Visual resolution of the orientation cue by the honeybee (Apis mellifera)

Bees were trained to discriminate between a pattern with two or more black bars and a similar pattern with the bars at right angles. Earlier measures of the resolution of oblique black and white regular gratings of different periods were confirmed. The positions of the training bars were shifted every 5 min to prevent the bees from using their locations as cues. To measure the length of the detectors of edge orientation, the trained bees were tested with targets filled with parallel short black/white edges of various lengths. The minimum individual length of edge required to discriminate the orientation cue was found to be near 3 degrees, and similar for vertical, horizontal and oblique edges. This is the first time that this kind of resolution has been measured in an invertebrate. The bees learn and recognize the edge orientation, not the lay-out of the pattern.     

Vision of the honeybee Apis mellifera for patterns with one pair of equal orthogonal bars

The visual discrimination of patterns of two equal orthogonal black bars by honeybees has been studied in a Y-choice apparatus with the patterns presented vertically at a fixed range. Previous work shows that bees can discriminate the locations of one, or possibly more, contrasts in targets that are in the same position throughout the training. Therefore, in critical experiments, the locations of areas of black were regularly shuffled to make them useless as cues. The bees discriminate consistent radial and tangential cues irrespective of their location on the target during learning and testing. Orientation cues, to be discriminated, must be presented on corresponding sides of the two targets. When orientation, radial and tangential cues are omitted or made useless by alternating them, discrimination is impossible, although the patterns may look quite different to us. The shape or the layout of local cues is not re-assembled from the locations of the bars, even when there are only two bars in the pattern, as if the bees cannot locate the individual bars within the large spatial fields of their global filters.     

Spatial coincidence of cues in visual learning by the honeybee (Apis mellifera)

The discrimination of patterns was studied in a Y-choice chamber fitted with a transparent baffle in each arm, through which the bees had a choice of two targets via openings 5cm wide. The bees see the positive (rewarded) and the negative (unrewarded) targets from a fixed distance. The patterns were bars (subtending 22 degrees x5.4 degrees at the point of choice) presented in one-quarter of each target. The bars were moved to a different quarter of the target every 5min, to make the location of black useless as a cue. A coincident presentation is when the bar on the left target is on the same side of the target as the bar on the right target. The bees learn the orientation cue when the presentation is coincident but otherwise cannot learn it. This experiment shows that bees do not centre their attention on the individual bars, otherwise they would always discriminate the orientation. Centring the target as a whole precedes learning. Having learned with the bar on one side of the targets, bees do not recognize the same cue presented on the other side. A separate orientation cue can be learned on each side. A radial/tangential cue is preferred to a conflicting orientation cue.     

What the honeybee sees: a review of the recognition system of Apis mellifera

Abstract. For many years, two opposing theories have dominated our ideas of what honeybees see. The earliest proposal based on training experiments was that bees detected only simple attributes or features, irrespective of the actual pattern. The features demonstrated experimentally before 1940 were the disruption of the pattern (related to spatial frequency), the area of black or colour, the length of edge, and the angle of orientation of a bar or grating. Cues discovered recently are the range, and radial and tangential edges, and symmetry, relative to the fixation point, which is usually the reward hole. This theory could not explain why recognition failed when the pattern was moved. In the second theory, proposed in 1969, the bee detected the retinotopic directions of black or coloured areas, and estimated the areas of overlap and nonoverlap on each test pattern with the corresponding positions in the training pattern. This proposal explained the progressive loss of recognition as a test pattern was moved or reduced in size, but required that the bees saw and remembered the layout of every learned pattern and calculated the mismatch with each test image. Even so, the same measure of the mismatch was given by many test patterns and could not detect a pattern uniquely. Moreover, this theory could not explain the abundant evidence of simple feature detectors. Recent work has shown that bees learn one or more of a limited number of simple cues. A newly discovered cue is the position, mainly in the vertical direction, of the common centre (centroid) of black areas combined together. Significantly, however, the trained bees look for the cues mentioned above only in the range of places where they had occurred during the training. These two observations made possible a synthesis of both theories. There is no experimental evidence that the bees detect or re-assemble the layout of patterns in space; instead, they look for a cue in the expected place. With an array of detectors of the known cues, together with their directions, this mechanism would enable bees to recognize each familiar place from the coincidences of cues in different directions around the head.     

