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Recent developments allowed establishing virtual‐reality (VR) setups to study multiple aspects of visual learning in honey bees under controlled experimental conditions. Here, we adopted a VR environment to investigate the visual learning in the buff‐tailed bumble bee Bombus terrestris. Based on responses to appetitive and aversive reinforcements used for conditioning, we show that bumble bees had the proper appetitive motivation to engage in the VR experiments and that they learned efficiently elemental color discriminations. In doing so, they reduced the latency to make a choice, increased the proportion of direct paths toward the virtual stimuli and walked faster toward them. Performance in a short‐term retention test showed that bumble bees chose and fixated longer on the correct stimulus in the absence of reinforcement. Body size and weight, although variable across individuals, did not affect cognitive performances and had a mild impact on motor performances. Overall, we show that bumble bees are suitable experimental subjects for experiments on visual learning under VR conditions, which opens important perspectives for invasive studies on the neural and molecular bases of such learning given the robustness of these insects and the accessibility of their brain. [ABSTRACT FROM AUTHOR]

The question of whether individuals perform consistently across a variety of cognitive tasks is relevant for studies of comparative cognition. The honey bee (Apis mellifera) is an appropriate model to study cognitive consistency as its learning can be studied in multiple elemental and non-elemental learning tasks. We took advantage of this possibility and studied if the ability of honey bees to learn a simple discrimination correlates with their ability to solve two tasks of higher complexity, reversal learning and negative patterning. We performed four experiments in which we varied the sensory modality of the stimuli (visual or olfactory) and the type (Pavlovian or operant) and complexity (elemental or non-elemental) of conditioning to examine if stable correlated performances could be observed across experiments. Across all experiments, an individual's proficiency to learn the simple discrimination task was positively and significantly correlated with performance in both reversal learning and negative patterning, while the performances in reversal learning and negative patterning were positively, yet not significantly correlated. These results suggest that correlated performances across learning paradigms represent a distinct cognitive characteristic of bees. Further research is necessary to examine if individual cognitive consistency can be found in other insect species as a common characteristic of insect brains. [ABSTRACT FROM AUTHOR]

The "mental number line" (MNL) is a form of spatial numeric representation that associates small and large numbers with the left and right spaces, respectively. This spatio-numeric organization can be found in adult humans and has been related to cultural factors such as writing and reading habits. Yet, both human newborns and birds order numbers consistently with an MNL, thus raising the question of whether culture is a main explanation for MNL. Here, we explored the numeric sense of honey bees and show that after being trained to associate numbers with a sucrose reward, they order numbers not previously experienced from left to right according to their magnitude. Importantly, the location of a number on that scale varies with the reference number previously trained and does not depend on low-level cues present on numeric stimuli. We provide a series of neural explanations for this effect based on the extensive knowledge accumulated on the neural underpinnings of visual processing in honey bees and conclude that the MNL is a form of numeric representation that is evolutionarily conserved across nervous systems endowed with a sense of number, irrespective of their neural complexity. [ABSTRACT FROM AUTHOR]

Honey bees are reputed for their remarkable visual learning and navigation capabilities. These capacities can be studied in virtual reality (VR) environments, which allow studying performances of tethered animals in stationary flight or walk under full control of the sensory environment. Here, we used a 2D VR setup in which a tethered bee walking stationary under restrictive closed-loop conditions learned to discriminate vertical rectangles differing in color and reinforcing outcome. Closed-loop conditions restricted stimulus control to lateral displacements. Consistently with prior VR analyses, bees learned to discriminate the trained stimuli. Ex vivo analyses on the brains of learners and non-learners showed that successful learning led to a downregulation of three immediate early genes in the main regions of the visual circuit, the optic lobes (OLs) and the calyces of the mushroom bodies (MBs). While Egr1 was downregulated in the OLs, Hr38 and kakusei were coincidently downregulated in the calyces of the MBs. Our work thus reveals that color discrimination learning induced a neural signature distributed along the sequential pathway of color processing that is consistent with an inhibitory trace. This trace may relate to the motor patterns required to solve the discrimination task, which are different from those underlying pathfinding in 3D VR scenarios allowing for navigation and exploratory learning and which lead to IEG upregulation. [ABSTRACT FROM AUTHOR]

