Learning modifies attention during bumblebee visual search.

Abstract: The role of visual search during bee foraging is relatively understudied compared to the choices made by bees. As bees learn about rewards, we predicted that visual search would be modified to prioritise rewarding flowers. To test this, we ran an experiment testing how bee search differs in the initial and later part of training as they learn about flowers with either higher- or lower-quality rewards. We then ran an experiment to see how this prior training with reward influences their search on a subsequent task with different flowers. We used the time spent inspecting flowers as a measure of attention and found that learning increased attention to rewards and away from unrewarding flowers. Higher quality rewards led to decreased attention to non-flower regions, but lower quality rewards did not. Prior experience of lower rewards also led to more attention to higher rewards compared to unrewarding flowers and non-flower regions. Our results suggest that flowers would elicit differences in bee search behaviour depending on the sugar content of their nectar. They also demonstrate the utility of studying visual search and have important implications for understanding the pollination ecology of flowers with different qualities of reward. Significance statement: Studies investigating how foraging bees learn about reward typically focus on the choices made by the bees. How bees deploy attention and visual search during foraging is less well studied. We analysed flight videos to characterise visual search as bees learn which flowers are rewarding. We found that learning increases the focus of bees on flower regions. We also found that the quality of the reward a flower offers influences how much bees search in non-flower areas. This means that a flower with lower reward attracts less focussed foraging compared to one with a higher reward. Since flowers do differ in floral reward, this has important implications for how focussed pollinators will be on different flowers. Our approach of looking at search behaviour and attention thus advances our understanding of the cognitive ecology of pollination. Supplementary Information: The online version contains supplementary material available at 10.1007/s00265-024-03432-z.

A computational model of stereoscopic prey capture in praying mantises.

We present a simple model which can account for the stereoscopic sensitivity of praying mantis predatory strikes. The model consists of a single "disparity sensor": a binocular neuron sensitive to stereoscopic disparity and thus to distance from the animal. The model is based closely on the known behavioural and neurophysiological properties of mantis stereopsis. The monocular inputs to the neuron reflect temporal change and are insensitive to contrast sign, making the sensor insensitive to interocular correlation. The monocular receptive fields have a excitatory centre and inhibitory surround, making them tuned to size. The disparity sensor combines inputs from the two eyes linearly, applies a threshold and then an exponent output nonlinearity. The activity of the sensor represents the model mantis's instantaneous probability of striking. We integrate this over the stimulus duration to obtain the expected number of strikes in response to moving targets with different stereoscopic disparity, size and vertical disparity. We optimised the parameters of the model so as to bring its predictions into agreement with our empirical data on mean strike rate as a function of stimulus size and disparity. The model proves capable of reproducing the relatively broad tuning to size and narrow tuning to stereoscopic disparity seen in mantis striking behaviour. Although the model has only a single centre-surround receptive field in each eye, it displays qualitatively the same interaction between size and disparity as we observed in real mantids: the preferred size increases as simulated prey distance increases beyond the preferred distance. We show that this occurs because of a stereoscopic "false match" between the leading edge of the stimulus in one eye and its trailing edge in the other; further work will be required to find whether such false matches occur in real mantises. Importantly, the model also displays realistic responses to stimuli with vertical disparity and to pairs of identical stimuli offering a "ghost match", despite not being fitted to these data. This is the first image-computable model of insect stereopsis, and reproduces key features of both neurophysiology and striking behaviour.

Rhythmic abilities in humans and non-human animals: a review and recommendations from a methodological perspective.

Rhythmic behaviour is ubiquitous in both human and non-human animals, but it is unclear whether the cognitive mechanisms underlying the specific rhythmic behaviours observed in different species are related. Laboratory experiments combined with highly controlled stimuli and tasks can be very effective in probing the cognitive architecture underlying rhythmic abilities. Rhythmic abilities have been examined in the laboratory with explicit and implicit perception tasks, and with production tasks, such as sensorimotor synchronization, with stimuli ranging from isochronous sequences of artificial sounds to human music. Here, we provide an overview of experimental findings on rhythmic abilities in human and non-human animals, while critically considering the wide variety of paradigms used. We identify several gaps in what is known about rhythmic abilities. Many bird species have been tested on rhythm perception, but research on rhythm production abilities in the same birds is lacking. By contrast, research in mammals has primarily focused on rhythm production rather than perception. Many experiments also do not differentiate between possible components of rhythmic abilities, such as processing of single temporal intervals, rhythmic patterns, a regular beat or hierarchical metrical structures. For future research, we suggest a careful choice of paradigm to aid cross-species comparisons, and a critical consideration of the multifaceted abilities that underlie rhythmic behaviour. This article is part of the theme issue 'Synchrony and rhythm interaction: from the brain to behavioural ecology'.