Generalization in visual recognition by the honeybee (Apis mellifera) : A review and explanation

During a century of studies on honeybee vision, generalization was the word for the acceptance of an unfamiliar pattern in the place of the training pattern, or the ability to learn a common factor in a group of related patterns. The ideas that bees generalize one pattern for another, detect similarity and differences, or form categories, were derived from the use of the same terms in the human cognitive sciences. Recent work now reveals a mechanistic explanation for bees. Small groups of ommatidia converge upon feature detectors that respond selectively to certain parameters that are in the pattern: modulation in the receptors, edge orientations, or to areas of black or colour. Within each local region of the eye the responses of each type of feature detector are summed to form a cue. The cues are therefore not in the pattern, but are local totals in the bee. Each cue has a quality, a quantity and a position on the eye, like a neuron response. This summation of edge detector responses destroys the local pattern based on edge orientation but preserves a coarse, sparse and simplified version of the panorama. In order of preference, the cues are: local receptor modulation, positions of well-separated black areas, a small black spot, colour and positions of the centres of each cue, radial edges, the averaged edge orientation and tangential edges. A pattern is always accepted by a trained bee that detects the expected cues in the expected places and no unexpected cues. The actual patterns are irrelevant. Therefore we have an explanation of generalization that is based on experimental testing of trained bees, not by analogy with other animals.Historically, generalization appeared when the training patterns were regularly interchanged to make the bees examine them. This strategy forced the bees to ignore parameters outside the training pattern, so that learning was restricted to one local eye region. This in turn limited the memory to one cue of each type, so that recognition was ambiguous because the cues were insufficient to distinguish all patterns. On the other hand, bees trained on very large targets, or by landing on the pattern, learned cues in several eye regions, and were able to recognize the coarse configural layout.     

The visual system of the honeybee (Apis mellifera): the maximum length of the orientation detector

Bees were trained to discriminate between two or more black bars and similar bars at right angles, presented on a vertical surface. The positions of the bars were shifted every 5 min to prevent their locations being used as cues. The experiments exploit the fact that bees do not discriminate the global orientation of a straight line of small black squares that are individually resolved, because the local responses to equal lengths of edges at right angles cancel out, and each square has no residual orientation cue. The experiments measure the resolution of this effect by control of the width of the gaps between the squares. At the limit the unit orientation detectors cannot span the gaps. Training with vertical or with horizontal bars in separate experiments, and testing with vertical or horizontal lines of squares, shows that the vertical gaps in horizontal rows are detected with better resolution than horizontal gaps in vertical rows. The results show that unit orientation detectors span not more than 3 ommatidia.     

Pattern vision of the honeybee (Apis mellifera). What is an oriented edge?

Pairs of black patterns on a white background, one rewarded the other not, were presented vertically each in one arm of a Y-maze. During training the locations of the black areas were changed every 5 min to prevent the bees using them as cues, but cues from edges were kept consistent. Bees detect orientation even in a gradient that subtends 36° from black to white (normal to the edge). Orientation cues in short lengths of edge are detected and summed on each side of the fixation point, irrespective of the lay-out of the pattern. Edges at right angles reduce the total orientation cue. The polarity of edges in a sawtooth grating is weakly discriminated, but not the orientation of a fault line where two gratings meet. Edge quality can be discriminated, but is not recognised in unfamiliar orientations. When spot location is excluded as a cue, the orientation of a row of spots or squares which individually provide no net orientation cue is not discriminated. In conclusion, when locations of black areas are shuffled, the bees remember the sum of local orientation cues but not the global pattern, and there is no re-assembly of a pattern based on differently oriented edges. A neuronal model consistent with these results is presented. Accepted: 5 March 2000     

Visual discrimination of radial cues by the honeybee (Apis mellifera)

This is a systematic study of the discrimination of black radially symmetrical patterns presented on a white vertical background and subtending 45 degrees or 50 degrees at the point of choice in a Y-maze apparatus. Before discrimination can occur, the ability to fixate is promoted by any radial pattern irrespective of the number of symmetry axes. A ring of spots can also stabilize the eye before the positions of the spots are discriminated.Cues for discrimination are of two main types. First, with fixed patterns of sectors or spots, the cue is the location of an area of black relative to the fixation point, and the particular number of axes is less important than the size of the individual areas. Secondly, evidence is presented for a family of filters with large fields and coarse tuning that detect patterns of radially symmetrical edges. These filters become more evident when the patterns are made of thin black radial bars or when they are rotated at random during the training. An angular shift of one radial pattern relative to the other, or a difference between numbers of bars, is best discriminated when one of the patterns but not the other has angles of 30 degrees, 60 degrees, or 120 degrees between radial edges, and least when the angles are 90 degrees. Baffles in the apparatus make the bees pause and fixate so that discrimination is improved. When targets are rotated during the learning process, radial cues for discriminations must be presented as edges, not as spots or areas. Besides detecting and fixating flowers, this system could be useful to estimate the perfection of their symmetry.     

