George Adrian Horridge

Visual figure–ground discrimination in the honeybee: the role of motion parallax at boundaries

Free flying bees were trained to collect a reward of sugar-water from a structured figure, placed at a randomly varying location on a sheet of transparent Perspex, positioned 5 cm above a structured Background. During subsequent tests, done in the absence of a reward, the bees’ landings on the boundaries of the figure, as well as within the figure and outside it, were recorded. The same bees were also tested with the figure placed directly on the background, thus eliminating the difference in height between the figure and the background. The results of both types of tests were then compared to identify and investigate the cues that bees use to detect a structured figure, when presented over a structured background. The structure of both the figure and the background were varied in a series of experiments, training a fresh group of bees in each experiment. A randomly structured figure presented against a randomly structured background cannot be detected by the bees unless it is raised above the background. A height difference of 2 cm is sufficient to elicit a rate of landings on the figure that is significantly higher than the chance level. The detectability of the figure does not depend upon the shape of the figure or on differences in density between the structures of the figure and the background. Thus, in detecting the raised figure, the only cue used by the bees appears to be the apparent motion of the figure relative to the background. The majority of landings on a raised figure occur at its boundaries. This shows that the visual stimulus that is crucial in detecting the figure is the local discontinuity in apparent motion that occurs at the boundary. We refer to this as ‘boundary parallax ’. In a series of experiments that used a striped background and a variety of structured figures, three different types of boundary parallax were offered to the bees. These were: (i) ‘covering parallax’, at a boundary in which stripes on either side of the boundary are parallel to the boundary; (ii) ‘shearing parallax’, in which stripes on either side are perpendicular to the boundary and (iii) ‘orthogonal parallax’, in which the stripes on one side are perpendicular to those on the other side. The bees performed very well at detecting raised boundaries that offered covering or shearing parallax, despite the fact that such boundaries are not readily discernible on the basis of their static geometry. On the other hand, bees performed poorly in detecting raised boundaries that offered orthogonal parallax, despite the fact that such boundaries are geometrically quite vivid to the human eye. We propose two neural models for the detection of boundary parallax that account for the sensitivity of bees to covering and shearing parallax and their insensitivity to orthogonal parallax.

The superposition eye of skipper butterflies

1. The anatomy of the eye is described in seven representative genera of Australian Hesperioidea. Between the crystalline cones and the long rhabdom is a wide clear zone crossed by narrow extensions of the retinula cells. The distal pigment remains between the cones even in daylight. 2. No evidence of functional light guides crossing the clear zone could be found. 3. A real erect image is formed on the receptor layer. The acuity and origin of this image were investigated by several methods. 4. The angular sensitivity curve of the receptors is 6 to 8°wide at the 50% sensitivity contour. 5. Optomotor experiments with stripes of differing widths show that the angular sensitivity of the receptors is fully utilized behaviourally, and that the eye functions in relatively dimlight. Adaptation changes are small. 6. A parallel beam falling on the eye reaches a single receptor via a circular patch of facets subtending about 30° at the centre of the eye. This was directly demonstrated by recording from a retinula cell and stimulating the eye by a moveable slit of parallel rays. This also demonstrates the wide acceptance angle of the exposed ends of the rhabdom columns. 7. When the eye is illuminated by a parallel beam, light is reflected back out of the eye. All the reflected light is contained in an angle of ±5° to the incident beam, although it enters and emerges via the large patch of facets mentioned above (6). Again, no effects of adaptation were observed. 8. The relation between the direction in which a ray enters the optical system of the cornea and cone and the direction it leaves was measured directly by a rotatable microscope of narrow aperture. 9. The mechanism by which the optical system forms the erect image on the receptor layer was demonstrated by tracing rays through scale drawings of the components. To do this the refractive index was measured in all components. The corneal surface acting as a lens forms the first image within the cone. The crystalline cone is non-homogeneous and acts as second lens in each ommatidium. 10. The skipper eye therefore illustrates Exner’s superposition principle, and it does so in daylight.

Angular sensitivity of the retinula cells of dark-adapted worker bee

SummaryElectrophysiological determination of the angular sensitivity of 16 worker bee retinula cells gives a value for horizontal acceptance angle of 2.5°±0.4° (S.D.) and for vertical acceptance angle of 2.7°±0.8° (S.D.).This value is in agreement with previous behavioural studies, but is clearly at variance with a recent analysis of the ommatidial dioptric by ray optics, which gives a value of 5° for the acceptance angle. It is suggested that this results from the failure of ray optics to take diffraction effects into account.