An ecological approach to measuring synchronization abilities across the animal kingdom.

In this perspective paper, we focus on the study of synchronization abilities across the animal kingdom. We propose an ecological approach to studying nonhuman animal synchronization that begins from observations about when, how and why an animal might synchronize spontaneously with natural environmental rhythms. We discuss what we consider to be the most important, but thus far largely understudied, temporal, physical, perceptual and motivational constraints that must be taken into account when designing experiments to test synchronization in nonhuman animals. First and foremost, different species are likely to be sensitive to and therefore capable of synchronizing at different timescales. We also argue that it is fruitful to consider the latent flexibility of animal synchronization. Finally, we discuss the importance of an animal's motivational state for showcasing synchronization abilities. We demonstrate that the likelihood that an animal can successfully synchronize with an environmental rhythm is context-dependent and suggest that the list of species capable of synchronization is likely to grow when tested with ecologically honest, species-tuned experiments. This article is part of the theme issue 'Synchrony and rhythm interaction: from the brain to behavioural ecology'.

Rhythm interaction in animal groups: selective attention in communication networks.

Animals communicating interactively with conspecifics often time their broadcasts to avoid overlapping interference, to emit leading, as opposed to following, signals or to synchronize their signalling rhythms. Each of these adjustments becomes more difficult as the number of interactants increases beyond a pair. Among acoustic species, insects and anurans generally deal with the problem of group signalling by means of 'selective attention' in which they focus on several close or conspicuous neighbours and ignore the rest. In these animals, where signalling and receiving are often dictated by sex, the process of selective attention in signallers may have a parallel counterpart in receivers, which also focus on close neighbours. In birds and mammals, local groups tend to be extended families or clans, and group signalling may entail complex timing mechanisms that allow for attention to all individuals. In general, the mechanisms that allow animals to communicate in groups appear to be fully interwoven with the basic process of rhythmic signalling. This article is part of the theme issue 'Synchrony and rhythm interaction: from the brain to behavioural ecology'.

Synchrony of complex signals in an acoustically communicating katydid.

The ability to entrain to auditory stimuli has been a powerful method to investigate the comparative rhythm abilities of different animals. While synchrony to regular simple rhythms is well documented, synchrony to complex stimuli, with multiple components at unequal time intervals, is rarer. Several katydid species with simple calls have been shown to achieve synchrony as part of their natural calling interactions in multi-individual choruses. Yet no study so far has demonstrated synchrony in any insect with a complex call. Using natural calling behaviour and playback experiments, we investigated acoustic synchrony and the mechanisms underlying it in the katydid species Mecopoda 'Two Part Caller'. This species has a complex call consisting of a long trill followed by two or more chirps. We found that individual males synchronized trills and, to a lesser extent, chirps. Further investigation of trill synchrony showed that the timing of trills is modified by external trills but not chirps. Chirp synchrony is modified by external chirps, but also by trills. We suggest a qualitative two-oscillator model underlying synchrony in this species and discuss the implications for the evolution of acoustic synchrony.

Different effects of reward value and saliency during bumblebee visual search for multiple rewarding targets.

Several animals, including bees, use visual search to distinguish targets of interest and ignore distractors. While bee flower choice is well studied, we know relatively little about how they choose between multiple rewarding flowers in complex floral environments. Two factors that could influence bee visual search for multiple flowers are the saliency (colour contrast against the background) and the reward value of flowers. We here investigated how these two different factors contribute to bee visual search. We trained bees to independently recognize two rewarding flower types that, in different experiments, differed in either saliency, reward value or both. We then measured their choices and attention to these flowers in the presence of distractors in a test without reinforcement. We found that bees preferred more salient or higher rewarding flowers and ignored distractors. When the high-reward flowers were less salient than the low-reward flowers, bees were nonetheless equally likely to choose high-reward flowers, for the reward and saliency values we used. Bees were also more likely to attend to these high-reward flowers, spending higher inspection times around them and exhibiting faster search times when choosing them. When flowers differed in reward, we also found an effect of the training order with low-reward targets being more likely to be chosen if they had been encountered during the more immediate training session prior to the test. Our results parallel recent findings from humans demonstrating that reward value can attract attention even when targets are less salient and irrelevant to the current task.

Insect Neurobiology: Divergent Neural Computations in Predatory Insects.