Some labels that are recognized on landmarks by the honeybee (Apis mellifera)

Freely flying bees were trained in a situation that resembled the natural task of a bee arriving at a foraging site that was located by a landmark. The bees' task was to locate the reward in the arm of the Y-choice apparatus, where a black pattern on a white background was displayed in one arm versus a white target in the other arm, at a range of 27 cm. The alternative patterns for the training included previously identified cues. They were: an oblique bar, three parallel oblique bars, an oblique grating, a square cross, six spokes, a large or a small spot, a spotty modulation, or a ring. The trained bees were given a variety of interleaved tests to discover the labels they had used to identify the patterns. A label is defined as the coincidence of cues that contributed to the recognition of a single landmark. The bees learned, firstly, the black area at the expected place, secondly, modulation caused by edges at the expected place. These cues were quantified and always available. In addition, the orientation cue was learned from a grating that covered the target, but was ignored in a single bar. The bees learned the positions of the centres of black and of radial symmetry. In tests, they also recognized unfamiliar cues that were not displayed in the training. The cues and preferences were similar to those used to discriminate between two targets. The new experiments validate some old conclusions that have been controversial for 40 years.     

Visual discriminations of spokes, sectors, and circles by the honeybee (Apis mellifera)

A new cue for visual discrimination by the honeybee has been demonstrated. Bees detected the position of the centre of symmetry of radial patterns of spokes, sectors, and circles relative to their point of choice in the learning process, irrespective of the pattern. When trained with one of these patterns versus a blank target, the bees discriminated a shift in the position of the centre of symmetry by as little as 5 degrees , in some cases with unfamiliar test patterns. A pattern of spokes or rings also stabilized the vision of the bees in the horizontal plane so that the position of a plain black area could then be discriminated. In other experiments, bees discriminated half of a pattern of radial spokes or concentric circles from the other half, cut either vertically or horizontally, and irrespective of scale. Therefore these patterns were not detected by preformed combinations of orientation detectors or global templates with a single output. Instead, the crucial cue for detecting edges as radial or circular was the coincidence of responses of numerous local edge detectors having the appropriate convergence to a hub. Edges that converged towards a hub were detected by the bees as radial, and edges at right angles to these were parts of circles, irrespective of the actual pattern. Breaking the patterns of spokes or circles into rows of squares spoiled the discrimination if the squares were separately resolved. Alternatively, breaking the pattern into short bars that were separately resolved spoiled the discrimination when the bars subtended less than 3 degrees . The local feature detectors for spokes and circles therefore resembled those of the orientation detectors in being short, independent, and unable to span gaps of more than 3 degrees . In conclusion, radial and circular patterns were identified by the regional coincidences and convergence of local detectors of edge orientation, and the positions of the centres of symmetry were remembered as landmarks that helped locate the reward, but the patterns themselves were not remembered.     

Pattern recognition in honeybees: eidetic imagery and orientation discrimination

The roles of eidetic imagery and orientational cues, respectively, in the discrimination of visual patterns by honeybees (Apis mellifera) were evaluated by training the bees to discriminate between patterns consisting of periodic, black and white square wave gratings. Training and tests with a number of different pairs of patterns revealed that bees use orientational cues almost exclusively, if such are present, and make use of eidetic images only when orientational cues are not available. On the other hand, if a pattern carries strong orientational cues, bees learn the orientation even if it is irrelevant to the discrimination task on which they are trained.     

The preferences of the honeybee (Apis mellifera) for different visual cues during the learning process

By working with very simple images, a number of different visual cues used by the honeybee have been described over the past decades. In most of the work, the bees had no control over the choice of the images, and it was not clear whether they learned the rewarded pattern or the difference between two images. Preferences were known to exist when untrained bees selected one pattern from a variety of them, but because the preferences of the bees were ignored, it was not possible to understand how natural images displaying several cues were detected. The preferences were also essential to make a computer model of the visual system. Therefore experiments were devised to show the order of preference for the known cues in the training situation. Freely flying bees were trained to discriminate between a rewarded target with one pattern on the left side and a different one on the right, versus a white or neutral target. This arrangement gave the bees a choice of what to learn. Tests showed that in some cases they learned two or three cues simultaneously; in other cases the bees learned one, or they preferred to avoid the unrewarded target. By testing with different combinations of patterns, it was possible to put the cues into an order of preference. Of the known cues, loosely or tightly attached to eye coordinates, a black or blue spot was the most preferred, followed by strong modulation caused by edges, the orientation of parallel bars, six equally spaced spokes, a clean white target, and then a square cross and a ring. A patch of blue colour was preferred to yellow.     

