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Ventral detection of coloured targets depends on achromatic receptor-speci®c contrasts. The bees' performance (percentage of correct choices) is represented as a function of the visual angle subtended by the colour target to the bee's eye. Each curve was obtained using an independent group of bees. Points on a curve represent the mean performance of the bees tested with that particular stimulus. Vertical bars represent SE of the mean. Horizontal bars represent the angular error de®ned for each visual angle (see Materials and methods). The hatched line at 60% corresponds to the minimum visual angle (a min ) at which the bees still detect the target. This angle can be read on the abscissa from the arrows. Absence of S-receptor contrast does not aect performance (a min = 5.9 0.5°), whereas absence of M-and L-receptor contrast signi®cantly impairs the detection task (a min = 10.3 0.9° and 17.6 3°, respectively). Diamonds: stimulus presenting all chromatic and achromatic contrasts (HKS-3N) (n = 16 bees); triangles: stimulus devoid of S-receptor contrast (HKS-8N) (n = 8 bees); squares: stimulus devoid of M-receptor contrast (HKS-41N) (n = 7 bees); circles: stimulus devoid of L-receptor contrast (HKS-82N) (n = 12 bees)
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Honeybees Apis mellifera detect coloured targets presented to the frontal region of their compound eyes using their colour vision system at larger
visual angles (α > 15°), and an achromatic visual system based on the long-wave photoreceptor type at smaller visual angles
(5° < α < 15°). Here we examine the capability of the dorsal, ventral and front...
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Context 1
... minimum visual angle for the ventral detection of a coloured stimulus varied depending on the presence or absence of speci®c-receptor contrasts (Fig. 6). Suppres- sion of S-receptor contrast (HKS 8N) did not aect the detection task: a min was 5.9 0.5°, and comparable with that obtained with the stimulus that provided all receptor-speci®c contrasts (HKS 3N: 7.1 0.5°; see above). On the other hand, suppression of M-or L- receptor contrast did aect the detection task: a min was 10.3 ...
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Colour vision was first demonstrated with behavioural experiments in honeybees 100 years ago. Since that time a wealth of quality physiological data has shown a highly conserved set of trichromatic colour receptors in most bee species. Despite the subsequent wealth of behavioural research on honeybees and bumblebees, there currently is a relative d...
Background:
Recent studies on colour discrimination suggest that experience is an important factor in how a visual system processes spectral signals. In insects it has been shown that differential conditioning is important for processing fine colour discriminations. However, the visual system of many insects, including the honeybee, has a complex...
Citations
... The bee's eye can recognize most colors as human eye does, and have adapted well to see blue, green, and ultra-violet (UV) light. This allows them to see colors and ultraviolet nectar guides on flowers which guide bees to the nectar [17,18]. The Morpho butterfly, whose eyes are sensitive to the UV, visible, and near-infrared (NIR) spectra, has better vision [19]. ...
Natural compound eyes have excellent optical characteristics, namely large field of view, small size, no aberration, and sensitive to motion. Some arthropods have more powerful vision. For example, the Morpho butterfly’s compound eyes can perceive the near-infrared and ultraviolet light that the human eye cannot see. This wide-band imaging with a large field of view has great potential in wide-area surveillance, all-weather panoramic imaging, and medical imaging. Hence, a wide-band spherical compound eye camera inspired by the Morpho butterfly’s eye was proposed. The wide-band spherical compound eye camera which can achieve a large field of view (360° × 171°) imaging over a wide range of wavelengths from 400nm to 1000nm, mainly consists of three parts: a wide-band spherical compound eye with 234 sub-eyes for light collection, a wide-band optical relay system for light transmission, and a wide-band CMOS image sensor for photoelectric conversion. Our experimental results show that the wide-band spherical compound eye camera not only captures a large field of view without anomalous blurring or aberrations but also perceives near-infrared light that is not recognized by the human eye. These features make it possible for distortion-free panoramic vision and panoramic medical diagnosis.