A comparative approach to neuroscience can greatly increase our understanding of how mechanisms map onto behaviour. A new study comparing two predatory insects demonstrates how neurons that are homologous can nonetheless mediate different computations and behaviour.

Second-order cues to figure motion enable object detection during prey capture by praying mantises.

Detecting motion is essential for animals to perform a wide variety of functions. In order to do so, animals could exploit motion cues, including both first-order cues-such as luminance correlation over time-and second-order cues, by correlating higher-order visual statistics. Since first-order motion cues are typically sufficient for motion detection, it is unclear why sensitivity to second-order motion has evolved in animals, including insects. Here, we investigate the role of second-order motion in prey capture by praying mantises. We show that prey detection uses second-order motion cues to detect figure motion. We further present a model of prey detection based on second-order motion sensitivity, resulting from a layer of position detectors feeding into a second layer of elementary-motion detectors. Mantis stereopsis, in contrast, does not require figure motion and is explained by a simpler model that uses only the first layer in both eyes. Second-order motion cues thus enable prey motion to be detected, even when perfectly matching the average background luminance and independent of the elementary motion of any parts of the prey. Subsequent to prey detection, processes such as stereopsis could work to determine the distance to the prey. We thus demonstrate how second-order motion mechanisms enable ecologically relevant behavior such as detecting camouflaged targets for other visual functions including stereopsis and target tracking.

Motion-in-depth perception and prey capture in the praying mantis Sphodromantis lineola.

Perceiving motion-in-depth is essential to detecting approaching or receding objects, predators and prey. This can be achieved using several cues, including binocular stereoscopic cues such as changing disparity and interocular velocity differences, and monocular cues such as looming. Although these have been studied in detail in humans, only looming responses have been well characterized in insects and we know nothing about the role of stereoscopic cues and how they might interact with looming cues. We used our 3D insect cinema in a series of experiments to investigate the role of the stereoscopic cues mentioned above, as well as looming, in the perception of motion-in-depth during predatory strikes by the praying mantis Sphodromantis lineola Our results show that motion-in-depth does increase the probability of mantis strikes but only for the classic looming stimulus, an expanding luminance edge. Approach indicated by radial motion of a texture or expansion of a motion-defined edge, or by stereoscopic cues, all failed to elicit increased striking. We conclude that mantises use stereopsis to detect depth but not motion-in-depth, which is detected via looming.

Contrast thresholds reveal different visual masking functions in humans and praying mantises.

Recently, we showed a novel property of the Hassenstein-Reichardt detector, namely that insect motion detection can be masked by 'undetectable' noise, i.e. visual noise presented at spatial frequencies at which coherently moving gratings do not elicit a response (Tarawneh et al., 2017). That study compared the responses of human and insect motion detectors using different ways of quantifying masking (contrast threshold in humans and masking tuning function in insects). In addition, some adjustments in experimental procedure, such as presenting the stimulus at a short viewing distance, were necessary to elicit a response in insects. These differences offer alternative explanations for the observed difference between human and insect responses to visual motion noise. Here, we report the results of new masking experiments in which we test whether differences in experimental paradigm and stimulus presentation between humans and insects can account for the undetectable noise effect reported earlier. We obtained contrast thresholds at two signal and two noise frequencies in both humans and praying mantises (Sphodromantis lineola), and compared contrast threshold differences when noise has the same versus different spatial frequency as the signal. Furthermore, we investigated whether differences in viewing geometry had any qualitative impact on the results. Consistent with our earlier finding, differences in contrast threshold show that visual noise masks much more effectively when presented at signal spatial frequency in humans (compared to a lower or higher spatial frequency), while in insects, noise is roughly equivalently effective when presented at either the signal spatial frequency or lower (compared to a higher spatial frequency). The characteristic difference between human and insect responses was unaffected by correcting for the stimulus distortion caused by short viewing distances in insects. These findings constitute stronger evidence that the undetectable noise effect reported earlier is a genuine difference between human and insect motion processing, and not an artefact caused by differences in experimental paradigms.

A Novel Form of Stereo Vision in the Praying Mantis.