Pattern discrimination by the honeybee: disruption as a cue

The discrimination of pattern disruption in freely flying honeybees (Apis mellifera) was examined. Bees were trained to discriminate at a fixed distance between a regularly repeated black/white pattern and the same pattern at a different magnification in targets of the same angular size. The locations of areas of black were regularly shuffled to make them useless as cues. The results of the experiments indicate that the bees discriminate the disruption of the pattern as a whole, irrespective of the actual pattern. Bees trained to prefer a larger period transfer to an even larger period, when given a forced choice with a pair of patterns of differing disruption from those they were trained on, as if their spontaneous preference has not been overcome. Bees trained to prefer a smaller period, however, prefer the former negative pattern rather than transfer to an even smaller period. These results show that the bees do not rely solely on learning the absolute period of a pattern nor the relative disruption of two patterns, and they are confused when these two cues conflict in tests with unfamiliar targets. Bees can discriminate between fields of view that differ in average disruption as a generalized cue, irrespective of pattern. Accepted: 7 April 1997     

Two-dimensional pattern discrimination by the honeybee

For a reward of sugar, bees will learn to prefer a pattern rather than an alternative similar one. This visual discrimination allows us to measure resolution, and to search for the cues that the bees remember and later use to recognize the rewarded pattern. Two systems in parallel, analogous to low pass and high pass filters, are distinguished. The first system discriminates the location and size of at least one area of contrast on each side of the target, with inputs from blue and green receptors, but the ability to discriminate the location of colour depends upon fixation. The bees remember less than a low resolution copy of the image, even when they fixate on a vertical pattern. The second system amplifies the contrast at edges in the pattern, ignoring the direction of contrast, and controls fixation upon the target. Edges are discriminated according to their orientation and radial or tangential arrangement. An axis of bilateral symmetry is detected. However, the relative locations of cues within the image are lost, apparently because the relevant neurones have very large fields. Only the cues, not the whole patterns, are preserved in memory. This system is colour blind because its input is restricted to the receptors with peak sensitivity in the green. The two systems together discriminate many simple patterns, but not all, because the filters are limited in variety.     

Recognition of a familiar place by the honeybee (<Emphasis Type="Italic">Apis mellifera</Emphasis>)

Recent work shows that at any one place bees detect a limited variety of simple cues in parallel. At each choice point, they recognize a few cues in the range of positions where the cues occurred during the learning process. There is no need to postulate that they re-assemble the surrounding panorama in memory; only that they retain memories of the coincidences of cues in the expected retinotopic directions. The cues could be stimuli that excite groups of peripheral visual neurons. All the experimentally known cues are described, including modulation of the receptors, the locations of areas of black or colour, the nearness, size, averaged edge orientation, and radial and tangential edges. Cues of each type are separately summed within large fields, the size of which varies with the cue. Local orientation cues from edges at right angles cancel each other within each field, which also suggests that the discrimination of shape and texture is limited. Resolution depends on lateral interactions and the number of ommatidia required for each cue. To identify a new place, a few sparse cues, together with their directions, are learned in orientation flights. When the bee returns, the cues in the panorama are progressively matched as they coincide with the cues in memory. The limited number of cues, though economical for memory, may restrict the foraging behaviour and lead to flower constancy. This kind of a visual system is a candidate model for other animals or machines with economical processing systems.     

Pattern discrimination by the honeybee (Apis mellifera): training on two pairs of patterns alternately

Pattern discrimination in the honeybee was studied by training alternately with two different pairs of patterns. Individually marked bees made a forced choice from a fixed distance in a standard Y-choice maze for a reward of sugar solution. Bees were trained, first on one pair of patterns for 10min then on a second pair, and so on, alternately between the two pairs. The pairs of patterns were selected to test the hypothesis that bees have a limited number of parallel mechanisms for the detection and discrimination of certain generalized global features. If this is so, it might be expected that each channel could process one pair of patterns simultaneously, but two pairs of patterns that are processed by the same channel would interfere with each other during the learning process. Features tested were: average orientation of edges, radial and tangential edges based on a symmetry of three or six, the position of a black spot, and the exchange of black and white. The bees fail to learn when the two alternated pairs of patterns offer the same feature, and they discriminate when the pairs offer two different features.     