... Colour and pattern perception in bees has been widely investigated, and it has been often assumed, implicitly and sometimes explicitly, that bees will adopt movement patterns that optimally support solving the perceptual learning tasks, e.g., approach a target in the most convenient way to view all available visual features (e.g., Wehner, 1972;Menzel and Lieke, 1983;Lehrer, 1998;Giurfa et al., 1999a;Hempel de Ibarra et al., 2002;Thivierge et al., 2002;Zhang et al., 2004;Dyer et al., 2005;Wu et al., 2013;Avarguès-Weber et al., 2020). However, the viewing conditions of individual bees will be wholly dependent upon their flight behaviour during approach and landing on the stimulus (Hertz, 1935;Wehner and Flatt, 1977;Giurfa et al., 1999b). Previous evidence suggests that bees might generally prefer to approach vertically presented stimuli from below (Anderson, 1977;Giger, 1996), which could significantly affect perception and learning processes. ...
... A transparent pipette nib (4 mm diameter) inserted in the centre of the stimulus was backfilled with 50% sucrose solution. The nib was a short protrusion and inconspicuous, as we know from our previous studies investigating the spatial resolution of bee vision with different colours and coloured patterns, and showing that bees easily learn the colours of large patterns from a distance (e.g., Giurfa et al., 1996;Giurfa et al., 1999b;Hempel de Ibarra et al., 2001;Wertlen et al., 2008). The nib was filled with sucrose solution during training trials, and empty during test trials. ...
Gaze direction is closely coupled with body movement in insects and other animals. If movement patterns interfere with the acquisition of visual information, insects can actively adjust them to seek relevant cues. Alternatively, where multiple visual cues are available, an insect’s movements may influence how it perceives a scene. We show that the way a foraging bumblebee approaches a floral pattern could determine what it learns about the pattern. When trained to vertical bicoloured patterns, bumblebees consistently approached from below centre in order to land in the centre of the target where the reward was located. In subsequent tests, the bees preferred the colour of the lower half of the pattern that they predominantly faced during the approach and landing sequence. A predicted change of learning outcomes occurred when the contrast line was moved up or down off-centre: learned preferences again reflected relative frontal exposure to each colour during the approach, independent of the overall ratio of colours. This mechanism may underpin learning strategies in both simple and complex visual discriminations, highlighting that morphology and action patterns determines how animals solve sensory learning tasks. The deterministic effect of movement on visual learning may have substantially influenced the evolution of floral signals, particularly where plants depend on fine-scaled movements of pollinators on flowers.
... However, the viewing conditions of individual bees will be wholly dependent upon their flight behaviour during approach and landing on the stimulus ( Giurfa et al., 1999b;Hertz, 1935;Wehner and Flatt, 1977). Previous evidence suggests that bees might generally prefer to approach vertically-presented stimuli from below (Anderson, 1977;Giger, 1996), which could significantly affect perception and learning processes. ...
Gaze direction is closely coupled with body movement in insects and other animals. If movement patterns interfere with the acquisition of visual information, insects can actively adjust them to seek relevant cues. Alternatively, where multiple visual cues are available, an insects movements may influence how it perceives a scene. We show that the way a foraging bumblebee approaches a floral pattern could determine what it learns about the pattern. When trained to vertical bicoloured patterns, bumblebees consistently approached from below centre in order to land in the centre of the target where the reward was located. In subsequent tests, the bees preferred the colour of the lower half of the pattern that they predominantly faced during the approach and landing sequence. A predicted change of learning outcomes occurred when the contrast line was moved up or down off-centre: learned preferences again reflected relative frontal exposure to each colour during the approach, independent of the overall ratio of colours. This mechanism may underpin learning strategies in both simple and complex visual discriminations, highlighting that morphology and action patterns determines how animals solve sensory learning tasks. The deterministic effect of movement on visual learning may have substantially influenced the evolution of floral signals, particularly where plants depend on fine-scaled movements of pollinators on flowers.