Free-flying bees learn efficiently to solve numerous visual tasks. Yet, the neural underpinnings of this capacity remain unexplored. We used a 3D virtual reality (VR) environment to study visual learning and determine if it leads to changes in immediate early gene (IEG) expression in specific areas of the bee brain. We focused on kakusei, Hr38 and Egr1, three IEGs that have been related to bee foraging and orientation, and compared their relative expression in the calyces of the mushroom bodies, the optic lobes and the rest of the brain after color discrimination learning. Bees learned to discriminate virtual stimuli displaying different colors and retained the information learned. Successful learners exhibited Egr1 upregulation only in the calyces of the mushroom bodies, thus uncovering a privileged involvement of these brain regions in associative color learning and the usefulness of Egr1 as a marker of neural activity induced by this phenomenon. The neural bases of visual learning in bees have been understudied, relative to the olfactory learning process. Using a 3D virtual reality environment and gene expression analyses, the neural underpinnings of visual learning are explored here. [ABSTRACT FROM AUTHOR]

Honey bees exhibit remarkable visual learning capacities, which can be studied using virtual reality (VR) landscapes in laboratory conditions. Existing VR environments for bees are imperfect as they provide either open-loop conditions or 2D displays. Here we achieved a true 3D environment in which walking bees learned to discriminate a rewarded from a punished virtual stimulus based on color differences. We included ventral or frontal background cues, which were also subjected to 3D updating based on the bee movements. We thus studied if and how the presence of such motion cues affected visual discrimination in our VR landscape. Our results showed that the presence of frontal, and to a lesser extent, of ventral background motion cues impaired the bees' performance. Whenever these cues were suppressed, color discrimination learning became possible. We analyzed the specific contribution of foreground and background cues and discussed the role of attentional interference and differences in stimulus salience in the VR environment to account for these results. Overall, we show how background and target cues may interact at the perceptual level and influence associative learning in bees. In addition, we identify issues that may affect decision-making in VR landscapes, which require specific control by experimenters. [ABSTRACT FROM AUTHOR]

The adipokinetic hormone (AKH) of insects is considered an equivalent of the mammalian hormone glucagon as it induces fast mobilization of carbohydrates and lipids from the fat body upon starvation. Yet, in foraging honey bees, which lack fat body storage for carbohydrates, it was suggested that AKH may have lost its original function. Here we manipulated the energy budget of bee foragers to determine the effect of AKH on appetitive responses. As AKH participates in a cascade leading to acceptance of unpalatable substances in starved Drosophila, we also assessed its effect on foragers presented with sucrose solution spiked with salicin. Starved and partially-fed bees were topically exposed with different doses of AKH to determine if this hormone modifies food ingestion and sucrose responsiveness. We found a significant effect of the energy budget (i.e. starved vs. partially-fed) on the decision to ingest or respond to both pure sucrose solution and sucrose solution spiked with salicin, but no effect of AKH per se. These results are consistent with a loss of function of AKH in honey bee foragers, in accordance with a social life that implies storing energy resources in the hive, in amounts that exceed individual needs. [ABSTRACT FROM AUTHOR]

Understanding the neural principles governing taste perception in species that bear economic importance or serve as research models for other sensory modalities constitutes a strategic goal. Such is the case of the honey bee (Apis mellifera), which is environmentally and socioeconomically important, given its crucial role as pollinator agent in agricultural landscapes and which has served as a traditional model for visual and olfactory neurosciences and for research on communication, navigation, and learning and memory. Here we review the current knowledge on honey bee gustatory receptors to provide an integrative view of peripheral taste detection in this insect, highlighting specificities and commonalities with other insect species. We describe behavioral and electrophysiological responses to several tastant categories and relate these responses, whenever possible, to known molecular receptor mechanisms. Overall, we adopted an evolutionary and comparative perspective to understand the neural principles of honey bee taste and define key questions that should be answered in future gustatory research centered on this insect. [ABSTRACT FROM AUTHOR]

The capacity to process numbers can be found in many vertebrate species, which share similar behavioral and neural mechanisms for number estimation. Honeybees possess a miniature brain but exhibit remarkable cognitive abilities, including the capacity to perform numerosity judgments in a foraging context. Honeybee foragers can count up to four landmarks en route to the goal and use this information to decide where to land. They also learn to match visual images based on item number and may use absolute or relative numerosity. They can be trained to choose item arrays based on rules such as 'smaller than', in which case their performance reveals the existence of zero as a conceptual low end of a succession of positive numbers. Moreover, in symbolic-matching protocols, they learn to master visual discriminations based on subtracting or adding one item to a perceived sample, depending on the color of the sample array. Here I review the works on numeric processing in bees and discuss them from a cognitive and ecological perspective. I conclude that these abilities exhibit distinctive features of the vertebrates' numeric systems, and argue in favor of an evolutionary convergence of numeric abilities in many animal species, including vertebrates, and invertebrates. [ABSTRACT FROM AUTHOR]