Visual discrimination by the honeybee (Apis mellifera): the position of the common centre as the cue

Abstract. Bees can be trained to discriminate between a target with a 20° spot above a 10° spot of the same colour, and another target with the spots exchanged in position. Tests show that they do not remember the separate positions of spots of the same colour (including black) on the same target. The bees discriminate the difference in positions, in the vertical direction, of the common centres of the spots taken together, with or without green contrast.
Similar results are obtained in discriminations of a fixed T shape, each composed of two broad black bars subtending 8 by 24°, vs the same shape inverted. The trained bees fail to discriminate between the T shapes when the centroids are at the same level in the vertical direction. Moving the shapes in the horizontal direction in tests has less effect. Quite different results are obtained when the two bars of the T shape differ in colour. The bees discriminate the positions of the two colours separately, but they still fail to discriminate the shape of the T. The results can be explained by filters that detect the intensities within their fields, irrespective of shape, and weigh them according to their vertical angles from the horizontal midline. The normal function of these filters could be to detect the levels of objects relative to the horizon when the bee is in flight.     

How Bees Discriminate a Pattern of Two Colours from Its Mirror Image

A century ago, in his study of colour vision in the honeybee (Apis mellifera), Karl von Frisch showed that bees distinguish between a disc that is half yellow, half blue, and a mirror image of the same. Although his inference of colour vision in this example has been accepted, some discrepancies have prompted a new investigation of the detection of polarity in coloured patterns. In new experiments, bees restricted to their blue and green receptors by exclusion of ultraviolet could learn patterns of this type if they displayed a difference in green contrast between the two colours. Patterns with no green contrast required an additional vertical black line as a landmark. Tests of the trained bees revealed that they had learned two inputs; a measure and the retinotopic position of blue with large field tonic detectors, and the measure and position of a vertical edge or line with small-field phasic green detectors. The angle between these two was measured. This simple combination was detected wherever it occurred in many patterns, fitting the definition of an algorithm, which is defined as a method of processing data. As long as they excited blue receptors, colours could be any colour to human eyes, even white. The blue area cue could be separated from the green receptor modulation by as much as 50°. When some blue content was not available, the bees learned two measures of the modulation of the green receptors at widely separated vertical edges, and the angle between them. There was no evidence that the bees reconstructed the lay-out of the pattern or detected a tonic input to the green receptors.     

Tactile learning in the honeybee

Free-flying bees were conditioned on a vertical wall to a vertical tactile pattern consisting of parallel lines of grooves and elevations. The asymptote of the learning curve is reached after approximately 25 rewards. Bees can discriminate the conditioned vertical pattern from a horizontal or diagonal alternative. Angle discrimination is apparent only for relatively coarse tactile cues. The proboscis extension response of fixed bees was used to condition bees to a vertical tactile pattern which was presented to the antennae. The learning curve reaches an asymptote after 4 rewards. After 7 unrewarded extinction trials the conditioned responses are reduced to 50%. Bees show best discrimination for patterns whose edges they can scan with their antennae. The animals show a high degree of generalization by responding to an object irrespective of the trained pattern. Under laboratory conditions fixed bees can discriminate the angles and spatial wavelengths of fine tactile patterns consisting of parallel grooves. Bees can also discriminate forms and sizes of tactile patterns. They do not discriminate between different types of edges and between positive and negative forms. Accepted: 17 September 1998     

The anti-intuitive visual system of the honey bee

Because bees fly around, visit flowers and chase mates, we conclude intuitively that they see things as we do. But their vision is unexpectedly different, so we say it is anti-intuitive. Detailed tests have demonstrated separate detectors for modulation of blue and green receptors, edge orientation (green only), and areas of black. The edge detectors are about 3° across, independent, and not re-assembled to make lines, shapes or textures. Instead, the detectors of each type are summed quantitatively to form cues in each local region with an order of preference for learning the cues. Trained bees remember the positions of the total modulation (preferred), the average edge orientation, areas of black or colour, and positions of hubs of radial and circular edges in each local region, but not the original responses, so the pattern is lost. When presented with a yellow spot on a blue background with no UV reflected, the preferred cue is not the colour, but a measure of the modulation detected by the green and separately by the blue receptors.