The honeybee (Apis mellifera) detects bilateral symmetry and discriminates its axis

Abstract Honeybees were trained and tested with a choice between a black and white pattern composed of two pairs of equal orthogonal bars with bilateral symmetry and the same or a similar pattern with a different symmetry. The targets subtended

The eye of Anoplognathus (Coleoptera, Scarabaeidae)

The night flying scarabaeid beetle Anoplognathus provides an example of a dark-adapted clear-zone compound eye in which rays from a distant point source, entering by a large patch of facets, are imperfectly focused upon the receptor layer. The optical system of the eye was investigated by six methods, all of which give similar results: (1) ray tracing through structures of known refractive index, (2) measurement of visual fields of single receptors, (3) measurement of the divergence of eyeshine, and (4) of the optomotor response to stripes of decreasing width, and (5) by direct observation of distribution of light within the eye. Finally (6) anatomically there is no single plane upon which an image could be focused. In each ommatidium, beneath the thick cornea, with its short corneal cone, lies a non-homogeneous crystalline cone (range of r. i. 1.442-1.365) that is significant in partially focusing rays across the wide clear zone (340 μm) in the dark-adapted eye. On the proximal side of the clear zone the rhabdoms form 7-lobed columns, isolated from each other over half their length by a tracheal tapetum. In the light-adapted eye the cone cells extend to form a crystalline tract (70-90 μm long) which is surrounded by dense pigment, and the optical path across the clear zone is completed by retinula cell columns that are of higher density than the surrounding cells. Pigment movement upon adaptation takes about 10 min to complete. Dark adaptation can be induced only at night on account of a strong diurnal rhythm. Eyeshine can be seen in the dark-adapted eye so long as the distal pigment leaves free the tips of the crystalline cones. Eyeshine falls to 50% at an angle of 12° from the direction of a parallel beam shining on the eye, as is consistent with a partial focus in which the distribution of light on the receptor layer is 18°-24° wide at the 50% contour. This distribution was confirmed by direct examination of the inside of the eye and by measurement of receptor fields as follows. The mean acceptance angle for 13 light-adapted units was 12.57° ± 1.97° s. d. and that of 10 dark-adapted ones 20.3° ± 3.36° s. d. The sensitivity to a point source on axis is increased at least 1000 fold by dark adaptation. Rays traced through a scale drawing of the eye, with refractive index measured for each component, show how the eye as a whole comes to be partially focused, and predicts an acceptance angle of 12° in the light-adapted and 20°-24° in the dark-adapted eye. In optomotor experiments dark-adapted Anoplognathus does not respond to stripes narrower than 18° repeat period, but light-adapted beetles respond down to 10°. The optomotor experiments also show a 1000 fold increase in sensitivity when dark-adapted at night. The eye has poor acuity that goes with wide visual fields of its receptors, and this is surprising when other excellently focused clear zone eyes are known. A possible compensation for the poor acuity is that the aperture of the eye can be larger, so that sensitivity although only to large objects, is that much increased.

Single electrode studies on the retina of the butterflyPapilio

Summary1.The butterfly retina exhibits strong interactions between photoreceptor responses recorded intracellularly. In general, the receptor which is locally giving the largest response suppresses the responses of neighbouring receptors that are less strongly stimulated. The effect enhances the differences between the primary photo-receptors and reduces responses to stimuli that excite all receptors together.2.The interaction is explained in terms of a high extracellular resistance, so that receptor currents pass through other receptors in the opposite direction to those of their own responses. The result is that receptors are actively turned off by colours away from their own peak wavelength.3.This effect applies most strongly to colour and to polarization plane when the stimulus is a point source on axis, and is therefore strong between the receptors of the same ommatidium.4.The result is that spectral sensitivity peaks and angular sensitivity peaks are narrower, and polarisation sensitivity is greater, than expected from single retinula cells in isolation. The sensitivities measured electrophysiologically cannot be easily related to the physical properties of the visual pigments. Polarisation sensitivity (PS) can reach 50.5.There are four types of primary photoreceptor, with peak near 380 nm, 450 nm, 550 nm and 610 nm. Cell marking usually reveals these as single retinula cells. Near the peak spectral sensitivity the responses are up to 60 mV positive-going, but away from the peak they can be negative-going.6.Anatomically the retina ofPapilio has four distal, four proximal retinula cells, and a ninth basal cell. Narrow pigment cells and tracheoles squeeze through the substantial basement membrane along with each bundle of nine axons.7.Two of the distal retinula cells contain red pigment grains near the rhabdom. The distal retinula cells are UV or blue sensitive. Green sensitive cells are proximal and can be coupled in opposite pairs. Red sensitive cells are proximal.8.The UV sensitive cell with peak near 380 nm is the most sensitive of the cell types when measured by the position of theV/logI curve on the intensity axis at the spectral peak of each type. The red-sensitive cells are also sensitive. By its inhibitory effect, interaction between receptors reduces the sensitivity measurement on this scale.9.Angular sensitivities measured with positive-going responses near the spectral peaks are narrow (Δρ-2°); when measured with negative-going responses they are wider (Δρ=3° to 5°).10.One type of unit has only negative-going responses to −60 mV, with Δp=2° to 5°, spectral peak near 550 nm and sometimes also 380 nm or 450 nm. This type has not been marked and is regarded as a restricted channel for return current. ItsV/logI curve extends over an intensity range of 106.11.The variety of the units suggests that their responses are not due to a simple regular network with all units connected indiscriminately to all others at all times through their terminals. There are selective channels for current flow and some retinula cells appear to be little influenced by others.12.Theory shows that when there is a direct electrical coupling between a pair of retinula cells (not passing through the extracellular space) it is possible to balance out the negative interactions caused by current flow through their terminals. Far from degenerating the signals, direct electrical coupling can cancel the negative interaction, and this may be its normal function.