Stereopsis is the ability to estimate distance based on the different views seen in the two eyes [1-5]. It is an important model perceptual system in neuroscience and a major area of machine vision. Mammalian, avian, and almost all machine stereo algorithms look for similarities between the luminance-defined images in the two eyes, using a series of computations to produce a map showing how depth varies across the scene [3, 4, 6-14]. Stereopsis has also evolved in at least one invertebrate, the praying mantis [15-17]. Mantis stereopsis is presumed to be simpler than vertebrates' [15, 18], but little is currently known about the underlying computations. Here, we show that mantis stereopsis uses a fundamentally different computational algorithm from vertebrate stereopsis-rather than comparing luminance in the two eyes' images directly, mantis stereopsis looks for regions of the images where luminance is changing. Thus, while there is no evidence that mantis stereopsis works at all with static images, it successfully reveals the distance to a moving target even in complex visual scenes with targets that are perfectly camouflaged against the background in terms of texture. Strikingly, these insects outperform human observers at judging stereoscopic distance when the pattern of luminance in the two eyes does not match. Insect stereopsis has thus evolved to be computationally efficient while being robust to poor image resolution and to discrepancies in the pattern of luminance between the two eyes. VIDEO ABSTRACT.

Apparent Motion Perception in the Praying Mantis: Psychophysics and Modelling.

Apparent motion is the perception of motion created by rapidly presenting still frames in which objects are displaced in space. Observers can reliably discriminate the direction of apparent motion when inter-frame object displacement is below a certain limit, Dmax . Earlier studies of motion perception in humans found that Dmax is lower-bounded at around 15 arcmin, and thereafter scales with the size of the spatial elements in the images. Here, we run corresponding experiments in the praying mantis Sphodromantis lineola to investigate how Dmax scales with the element size. We use random moving chequerboard patterns of varying element and displacement step sizes to elicit the optomotor response, a postural stabilization mechanism that causes mantids to lean in the direction of large-field motion. Subsequently, we calculate Dmax as the displacement step size corresponding to a 50% probability of detecting an optomotor response in the same direction as the stimulus. Our main findings are that the mantis Dmax scales roughly as a square-root of element size and that, in contrast to humans, it is not lower-bounded. We present two models to explain these observations: a simple high-level model based on motion energy in the Fourier domain and a more-detailed one based on the Reichardt Detector. The models present complementary intuitive and physiologically-realistic accounts of how Dmax scales with the element size in insects. We conclude that insect motion perception is limited by only a single stage of spatial filtering, reflecting the optics of the compound eye. In contrast, human motion perception reflects a second stage of spatial filtering, at coarser scales than imposed by human optics, likely corresponding to the magnocellular pathway. After this spatial filtering, mantis and human motion perception and Dmax are qualitatively very similar.

Stereopsis in animals: evolution, function and mechanisms.

Stereopsis is the computation of depth information from views acquired simultaneously from different points in space. For many years, stereopsis was thought to be confined to primates and other mammals with front-facing eyes. However, stereopsis has now been demonstrated in many other animals, including lateral-eyed prey mammals, birds, amphibians and invertebrates. The diversity of animals known to have stereo vision allows us to begin to investigate ideas about its evolution and the underlying selective pressures in different animals. It also further prompts the question of whether all animals have evolved essentially the same algorithms to implement stereopsis. If so, this must be the best way to do stereo vision, and should be implemented by engineers in machine stereopsis. Conversely, if animals have evolved a range of stereo algorithms in response to different pressures, that could inspire novel forms of machine stereopsis appropriate for distinct environments, tasks or constraints. As a first step towards addressing these ideas, we here review our current knowledge of stereo vision in animals, with a view towards outlining common principles about the evolution, function and mechanisms of stereo vision across the animal kingdom. We conclude by outlining avenues for future work, including research into possible new mechanisms of stereo vision, with implications for machine vision and the role of stereopsis in the evolution of camouflage.

Invisible noise obscures visible signal in insect motion detection.

The motion energy model is the standard account of motion detection in animals from beetles to humans. Despite this common basis, we show here that a difference in the early stages of visual processing between mammals and insects leads this model to make radically different behavioural predictions. In insects, early filtering is spatially lowpass, which makes the surprising prediction that motion detection can be impaired by "invisible" noise, i.e. noise at a spatial frequency that elicits no response when presented on its own as a signal. We confirm this prediction using the optomotor response of praying mantis Sphodromantis lineola. This does not occur in mammals, where spatially bandpass early filtering means that linear systems techniques, such as deriving channel sensitivity from masking functions, remain approximately valid. Counter-intuitive effects such as masking by invisible noise may occur in neural circuits wherever a nonlinearity is followed by a difference operation.

The optomotor response of the praying mantis is driven predominantly by the central visual field.

