted
sideways; the stripes of the pattern are either parallel to the long axis of
the body (lower picture, lower curve) or perpendicular to it (upper
picture and curve). At all distances from the lens, the cutoff frequency is
lower for stripes perpendicular to the long axis of the head than for a
parallel orientation. The symbols in the curves indicate the means and
standard deviations for 5 ocellar lenses. The axial extent of the
microvillar zone is indicated on the scale on the right
146
H. Schuppe, R. Hengstenberg: Optical properties and functional role of the dorsal ocelli of Calliphora
A test pattern of parallel stripes was arranged horizontally below the
chamber containing the preparation i.e. approximately perpendicular to
the optical axis of the tested lens (Fig. 2). The stripes were presented in
two orthogonal orientations. The spatial cutoff frequency, measured at a
particular distance behind the lens, depended on the orientation of the striped
pattern : when the stripes were parallel to the long axis of the body (Fig.
3, lower inset) the spatial cutoff frequencies were distinctly higher (Fig. 3,
lower curve) than when the stripes were oriented across the body axis
(Fig. 3, upper inset and upper curve). In the region of the microvillar zone,
15 µm behind the lens, stripes parallel to the long axis of the body were
transmitted down to a spatial wavelength averaging 56°. With patterns
rotated by 90°, the (extrapolated) limiting value was ca. 135° spatial
wavelength. In the anterior focal plane as well, striped patterns were
imaged more sharply if the stripes were parallel to the long axis of the body.
In the posterior focal plane, however, imaging of stripes was better when
they were oriented transversely.
A photomicrograph of a section through the lateral ocellus was used to
make a crude reconstruction of the optical acceptance region at various
points in the retina of the lateral ocellus (Fig. 4). As a consequence of
underfocussed optics, the angular region from which light is incident on
the tip of the individual photoreceptor cell is not equivalent with the image
forming ray path. At the tip of photoreceptors the optical acceptance region
is particularly large in the part of the retina under the middle of the lens
(Fig. 4a). lt is relatively small in the retinal region below the edge of the
lens (Fig. 4c). Hence objects located at the sides of the animals are imaged
especially sharply on the retina.
Visual fields of the ocelli. During walking, as in flight, the combined
ocellar visual fields cover the entire upper hemisphere of the surroundings
and some part of the lower hemisphere. The visual fields of the lateral ocelli
are not centered exactly sideways but are shifted slightly backwards. This
corresponds to the orientation of the retinae (Fig. lb) each containing
about 220 photoreceptor cells (mean of two lateral ocelli). The extent of
each visual field, both of the lateral and median ocelli as determined by
our ERG-measurements (Figs. 5, 7) corresponds fairly closely to
Cornwell's (1955) data on the boundaries of the visual fields. With the
nearly flat back surface of the head (posterior plane of the head) perpendicular to the horizontal plane, the ERG-amplitudes were largest, when
the stimulus was at an elevation of 30° (Fig. 5). Thus the stimulus direction
for maximal ERGamplitude does not coincide with the optical axis which
is about 70° above the horizontal in the case of the median ocellus and ca.
75° in the lateral ocelli. This discrepancy can be ascribed to the off center
position of the retina (Fig. lc).
In flight, as a rule, the posterior plane of the head is tilted backwards the
angle between head and body being relatively constant (Fig. 6a, b). The
average head-tilt angle 8 of the animals flying in the cage was 29° ± 15°
SD. Thus in flight the stimulus direction for maximal
Fig. 4a-c. Angular region from
which light is incident at 3
different sites of the retina of the
lateral ocellus of Calliphora. lt is
emphasized that each of these
sites is out of focus. For each
retinal position the angle
between the limits of the
acceptance region is indicated.
The reconstruction is based on
the assumptions that the lens
material has an effective
refractive index of 1.55
(Cornwell 1955) and that the
refractive index of the corneageal layer between lens
and retina is 1.34 (see above).
The acceptance region is
delimited by either the edges of
the lens or by the limiting angle
for total reflection
Fig. 5. Visual fields of the median (left) and a lateral (right) ocellus
when the posterior plane of the head is vertical. The height of the thick
black bars represents the amplitude of the first positive transient in the
ocellar ERG, as a function of the direction of the stimulus light
source. Thin bars: standard deviation. The data were obtained from 4
median and 4 lateral ocelli, and all values were normalized - with
respect to the response amplitude for a stimulus at the horizontal
position in the sagittal plane (median ocellus) or 30° above the
horizontal in the transverse plane (lateral ocelli). The drawings in the
middle column show the orientations of the test planes. D, dorsal; V,
ventral; R , right; L, left; A, anterior; P, posterior; • indicates a
posterior position where the light stimulus is obscured by the body
H. Schuppe, R. Hengstenberg: Optical properties and functional role of the dorsal ocelli of Calliphora
Fig. 6. a Histogram of head angles of Calliphora flying freely in a cubic
cage measuring 50 cm on each edge. During flight the head
is tilted backwards. δ, angle between the posterior head plane and the
vertical (head-tilt angle). n, frequency of observations per bin of 5° width.