A Diurnal Moth Superposition Eye with High Resolution Phalaenoides tristifica (Agaristidae)

This common Australian moth flies slowly and only in bright sunlight, but the compound eye has a sharply focused superposition image, to which 120-150 facets contribute. A distant point source is focused to form a blur circle on the retina. The diameter of this blur circle at 50% intensity, calculated from the width of the angular distribution of eyeshine, is 1.5-2.0° subtended at the centre of the eye, matching the interommatidial angle. The compromise between acuity and sensitivity, which is dependent on rhabdom spacing in relation to the blur circle diameter, has been struck with approximately 50% of the converging light from a distant point source falling on a single rhabdom. The F value of the focusing arrangement, defined as (focal length/aperture) is approximately 0.9. The structure of the eye, which undergoes negligible change on adaptation to light, is described by electron microscopy. The optical system is examined. The cornea and crystalline cone taken together constitute an afocal combination of lenses. Although the retinula cell columns act as light guides, a negligible contribution passes down them because rays are not focused upon their distal ends. The rhabdom columns are isolated from each other by complete sleeves of specialized tracheae backed by screening pigment. The e. r. g. is dominated by a single visual pigment resembling a rhodopsin with peak near 530 nm but adaptation studies suggest a small amount of a second pigment peaking near 360 nm. There are 14-16 retinula cells per ommatidium. An explanation for this great number, together with the use of a superposition image in daylight, cannot be offered until the visual behaviour is better understood. Apparently the eye is adapted for extreme sensitivity compatible with good resolution, and possibly this moth can see small contrast differences in small objects. For reasons that are discussed, a similar sharp focus is not to be expected in the eyes of moths that fly in dim light.

Fly Photoreceptors. I. Physical Separation of Two Visual Pigments in Calliphora Retinula Cells 1-6

The two peaks of the spectral sensitivity curves of Calliphora correspond to two visual pigments. The peak sensitivity to polarized light for the u. v. sensitive pigment is at an angle to that for the green-sensitive pigment. The change in angle of the maximum polarization sensitivity as a function of wavelength occurs near 400 nm; in this transition the curves do not follow a cos2 function. The angle between the two maxima is different for each retinula cell. The only explanation of this phenomenon is that there are two visual pigments in different parts of the receptor, and one part is twisted relative to the other. There are therefore two metarhodopsins and the adaptation mechanisms are partially separate for the two peaks of the spectral sensitivity. The inference of two separated pigments modifies the interpretation of much previous work on fly photoreceptors.

The optical function of changes in the medium surrounding the cockroach rhabdom

SummaryIn the dark-adapted eye of the cockroachPeriplaneta, the fused rhabdom is surrounded by a clear watery palisade; in the light-adapted eye this is replaced by pigment. The refractive indices of the rhabdom and its surround have been measured. The physiological effects of this change in structure has been analysed by the electromagnetic theory of light guides. The optical constants are theoretically consistent with the measured tenfold change in sensitivity and changes in acceptance angle of the retinula cells from 6.7 ° ¦(dark-adapted) to 2.4 ° (light-adapted).

Fly photoreceptors. II. Spectral and polarized light sensitivity in the drone fly Eristalis.

Eristalis tenax, the honeybee mimic, has photoreceptors mainly with double peaks as in typical flies, but the peaks are near 350 and 450 nm. Other cell types with peaks at 350 or 450 or 520 nm were encountered but not commonly. Measurements of the polarization sensitivity lead to the conclusion, as in Calliphora, that where there are two visual pigments they are separated in proximal and distal parts of the rhabdomere, with a twist between the two parts. Therefore there must also be two corresponding metarhodopsins. Receptors with a single spectral peak do not show this effect. Self-absorption can be excluded as an influence on spectral or polarization sensitivity. In its colour vision the drone fly is more like a typical fly than a bee but it has less green sensitive receptors and more blue sensitive ones than calliphora.