* Your assessment is very important for improving the workof artificial intelligence, which forms the content of this project
Download J Comp Physiol A (1993) 173:143-149
Survey
Document related concepts
Magnetic circular dichroism wikipedia , lookup
Confocal microscopy wikipedia , lookup
Nonlinear optics wikipedia , lookup
Fourier optics wikipedia , lookup
Anti-reflective coating wikipedia , lookup
Nonimaging optics wikipedia , lookup
Optical coherence tomography wikipedia , lookup
Optical illusion wikipedia , lookup
Lens (optics) wikipedia , lookup
Schneider Kreuznach wikipedia , lookup
Interferometry wikipedia , lookup
Retroreflector wikipedia , lookup
Transcript
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. References Case R (1957) Differentiation of the effects of pH and CO2 on spiracular function in insects. J Cell Comp Physiol 49:103-113 Cornwell PB (1955) The functions of the ocelli of Calliphora (Diptera) and Locusta (Orthoptera). J Exp Biol 32:217-237 Goodman LJ (1981) Organisation and physiology of the insect dorsal ocellar system. In: Autrum H (ed) Comparative physiology and evolution of vision in invertebrates. Invertebrate visual centers and behavior II (Handbook of sensory physiology, vol VII/6C). Springer, Berlin Heidelberg New York, pp 201-286 Gregor F, Povolny D (1964) Eine Ausbeute von synanthropen Fliegen aus Tirol. Zool Listy 13:229-248 Hengstenberg R (1985) Zur Bedeutung der Ozellen für die Roll wahrnehmung bei Calliphora. Verh Dtsch Zool Ges 78:228 Hengstenberg R, Hengstenberg B (1980) Intracellular staining of insect neurons with procion yellow. In: Strausfeld NJ, Miller TA (eds) Neuroanatomical techniques. Insect nervous system. Springer, New York Heidelberg Berlin, pp 308-324 Hengstenberg R, Sandeman DC, Hengstenberg B (1986) Compensatory head roll in the blowfly Calliphora during flight. Proc R Soc Lond B 227:455-482 Hesse R (1908) Das Sehen der niederen Tiere. G Fischer, Jena, pp 1-47 Homann H (1924) Zum Problem der Ocellenfunktion bei den Insekten. Z Vergl Physiol 1:541-578 Isiche J, Hillerton JE, Nowell F (1992) Colonization of the mouse cadaver by flies in southern England. Med Vet Entomol 6:168-170 Karnovsky MJ (1965) A formaldehyde-glutaraldehyde fixative of high osmolality for use in electron microscopy. J Cell Biol 27:137A Kastberger G (1990) The ocelli control the flight course in honeybees. Physiol Entomol 15:337-346 Metschl N (1963) Elektrophysiologische Untersuchungen an den Ocellen von Calliphora. Z Vergl Physiol 47:230-255 Nässel DR, Hagberg M (1985) Ocellar interneurones in the blowfly Calliphora erythrocephala: Morphology and central projections. Cell Tissue Res 242: 417-426 Nuorteva P (1966) Local distribution of blowflies in relation to human settlement in an area around the town of Forssa in South Finland. Ann Entomol Fenn 32:128-137 Schmidt B (1975) Die neuronale Organisation in den Ocellen von Drosophila. Thesis, Universität Freiburg i. Br. Stange G (1981) The ocellar component of flight equilibrium control in dragonflies. J Comp Physiol 141:335-347 Strausfeld NJ, Bassemir UK (1985) Lobula plate and ocellar interneurons converge onto a cluster of descending neurons leading to neck and leg motor neuropil in Calliphora erythrocephala. Cell Tissue Res 240:617-640 Taylor CP (1981) Contribution of compound eyes and ocelli to steering of locusts in flight 1. Behavioural analysis. J Exp Biol 93:1-18 Toh Y, Tateda H (1991) Structure and function of the insect ocellus. Zool Sci 8:395-413 Wehner R (1987) "Matched filters"-neural models of the external world. J Comp Physiol A 161:511-531 Wehrhahn C (1984) Ocellar vision and orientation in flies. Proc R Soc Lond B 222:409-411 Wellington WG (1953) Motor responses evoked by the dorsal ocelli of Sarcophaga aldrichi Parker, and the orientation of the fly to plane polarised light. Nature (Lond) 172:1177-1179 Wilson M (1978) The functional organisation of locust ocelli. J Comp Physiol 124:297-316