Abstract The honey bee Apis mellifera is a major insect model for studying visual cognition. Free-flying honey bees learn to associate different visual cues with a sucrose reward and may deploy sophisticated cognitive strategies to this end. Yet, the neural bases of these capacities cannot be studied in flying insects. Conversely, immobilized bees are accessible to neurobiological investigation but training them to respond appetitively to visual stimuli paired with sucrose reward is difficult. Here we succeeded in coupling visual conditioning in harnessed bees with pharmacological analyses on the role of octopamine (OA), dopamine (DA) and serotonin (5-HT) in visual learning. We also studied if and how these biogenic amines modulate sucrose responsiveness and phototaxis behaviour as intact reward and visual perception are essential prerequisites for appetitive visual learning. Our results suggest that both octopaminergic and dopaminergic signaling mediate either the appetitive sucrose signaling or the association between color and sucrose reward in the bee brain. Enhancing and inhibiting serotonergic signaling both compromised learning performances, probably via an impairment of visual perception. We thus provide a first analysis of the role of aminergic signaling in visual learning and retention in the honey bee and discuss further research trends necessary to understand the neural bases of visual cognition in this insect. [ABSTRACT FROM AUTHOR]

To study visual learning in honey bees, we developed a virtual reality (VR) system in which the movements of a tethered bee walking stationary on a spherical treadmill update the visual panorama presented in front of it (closed-loop conditions), thus creating an experience of immersion within a virtual environment. In parallel, we developed a small Y-maze with interchangeable end-boxes, which allowed replacing repeatedly a freely walking bee into the starting point of the maze for repeated decision recording. Using conditioning and transfer experiments between the VR setup and the Y-maze, we studied the extent to which movement freedom and active vision are crucial for learning a simple color discrimination. Approximately 57% of the bees learned the visual discrimination in both conditions. Transfer from VR to the maze improved significantly the bees' performances: 75% of bees having chosen the CS+ continued doing so and 100% of bees having chosen the CS- reverted their choice in favor of the CS+. In contrast, no improvement was seen for these two groups of bees during the reciprocal transfer from the Y-maze to VR. In this case, bees exhibited inconsistent choices in the VR setup. The asymmetric transfer between contexts indicates that the information learned in each environment may be different despite the similar learning success. Moreover, it shows that reducing the possibility of active vision and movement freedom in the passage from the maze to the VR impairs the expression of visual learning while increasing them in the reciprocal transfer improves it. Our results underline the active nature of visual processing in bees and allow discussing the developments required for immersive VR experiences in insects. [ABSTRACT FROM AUTHOR]

Among insects, Hymenoptera present a striking olfactory system with a clear neural dichotomy from the periphery to higher order centers, based on two main tracts of second-order (projection) neurons: the medial and lateral antennal lobe tracts (m-ALT and l-ALT). Despite substantial work on this dual pathway, its exact function is yet unclear. Here, we ask how attributes of odor quality and odor quantity are represented in the projection neurons (PNs) of the two pathways. Using in vivo calcium imaging, we compared the responses of m-ALT and l-ALT PNs of the honey bee Apis mellifera to a panel of 16 aliphatic odorants, and to three chosen odorants at eight concentrations. The results show that each pathway conveys differential information about odorants’ chemical features or concentration to higher order centers. While the l-ALT primarily conveys information about odorants’ chain length, the m-ALT informs about odorants’ functional group. Furthermore, each tract can only predict chemical distances or bees’ behavioral responses for odorants that differ according to its main feature, chain length or functional group. Generally l-ALT neurons displayed more graded dose–response relationships than m-ALT neurons, with a correspondingly smoother progression of inter-odor distances with increasing concentration. Comparison of these results with previous data recorded at AL input reveals differential processing by local networks within the two pathways. These results support the existence of parallel processing of odorant features in the insect brain. [ABSTRACT FROM AUTHOR]