The optomotor response has been widely used to investigate insect sensitivity to contrast and motion. Several studies have revealed the sensitivity of this response to frequency and contrast, but we know less about the spatial integration underlying this response. Specifically, few studies have investigated how the horizontal angular extent of stimuli influences the optomotor response. We presented mantises with moving gratings of varying horizontal extents at three different contrasts in the central or peripheral regions of their visual fields. We assessed the relative effectivity of different regions to elicit the optomotor response and modelled the dependency of the response on the angular extent subtended by stimuli at these different regions. Our results show that the optomotor response is governed by stimuli in the central visual field and not in the periphery. The model also shows that in the central region, the probability of response increases linearly with increase in horizontal extent up to a saturation point. Furthermore, the dependency of the optomotor response on the angular extent of the stimulus is modulated by contrast. We discuss the implications of our results for different modes of stimulus presentation and for models of the underlying mechanisms of motion detection in the mantis.

Attention-like processes in insects.

Attention is fundamentally important for sensory systems to focus on behaviourally relevant stimuli. It has therefore been an important field of study in human psychology and neuroscience. Primates, however, are not the only animals that might benefit from attention-like processes. Other animals, including insects, also have to use their senses and select one among many stimuli to forage, avoid predators and find mates. They have evolved different mechanisms to reduce the information processed by their brains to focus on only relevant stimuli. What are the mechanisms used by insects to selectively attend to visual and auditory stimuli? Do these attention-like mechanisms achieve the same functions as they do in primates? To investigate these questions, I use an established framework for investigating attention in non-human animals that proposes four fundamental components of attention: salience filters, competitive selection, top-down sensitivity control and working memory. I discuss evidence for each of these component processes in insects and compare the characteristics of these processes in insects to what we know from primates. Finally, I highlight important outstanding questions about insect attention that need to be addressed for us to understand the differences and similarities between vertebrate and insect attention.

Small or far away? Size and distance perception in the praying mantis.

Stereo or '3D' vision is an important but costly process seen in several evolutionarily distinct lineages including primates, birds and insects. Many selective advantages could have led to the evolution of stereo vision, including range finding, camouflage breaking and estimation of object size. In this paper, we investigate the possibility that stereo vision enables praying mantises to estimate the size of prey by using a combination of disparity cues and angular size cues. We used a recently developed insect 3D cinema paradigm to present mantises with virtual prey having differing disparity and angular size cues. We predicted that if they were able to use these cues to gauge the absolute size of objects, we should see evidence for size constancy where they would strike preferentially at prey of a particular physical size, across a range of simulated distances. We found that mantises struck most often when disparity cues implied a prey distance of 2.5 cm; increasing the implied distance caused a significant reduction in the number of strikes. We, however, found no evidence for size constancy. There was a significant interaction effect of the simulated distance and angular size on the number of strikes made by the mantis but this was not in the direction predicted by size constancy. This indicates that mantises do not use their stereo vision to estimate object size. We conclude that other selective advantages, not size constancy, have driven the evolution of stereo vision in the praying mantis.This article is part of the themed issue 'Vision in our three-dimensional world'.

Insect stereopsis demonstrated using a 3D insect cinema.

Stereopsis - 3D vision - has become widely used as a model of perception. However, all our knowledge of possible underlying mechanisms comes almost exclusively from vertebrates. While stereopsis has been demonstrated for one invertebrate, the praying mantis, a lack of techniques to probe invertebrate stereopsis has prevented any further progress for three decades. We therefore developed a stereoscopic display system for insects, using miniature 3D glasses to present separate images to each eye, and tested our ability to deliver stereoscopic illusions to praying mantises. We find that while filtering by circular polarization failed due to excessive crosstalk, "anaglyph" filtering by spectral content clearly succeeded in giving the mantis the illusion of 3D depth. We thus definitively demonstrate stereopsis in mantises and also demonstrate that the anaglyph technique can be effectively used to deliver virtual 3D stimuli to insects. This method opens up broad avenues of research into the parallel evolution of stereoscopic computations and possible new algorithms for depth perception.

Modality-specific attention in foraging bumblebees.

Attentional demands can prevent humans and other animals from performing multiple tasks simultaneously. Some studies, however, show that tasks presented in different sensory modalities (e.g. visual and auditory) can be processed simultaneously. This suggests that, at least in these cases, attention might be modality-specific and divided differently between tasks when present in the same modality compared with different modalities. We investigated this possibility in bumblebees (Bombus terrestris) using a biologically relevant experimental set-up where they had to simultaneously choose more rewarding flowers and avoid simulated predatory attacks by robotic 'spiders'. We found that when the tasks had to be performed using visual cues alone, bees failed to perform both tasks simultaneously. However, when highly rewarding flowers were indicated by olfactory cues and predators were indicated by visual cues, bees managed to perform both tasks successfully. Our results thus provide evidence for modality-specific attention in foraging bees and establish a novel framework for future studies of crossmodal attention in ecologically realistic settings.