... Besides, it can recognize objects with a high speed. These features enable the SCECam to have a great potential for a broad range of applications including surveillance imaging, fast target detection and recognition [18][19][20], collision-free navigation of terrestrial and aerospace vehicles [21][22][23][24] and so on. ...
In recent years, the compound eye imaging system has attracted great attention due to its fascinating optical features such as large field of view (FOV), small volume and high acuity to moving objects. However, it is still a big challenge to fabricate such a whole system due to the mismatch between the spherical compound eye imaging element and the planar imaging sensor. In this work, we demonstrate a kind of hemispherical compound eye camera (SCECam) which analogs the eye of the fruit fly. The SCECam consists of three sub-systems, a hemispherical compound eye, an optical relay system and a commercial CMOS imaging sensor. By introducing an intermediate optical relay system, the curved focal plane after the compound eye can be transformed and projected onto the planar focal plane of the imaging sensor. In this way, the SCECam can realize a large FOV (up to 122.4°) with 4400 ommatidia, which makes it possible to detect and locate fast moving objects at a very fast speed. It is calculated that the recognition speed of the SCECam is two to three orders of magnitude higher than those conventional methods such as the Canny and Log edge-detection methods.
... Our conclusions are in line with experimental results showing the importance of the long-wavelength channel in target detection at the limit of the honeybee's eye's resolution (Giurfa et al. 1996;Dyer et al. 2008) and in edge detection (Giger and Srinivasan 1996). Interestingly, medium-wavelength-sensitive receptors yield high signal-to-noise ratios as well, but only for petals (Fig. 3), which might be linked to the supplementary role of medium-wavelength receptors in ventral target detection in honeybees (Giurfa et al. 1999). When comparing different flower parts, it is worth pointing out how average petal colors-in accordance with their role in advertising the flower for the bee-elicit the highest responses in the receptors. ...
Many pollinating insects acquire their entire nutrition from visiting flowers, and they must therefore be efficient both at detecting flowers and at recognizing familiar rewarding flower types. A crucial first step in recognition is the identification of edges and the segmentation of the visual field into areas that belong together. Honeybees and bumblebees acquire visual information through three types of photoreceptors; however, they only use a single receptor type—the one sensitive to longer wavelengths—for edge detection and movement detection. Here, we show that these long-wavelength receptors (peak sensitivity at ~544 nm, i.e., green) provide the most consistent signals in response to natural objects. Using our multispectral image database of flowering plants, we found that long-wavelength receptor responses had, depending on the specific scenario, up to four times higher signal-to-noise ratios than the short- and medium-wavelength receptors. The reliability of the long-wavelength receptors emerges from an intricate interaction between flower coloration and the bee’s visual system. This finding highlights the adaptive significance of bees using only long-wavelength receptors to locate flowers among leaves, before using information provided by all three receptors to distinguish the rewarding flower species through trichromatic color vision.
Electronic supplementary material
The online version of this article (doi:10.1007/s00359-017-1156-x) contains supplementary material, which is available to authorized users.
... The dorsal region contains more type II ommatidia, with two UV receptors, while the ventral region contains more type III, with two B receptors . The concentration of B receptors in the ventral region of the eye is probably related to a better contrast detection by B receptors of terrestrial targets (Giurfa et al. 1999 ). Behavioral observations indicate that the dorsal rim area, which is crucial for polarization-based navigation, contains exclusively UV receptors (Helversen and Edrich 1974 ), but this has not yet been confi rmed at the molecular level. ...
The spectral sensitivity of photoreceptors is primarily determined by the expressed rhodopsins. After a brief introduction to the photochemistry of insect rhodopsins, the relatively simple case of bee visual pigments and photoreceptors is described, followed by the more complicated cases of butterflies and flies. Although the main focus is on the properties of visual pigments, considerable attention is also given to other photostable filter pigments that importantly modify the spectral properties of the photoreceptors. The sexual dimorphism of the filter pigments results in the sexual dimorphism of photoreceptor spectral sensitivities.