Pheromones are chemical substances released into the environment by an individual, which trigger stereotyped behaviors and/or physiological processes in individuals of the same species. Yet, a novel hypothesis has suggested that pheromones not only elicit innate responses but also contribute to behavioral plasticity by affecting the subjective evaluation of appetitive or aversive stimuli. To test this hypothesis, we exposed bees to three pheromonal components whose valence was either negative (i.e., associated with aversive events: isopentyl acetate and 2-heptanone) or positive (i.e., associated with appetitive events: geraniol). We then determined the effect of this exposure on the subjective evaluation of aversive stimuli by quantifying responsiveness to a series of increasing electric shock voltages before and after exposure. Two experiments were conducted varying the time-lapse between shock series (15 min in Experiment 1, and 24 h in Experiment 2). In Experiment 1, we observed a general decrease of shock responsiveness caused by fatigue, due to the short lapse of time between the two series of shocks. This decrease could only be counteracted by isopentyl acetate. The enhancing effect of isopentyl acetate on shock responsiveness was also found in Experiment 2. Conversely, geraniol decreased aversive responsiveness in this experiment; 2-heptanone did not affect aversive responsiveness in any experiment. Overall, our results demonstrate that certain pheromones modulate the salience of aversive stimuli according to their valence. In this way, they would affect the motivation to engage in aversive responses, thus acting as modulators of behavioral plasticity. [ABSTRACT FROM AUTHOR]

The honeybee olfactory system is a well-established model for understanding functional mechanisms of learning and memory. Olfactory stimuli are first processed in the antennal lobe, and then transferred to the mushroom body and lateral horn through dual pathways termed medial and lateral antennal lobe tracts (m-ALT and l-ALT). Recent studies reported that honeybees can perform elemental learning by associating an odour with a reward signal even after lesions in m-ALT or blocking the mushroom bodies. To test the hypothesis that the lateral pathway (l-ALT) is sufficient for elemental learning, we modelled local computation within glomeruli in antennal lobes with axons of projection neurons connecting to a decision neuron (LHN) in the lateral horn. We show that inhibitory spike-timing dependent plasticity (modelling non-associative plasticity by exposure to different stimuli) in the synapses from local neurons to projection neurons decorrelates the projection neurons’ outputs. The strength of the decorrelations is regulated by global inhibitory feedback within antennal lobes to the projection neurons. By additionally modelling octopaminergic modification of synaptic plasticity among local neurons in the antennal lobes and projection neurons to LHN connections, the model can discriminate and generalize olfactory stimuli. Although positive patterning can be accounted for by the l-ALT model, negative patterning requires further processing and mushroom body circuits. Thus, our model explains several–but not all–types of associative olfactory learning and generalization by a few neural layers of odour processing in the l-ALT. As an outcome of the combination between non-associative and associative learning, the modelling approach allows us to link changes in structural organization of honeybees' antennal lobes with their behavioural performances over the course of their life. [ABSTRACT FROM AUTHOR]

Honeybees (Apis mellifera) are insects living in colonies with a complex social organization. Their nest contains food stores in the form of honey and pollen, as well as the brood, the queen and the bees themselves. These resources have to be defended against a wide range of predators and parasites, a task that is performed by specialized workers, called guard bees. Guards tune their response to both the nature of the threat and the environmental conditions, in order to achieve an efficient trade-off between defence and loss of foraging workforce. By releasing alarm pheromones, they are able to recruit other bees to help them handle large predators. These chemicals trigger both rapid and longer-term changes in the behaviour of nearby bees, thus priming them for defence. Here, we review our current understanding on how this sequence of events is performed and regulated depending on a variety of factors that are both extrinsic and intrinsic to the colony. We present our current knowledge on the neural bases of honeybee aggression and highlight research avenues for future studies in this area. We present a brief overview of the techniques used to study honeybee aggression, and discuss how these could be used to gain further insights into the mechanisms of this behaviour. [ABSTRACT FROM AUTHOR]

