Pattern discrimination by the honeybee (Apis mellifera ) is colour blind for radial / tangential cues

Bees were trained to discriminate between two patterns, one of which was associated with a reward, in a Y-choice apparatus with the targets presented vertically at a distance at an angular subtense of 50°. Previous work with this apparatus has found discrimination between two patterns of coloured gratings or radial sectors that are fixed in different orientations during the training. When there was contrast to the blue receptors alone, gratings of period 6° were resolved, and 4° when there was contrast to the green receptors. In the present work, bees discriminate between a pattern containing tangentially arranged edges and one containing radially arranged edges, both with no average edge orientation. The targets were rotated every 5 min to make the locations of areas useless as cues. The edges remained consistently radial or tangential and were therefore the only cues. Tests with patterns of selected colours and various levels of grey show that for each colour there is a level of grey at which discrimination fails. Discrimination is therefore colour-blind. The same patterns were made with combinations of coloured papers that give no contrast to the green receptors or alternatively to the blue receptors. The bees discriminate only if the edges between colours present a contrast to the green receptors. The system that discriminates generalized radial and tangential cues is therefore colour blind because the inputs are restricted to the green receptors, not because receptor outputs are added together. The same result was obtained with a very coarse pattern of period 20°. Accepted: 10 January 1999     

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     

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.     

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.     

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.     

The effect of complexity on the discrimination of oriented bars by the honeybee (<Emphasis Type="Italic">Apis mellifera</Emphasis>)

Visual discrimination of black bars by honeybees was studied in a Y-choice apparatus with fixed vertical patterns at constant range. The problem is to discover how bees remember different degrees of complexity of the orientation cue. Previous conclusions with parallel gratings and single bars disagree. With broad bars versus orthogonal bars, the bees learn the orientation cue if the bars are centred at the same place, but they learn the position cue in the vertical direction when the bars are at different places on the two targets. With several bars on each target, the bees learn their orientation and positions. As fixed patterns increase in complexity, the bees follow a simple rule, to look only at the range of places where the cues were displayed. The frame of reference is disrupted when a black spot is added to the training pattern. There is abundant evidence that the bees do not re-assemble the pattern or learn shapes. The filters that detect the position and orientation cues are coarsely tuned, so that they respond in a graded way, but the memory of the range of directions of the cue, as seen from the point of choice, is more exact.     

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.     

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.     

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.     

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.     

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.     

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.     

Bee vision of pattern and 3D. The Bidder Lecture 1994

Insect vision is nothing if not active. The regular head movements, called saccades, enable the fly Drosophila to keep a straight path in flight despite inequalities in the thrust of the wings. Using their own motion, bees in flight measure the ranges of nearby objects. A long history of research shows that bees discriminate visually in ways that depend on their activity or task, so we must distinguish between vision during flying, fixating or hovering and landing. Bees return again and again for a reward of sugar solution and use their eyes to find their way. In an apparatus that makes them discriminate between two simulataneously visible but regularly interchanged targets, seen at a distance of 27 cm, bees are able to distinguish a remarkable number of simple patterns, but they fail in certain critical cases. The results can be explained with the hypothesis that bees have several broadly tuned overlapping filters with large fields that respond to the predominant orientation in a region of the image, and others for radial and circular patterns. Together with colour, these filters are independent of range. Bees prefer to use landmarks where they can, then global pattern at the largest scale, and lastly the detail around the goal. The way that discrimination of one visual feature is independent of other variables can be explained by models analogous to the colour triangle in colour discrimination.     

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.     

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     

Pattern discrimination in a hawkmoth: innate preferences,learning performance and ecology

Spatial patterns are important cues for flower detection and recognition by nectar-feeding insects. Pattern vision has been studied in much detail in bees and flies but rarely in butterflies and moths. In this paper, I present a first proof of pattern-learning abilities in a moth, and discuss reasons for the limitations to their pattern learning. The diurnal hawkmoth Macroglossum stellatarum spontaneously prefers patterned to uniformly coloured stimuli but can be trained to choose the uniform stimulus. By contrast, experience does not override the innate preferences for radial over tangential patterns, and for tangential over striped patterns. These results do not reflect bad visual discrimination but rather a lack of learning ability and motivation to abolish innate preferences. I propose that radial and tangential flower patterns are good predictors of nectar reward, a condition under which learning is unlikely to evolve. These patterns serve not only as cues for flower detection but also as guides to the reward. Hovering pollinators strongly depend on these guides and should therefore: (i). have rigid pattern preferences; and (ii). not be motivated to abolish these preferences as easily as their innate preferences for colours.     

Discrimination of coloured patterns by honeybees through chromatic and achromatic cues

We investigated pattern discrimination by worker honeybees, Apis mellifera, focusing on the roles of spectral cues and the angular size of patterns. Free-flying bees were trained to discriminate concentric patterns in a Y-maze. The rewarded pattern could be composed of either a cyan and a yellow colour, which presented both different chromatic and achromatic L-receptor contrast, or an orange and a blue colour, which presented different chromatic cues, but the same L-receptor contrast. The non-rewarded alternative was either a single-coloured disc with the colour of the central disc or the surrounding ring of the pattern, a checkerboard pattern with non-resolvable squares, the reversed pattern, or the elements of the training pattern (disc or ring alone). Bees resolved and learned both colour elements in the rewarded patterns and their spatial properties. When the patterns subtended large visual angles, this discrimination used chromatic cues only. Patterns with yellow or orange central discs were generalised toward the yellow and orange colours, respectively. When the patterns subtended a visual angle close to the detection limit and L-receptor contrast was mediating discrimination, pattern perception was reduced: bees perceived only the pattern element with higher contrast.     

Pattern vision of the honeybee (Apis mellifera): the effect of pattern on the discrimination of location

This paper investigates how the pattern influences the discrimination of different locations of two or more areas of black, white or colour. The coloured patterns were made from two calibrated coloured papers that give contrast only to green receptors, or alternatively only to blue receptors. The patterns are fixed during training. It is found that the discrimination of translocation of two areas of colour involves green receptors and also blue receptors, and the resolution depends strongly on the pattern. Patterns that offer horizontal strips and up-down differences in locations are well resolved, even with no green contrast. Resolution of left-right reversal is greatly improved when the patterns promote fixation in the horizontal plane, as if green contrast is essential to stabilize the eye in yaw. The addition of radial bars with green contrast, a central black spot or a black surround, is particularly effective. The additions promote fixation, and would aid the detection of natural symmetrical objects. Accepted: 30 May 1999     

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 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.