... Srinivasan and Lehrer 1984Lehrer , 1988Giurfa et al. 1996). The extent to which the S-and M-receptor contribute to achromatic vision has not been convincingly established, but some experimental studies indicate the possible involvement of the M-receptor (Menzel 1981;Zhang et al. 1995;Giurfa et al. 1999). Also, phototactic responses can be elicited with wavelengths across the visible spectrum of bees and it has been argued that phototaxis is based on the integration of signals from all three receptor types (Kaiser et al. 1977;Menzel and Greggers 1985). ...
Research in the honeybee has laid the foundations for our understanding of insect colour vision. The trichromatic colour vision of honeybees shares fundamental properties with primate and human colour perception, such as colour constancy, colour opponency, segregation of colour and brightness coding. Laborious efforts to reconstruct the colour vision pathway in the honeybee have provided detailed descriptions of neural connectivity and the properties of photoreceptors and interneurons in the optic lobes of the bee brain. The modelling of colour perception advanced with the establishment of colour discrimination models that were based on experimental data, the Colour-Opponent Coding and Receptor Noise-Limited models, which are important tools for the quantitative assessment of bee colour vision and colour-guided behaviours. Major insights into the visual ecology of bees have been gained combining behavioural experiments and quantitative modelling, and asking how bee vision has influenced the evolution of flower colours and patterns. Recently research has focussed on the discrimination and categorisation of coloured patterns, colourful scenes and various other groupings of coloured stimuli, highlighting the bees' behavioural flexibility. The identification of perceptual mechanisms remains of fundamental importance for the interpretation of their learning strategies and performance in diverse experimental tasks.
... The choice of the bees involved flying toward the target box and thus changes in the image falling in their compound eyes preceded the choice behavior. Furthermore, studies have shown that different regions of the bee's compound eye (ventral, dorsal and frontal) have different properties processing visual stimuli (Giurfa, Zaccardi, & Vorobyev, 1999). In particular, color detection efficiency cue varies depending on the region of the compound eye and the visual extent of the color cue. ...
Visual attention is commonly studied by using visuo-spatial cues indicating probable locations of a target and assessing the effect of the validity of the cue on perceptual performance and its neural correlates. Here, we adapt a cueing task to measure spatial cueing effects on the decisions of honeybees and compare their behavior to that of humans and monkeys in a similarly structured two-alternative forced-choice perceptual task. Unlike the typical cueing paradigm in which the stimulus strength remains unchanged within a block of trials, for the monkey and human studies we randomized the contrast of the signal to simulate more real world conditions in which the organism is uncertain about the strength of the signal. A Bayesian ideal observer that weights sensory evidence from cued and uncued locations based on the cue validity to maximize overall performance is used as a benchmark of comparison against the three animals and other suboptimal models: probability matching, ignore the cue, always follow the cue, and an additive bias/single decision threshold model. We find that the cueing effect is pervasive across all three species but is smaller in size than that shown by the Bayesian ideal observer. Humans show a larger cueing effect than monkeys and bees show the smallest effect. The cueing effect and overall performance of the honeybees allows rejection of the models in which the bees are ignoring the cue, following the cue and disregarding stimuli to be discriminated, or adopting a probability matching strategy. Stimulus strength uncertainty also reduces the theoretically predicted variation in cueing effect with stimulus strength of an optimal Bayesian observer and diminishes the size of the cueing effect when stimulus strength is low. A more biologically plausible model that includes an additive bias to the sensory response from the cued location, although not mathematically equivalent to the optimal observer for the case stimulus strength uncertainty, can approximate the benefits of the more computationally complex optimal Bayesian model. We discuss the implications of our findings on the field's common conceptualization of covert visual attention in the cueing task and what aspects, if any, might be unique to humans.