b Relationship between head-tilt angle and body pitch angle in freeflying Calliphora; the two are approximately linearly
correlated (both regression lines are shown). In long-distance straight
flight, the body is presumably kept relatively close to the
horizontal (and hence the head nearly vertical). ß, angle between the body
axis and the horizontal. c Visual field of the median ocellus
of Calliphora in flight. As in Fig. 5, the normalized amplitude of the
ocellar ERG (black bars) is shown as a function of stimulus direction. The data are for the median sagittal plane (Fig. 5) and adjusted for a
head-tilt angle of 29°
147
Fig. 7. Visual fields (stippled) of the median ocellus (a), and thy right
lateral ocellus (b) in a flying Calliphora. The diagrams an based on a
head-tilt angle of 29°. The boundaries of the visual field in the graphs
separate stimulus positions at which an ERG wa elicited and the
adjacent positions at which the averaged ERG amplitudes were
indistinguishable from the residual noise. On the left is represented the
part of the visual field within the anterior hemisphere, and on the right
the part in the posterior hemisphere R , right; L, left
ERG-amplitude was at an elevation of roughly 60° in case of
the median ocellus (Fig. 6c).
Responses to roll motion of longitudinal contours. The
astigmatism of the lens (Fig. 3) and the reduced optical
acceptance angle of lateral ocelli in lateral parts of the visual
field (Fig. 4) suggest that vertical movements of longitudinal Fig. 8. Visually elicited compensatory head-rolling of Calliphora in
contours may be perceived through the ocelli if the appropriate response to sinusoidal pattern movement as obtained during tethered
flight within a patterned cylinder which can be turned around the fly's long
neural connections were made.
axis. Top trace: angular position of the pattern as a function of time. At
To test this hypothesis, a pattern cylinder consisting of a 0° the boundary between the bright and dark halves of the pattern is
dark "ground" and a bright "sky", with the "horizon" horizontal. Middle trace: head-rolling (HR ) after occlusion of the ocelli.
placed at its natural position, was rolled sinusoidally (1 Hz, The head follows the pattern motion. Bottom trace: HR after the
compound eyes have been occluded; the head is turned independent of the
±90°; Fig. 8, top trace) around a fly flying stationarily in the pattern motion
wind-tunnel. Head roll movements were observed in flies
where either the 3 ocelli or both compound eyes were occluded
by black paint (Fig. 8). If the ocelli are occluded (Fig. 8,
middle trace), flies roll their head in phase with the stimulus, flies roll their head erratically (Fig. 8, lower trace), as in
apparently in an attempt to stabilize their head with respect to darkness. The lack of a distinct phase relationship with the
the visual surround. If, however, the 2 compound eyes are oc- stimulus motion demonstrates that, surprisingly, the contour
cluded, and the stimulus is presented through the ocelli,
motion is not sensed through the ocelli.
148
H. Schuppe, R. Hengstenberg: Optical properties and functional role of the dorsal ocelli of Calliphora
Fig. 9. a Phasic-tonic head-rolling of Calliphora in response to an
increase in ambient brightness, after occlusion of a lateral ocellus
(black dot). b Control without occlusion. Bottom trace: ambient light
intensity; baseline, surroundings dark (luminance I<10 cd/ m2 );
2
upward step, surroundings bright (I=4000 cd/m ). The light source
was a Philips TL fluorescent ring lamp, white 33 driven at 24 kHz.
HR, head-rolling; t , time; N, number of animals tested; n ,
number of trials
Contribution of the ocelli to the dorsal light response.
The skewed transverse sensitivity distribution of the
lateral ocelli (Fig. 5) lends itself to the design of a
simple roll detector: If the center of brightness is
assumed to be located in the zenith, the difference in
excitation (E) between the right (r) and the left (1)
ocellus, to light impinging vertically, is a linear
measure of roll angle R = c(Er-El) between - 60° < R <
+ 60° (c = const.). Beyond that range, up to the
receptive field boundaries, there is still a sizeable
signal of correct sign to control compensatory roll
turns.