The honeybee Apis mellifera is an established model for the study of visual orientation. Yet, research on this topic has focused on behavioral aspects and has neglected the investigation of the underlying neural architectures in the bee brain. In other insects, the anterior optic tubercle (AOTU), the lateral (LX) and the central complex (CX) are important brain regions for visuospatial performances. In the central brain of the honeybee, a prominent group of neurons connecting the AOTU with conspicuous microglomerular synaptic structures in the LX has been recently identified, but their neural organization and ultrastructure have not been investigated. Here we characterized these microglomerular structures by means of immunohistochemical and ultrastructural analyses, in order to evaluate neurotransmission and synaptic organization. Three-dimensional reconstructions of the pre-synaptic and post-synaptic microglomerular regions were performed based on confocal microscopy. Each presynaptic region appears as a large cup-shaped profile that embraces numerous postsynaptic profiles of GABAergic tangential neurons connecting the LX to the CX. We also identified serotonergic broad field neurons that probably provide modulatory input from the CX to the synaptic microglomeruli in the LX. Two distinct clusters of microglomerular structures were identified in the lateral bulb (LBU) and medial bulb (MBU) of the LX. Although the ultrastructure of both clusters is very similar, we found differences in the number of microglomeruli and in the volume of the pre-synaptic profiles of each cluster.We discuss the possible role of these microglomerular clusters in the visuospatial behavior of honeybees and propose research avenues for studying their neural plasticity and synaptic function. [ABSTRACT FROM AUTHOR]

The function of parallel neural processing is a fundamental problem in Neuroscience, as it is found across sensory modalities and evolutionary lineages, from insects to humans. Recently, parallel processing has attracted increased attention in the olfactory domain, with the demonstration in both insects and mammals that different populations of second-order neurons encode and/or process odorant information differently. Among insects, Hymenoptera present a striking olfactory system with a clear neural dichotomy from the periphery to higher-order centers, based on two main tracts of second-order (projection) neurons: the medial and lateral antennal lobe tracts (m-ALT and l-ALT). To unravel the functional role of these two pathways, we combined specific lesions of the m-ALT tract with behavioral experiments, using the classical conditioning of the proboscis extension response (PER conditioning). Lesioned and intact bees had to learn to associate an odorant (1-nonanol) with sucrose. Then the bees were subjected to a generalization procedure with a range of odorants differing in terms of their carbon chain length or functional group. We show that m-ALT lesion strongly affects acquisition of an odor-sucrose association. However, lesioned bees that still learned the association showed a normal gradient of decreasing generalization responses to increasingly dissimilar odorants. Generalization responses could be predicted to some extent by in vivo calcium imaging recordings of l-ALT neurons. The m-ALT pathway therefore seems necessary for normal classical olfactory conditioning performance. [ABSTRACT FROM AUTHOR]

Taste plays a crucial role in the life of honey bees as their survival depends on the collection and intake of nectar and pollen, and other natural products. Here we studied the tarsal taste of honey bees through a series of behavioral and electrophysiological analyses. We characterized responsiveness to various sweet, salty and bitter tastants delivered to gustatory sensilla of the fore tarsi. Behavioral experiments showed that stimulation of opposite fore tarsi with sucrose and bitter substances or water yielded different outcomes depending on the stimulation sequence. When sucrose was applied first, thereby eliciting proboscis extension, no bitter substance could induce proboscis retraction, thus suggesting that the primacy of sucrose stimulation induced a central excitatory state. When bitter substances or water were applied first, sucrose stimulation could still elicit proboscis extension but to a lower level, thus suggesting central inhibition based on contradictory gustatory input on opposite tarsi. Electrophysiological experiments showed that receptor cells in the gustatory sensilla of the tarsomeres are highly sensitive to saline solutions at low concentrations. No evidence for receptors responding specifically to sucrose or to bitter substances was found in these sensilla. Receptor cells in the gustatory sensilla of the claws are highly sensitive to sucrose. Although bees do not possess dedicated bitter-taste receptors in the tarsi, indirect bitter detection is possible because bitter tastes inhibit sucrose receptor cells of the claws when mixed with sucrose solution. By combining behavioral and electrophysiological approaches, these results provide the first integrative study on tarsal taste detection in the honey bee. [ABSTRACT FROM AUTHOR]