... Green-light processing both in the MU-VL and the MU-DL may encode spectral information directly related to the sun (Wehner and Rossel, 1985). The fact that intertubercle neurons in the MU-DL, which mostly process ventral eye information (Mota et al., 2011), are strongly activated by blue light is consistent with the higher proportion of M photoreceptors in the ventral part of the bee eye (Wakakuwa et al., 2005) and with an improved detection of targets in ventral eye regions based on contrast to M photoreceptors (Giurfa et al., 1999). These hypotheses constitute starting points for future studies aimed at unraveling the function of AOTu in honey bees. ...
Color vision in honey bees (Apis mellifera) has been extensively studied at the behavioral level and, to a lesser degree, at the physiological level by means of electrophysiological intracellular recordings of single neurons. Few visual neurons have been so far characterized in the lateral protocerebrum of bees. Therefore, the possible implication of this region in chromatic processing remains unknown. We performed in vivo calcium imaging of interneurons in the anterior optic tubercle (AOTu) of honey bees upon visual stimulation of the compound eye to analyze chromatic response properties. Stimulation with distinct monochromatic lights (ultraviolet [UV], blue, and green) matching the sensitivity of the three photoreceptor types of the bee retina induced different signal amplitudes, temporal dynamics, and spatial activity patterns in the AOTu intertubercle network, thus revealing intricate chromatic processing properties. Green light strongly activated both the dorsal and ventral lobes of the AOTu's major unit; blue light activated the dorsal lobe more while UV light activated the ventral lobe more. Eye stimulation with mixtures of blue and green light induced suppression phenomena in which responses to the mixture were lower than those to the color components, thus concurring with color-opponent processing. These data provide evidence for a spatial segregation of color processing in the AOTu, which may serve for navigation purposes.
... A. Avarguès-Weber et al. and Meyer 2002;Spaethe and Briscoe 2005), and (2) the anterior ventral region (av), whose function remains unclear and in which type III ommatidia are more frequent, thus constituting a region with a density of M (blue) receptors that is higher than that of the other regions of the retina (Wakakuwa et al. 2005; Figure 5b). Concentration of M receptors in the ventral region of the eye (also found in Manduca sexta by White et al. 2003) may be related to a better ventral detection of targets providing contrast to M receptors (Giurfa et al. 1999) and/or to enhanced colored target detection by this eye region (Menzel and Lieke 1983;Lehrer 1998Lehrer , 1999. ...
... This segregation of dorsoventral visual information in the AOTu of bees may be related to the specializations uncovered in the dorsal and ventral parts of the bee retina (see Section 3.2). Moreover, it may be part of the neural mechanisms behind the remarkable asymmetries in behavioral performances involving the dorsal and ventral eye regions (Menzel and Snyder 1974;Anderson 1977;Menzel and Lieke 1983;Rossel and Wehner 1986;Giger and Srinivasan 1997;Lehrer 1998Lehrer , 1999Giurfa et al. 1999). ...
The honey bee is a traditional animal model for the study of visual perception, learning, and memory. Extensive behavioral studies have shown that honey bees perceive, learn, and memorize colors, shapes, and patterns when these visual cues are paired with sucrose reward. Bee color vision is trichromatic, based on three photoreceptor types (S, M, L), which peak in the UV, blue, and green region of the spectrum. Perceptual color spaces have been proposed to account for bee color vision, and the anatomy of the visual neuropils in the bee brain was described to a large extent. In the last decade, conceptual and technical advances improved significantly our comprehension of visual processing in bees. At the behavioral level, unexpected cognitive visual capacities were discovered such as categorical and conceptual categorization. At the neurobiological level, molecular analyses of the compound eye revealed an intricate heterogeneity in the distribution of photoreceptors in the retina. Spatial segregation and integration of visual information in the bee brain has been analyzed at functional levels so far unexploited. These recent discoveries associated with the perspective of accessing the bee brain of harnessed bees while they perceive and learn visual cues open new avenues toward a comprehension of the neural substrates of visual perception and learning in bees. Understanding how the miniature brain of bees achieves sophisticated visual performances is a fundamental goal for the comparative study of vision and cognition.