This kind of detector can be maximally stimulated
when one, e.g. the left, lateral ocellus is occluded by black
paint, and the whole receptive field of the intact right
ocellus is stimulated by stepwise diffuse illumination
(Fig. 9) : In darkness the output of both ocelli is
nought, likewise the difference between the two and
consequently also the compensatory roll torque. At
"lights on", the right ocellus is maximally stimulated, as
if it were directed towards the center of brightness
whereas the occluded left ocellus remains unstimulated. In
this situation a head roll to the right (HR >0°) would
seem appropriate to correct, in free flight, the
apparent misalignment. The result of this experiment is
shown in Fig. 9: flies turn, in fact, their head in a
phasic-tonic manner in the expected direction (300 ms
time to peak) but the response is fairly small in
comparison to the variation of the responses. It
Fig. 10. a Tonic head-rolling of Callipho ra in response to an increase in
ambient brightness, after occlusion of a compound eye (black
area). b Control without occlusion. Bottom trace and abbreviations as in
Fig. 9
seems therefore unlikely that the ocelli are present in flies to
provide only this function.
If the same experiment is made with unilateral occlusion of a compound eye and all ocelli are left intact, a big
response in the same direction is elicited (Fig. 10). It rises
much slower (2-3 s time to peak) and maintains a
large steady state level (HR 40 ° ) over a long time.
Discussion
Calliphora ocelli are underfocussed astigmatic eyes (Fig.
3) with a skewed sensitivity profile (Figs. 5, 6). Their wide
visual fields are directed upwards and largely overlapping (Figs. 5, 6, 7). This conforms to the general
notion that ocelli, having low spatial resolution, function as
widefield brightness sensors.
But ocelli are not completely diffuse light sensors:
Coarse patterns are imaged onto the retina and there
is a preference for patterns in longitudinal orientations due
to the oval shape of the lenses having different curvatures
along the minor and major axis. Nevertheless, experiments with a pattern of 360° spatial wavelength (certainly
imaged onto the retina) showed that ocelli do not
utilize longitudinal patterns for control of head roll
(Fig. 8).
There is a minute contribution of ocelli to the dorsal
light response. In dorsal light response the head is turned with
its dorsal side towards the center of brightness, even if there
isn't any movement stimulus. This response can be
elicited by a steplike unequal illumination of both
H. Schuppe, R. Hengstenberg: Optical properties and functional role of the dorsal ocelli of Calliphora
lateral ocelli which corresponds to a sudden illusory
misalignment of the head (Fig. 9). The response elicited by
the ocelli is in the correct direction, but of very small size
compared to the dorsal light response that is mediated
by the compound eyes (Fig. 10). The results shown in
Figs. 9 and 10 suggest that the lateral ocelli contribute to
the control of the initial phase of the dorsal light response,
whereas the compound eyes mediate mainly the steady
state phase. But even in the initial phase, i.e. 100 ms after
stimulus onset, the compound eye component of the dorsal
light response is more than 3 times as large as the ocellar
component.
A dorsal light response was not observed in experiments in which a moving 360° pattern was used as stimulus, though pattern movement was accompanied by
changes in overall brightness of different sign in the
visual fields of each lateral ocellus. This was obviously due
to the comparatively smaller and slower contrast changes
under these stimulus conditions. Moreover, even in
experiments in which the ambient brightness was
changed in a stepwise manner a small head roll response
was seen only after statistical averaging of many trials.
Therefore in Calliphora, under natural stimulus conditions, the ocellar dorsal light response has apparently
little influence on head posture during flight. This is in
contrast to the role of ocelli in locusts and dragonflies
where brightness changes in the visual fields of lateral
ocelli cause strong head roll responses (Taylor 1981;
Stange 1981).
The organisation of the visual fields suggests that
ocelli gather information mainly from the dorsal hemisphere of the visual surroundings. The dorsal hemisphere is
richly structured in some of the natural habitats of
Calliphora, among which are forests (Gregor and Povolny
1964; Nuorteva 1966; Isiche et al. 1992), and thus may provide
visual cues for spatial orientation. However, up to now
there is only some electrophysiological indication
(Hengstenberg and Hengstenberg 1980) but no behavioral
evidence that coarse patterns, transmitted onto the
retina, may be detected by the ocelli of Calliphora.
The ocellar dorsal light response and behavioral observations on the orientation of walking flies (Cornwell
1955) suggest that in Calliphora the ocellar system complements the compound eye system to a certain degree,
especially in the fast dynamic range, with regard to the
dorsal light response. Neuroanatomical findings as well
indicate a relationship between the ocellar and optomotor systems: In the central nervous system of Calliphora interneurons of the ocellar system (L-neurons)
synapse with descending neurons (DNOVS 1-3) that also
receive input from movement-sensitive neurons of the
compound eyes (Strausfeld and Bassemir 1985). Thus
future work will have to concentrate not only on the
search for specific behavioral responses, mediated by the
ocelli, but will also have to consider how both visual
systems act in concert and, perhaps, influence each other.
Acknowledgements. We thank Professor Dr. K.G. Götz and the
members of his group for stimulating discussions, Mr. N. Bayer for
149
excellent technical assistance, Mrs. K. Bierig for her help in preparing
the figures and two anonymous referees for their instructive comments.
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