Within a honey bee colony, individuals performing different tasks exhibit different sensitivities to noxious stimuli. Noxious-stimulus sensitivity can be quantified in harnessed bees by measuring the sting extension response (SER) to a series of increasing voltages. Biogenic amines play a crucial role in the control of insect responsiveness. Whether or not these neurotransmitters affect the central control of aversive responsiveness, and more specifically of electric-shock responsiveness, remains unknown. Here we studied the involvement of the biogenic amines octopamine, dopamine and serotonin, and of the ecdysteroid 20-hydroxyecdisone in the central control of sting responsiveness to electric shocks. We injected pharmacological antagonists of these signaling pathways into the brain of harnessed bees and determined the effect of blocking these different forms of neurotransmission on shock responsiveness. We found that both octopamine and 20-hydroxyecdisone are dispensable for shock responsiveness while dopamine and serotonin act as down-regulators of sting responsiveness. As a consequence, antagonists of these two biogenic amines induce an increase in shock responsiveness to shocks of intermediate voltage; serotonin, can also increase non-specific responsiveness. We suggest that different classes of dopaminergic neurons exist in the bee brain and we define at least two categories: an instructive class mediating aversive labeling of conditioned stimuli in associative learning, and a global gain-control class which down-regulates responsiveness upon perception of noxious stimuli. Serotonergic signaling together with down-regulating dopaminergic signaling may play an essential role in attentional processes by suppressing responses to irrelevant, non-predictive stimuli, thereby allowing efficient behavioral performances. [ABSTRACT FROM AUTHOR]

A dopaminergic wanting system drives foraging in honey bees. A new study shows that encounters with the Asian hornet, a fierce bee predator, decrease brain dopamine levels and thus foraging. Stop signals, used to terminate the waggle dances of receivers, have the same effect, showing the power of bee communication. [ABSTRACT FROM AUTHOR]

We studied the involvement of the α8 subunit of nicotinic acetylcholine receptors (nAChRs) in olfactory learning and memory in Apis mellifera. We have previously shown, by injecting different nicotinic antagonists into the bee brain, that pharmacologically different subtypes of nAChRs are important for honeybee memory -α-bungarotoxin-sensitive receptors are necessary for memory consolidation and mecamylamine-sensitive receptors are involved in retrieval processes. Here, we took advantage of the honeybee genome sequencing and the development of a small interfering RNA (siRNA) tool to focus on the role of the α8 subunit, which has been shown to be expressed in brain areas important for olfactory learning, such as the antennal lobes and mushroom bodies. We first demonstrated the efficacy of the siRNA tool by showing a decrease of the α8 protein level at 6 h after brain injection of α8 siRNA. We then tested the general role of this subunit in olfactory conditioning, using brain systemic or localized siRNA injections in the antennal lobes or the calyces and vertical lobes of the mushroom bodies. These injections were performed at either 6 h before the learning acquisition or 6 h before the memory test. The most prominent result was that 6-h pre-test injection of siRNA in the mushroom body vertical lobes impaired memory retrieval at 24 and 48 h post-training. This indicated the importance of cholinergic extrinsic neurons and nAChRs containing the α8 subunit for this process. [ABSTRACT FROM AUTHOR]

Sensory systems use parallel processing to extract and process different features of environmental stimuli. Parallel processing has been studied in the auditory, visual, and somatosensory systems, but equivalent research in the olfactory modality is scarce. The honeybee Apis melliferais an interesting model for such research as its relatively simple brain contains a dual olfactory system, with a clear neural dichotomy from the periphery to higher-order centers, based on two main neuronal tracts [medial (m) and lateral (l) antenno-protocerebral tract (APT)]. The function of this dual system is as yet unknown, and attributes like odor quality and odor quantity might be separately encoded in these subsystems. We have thus studied olfactory coding at the input of both subsystems, using in vivo calcium imaging. As one of the subsystems (m-APT) has never been imaged before, a novel imaging preparation was developed to this end, and responses to a panel of aliphatic odorants at different concentrations were compared in both subsystems. Our data show a global redundancy of olfactory coding at the input of both subsystems but unravel some specificities for encoding chemical group and carbon chain length of odor molecules. [ABSTRACT FROM AUTHOR]

Visual performances of honeybees have been extensively studied using free-flying individuals trained to choose visual stimuli paired with sucrose reward. By contrast, harnessed bees in the laboratory were not thought to be capable of learning a Pavlovian association between a visual stimulus (CS) and sucrose reward (US). For reasons as yet unknown, harnessed bees only learn visual cues in association with sucrose if their antennae are ablated. However, slow acquisition and low retention performances are obtained in this case. Here, we established a novel visual conditioning protocol, which allows studying visual learning and memory in intact harnessed bees in the laboratory. This protocol consists of conditioning the sting extension reflex (SEA) by pairing a visual stimulus (CS+) with an electric shock punishment (US), and a different visual stimulus (CS-) with the absence of shock. Bees with intact antennae learned the discrimination between CS+ and CS- by using chromatic cues, achromatic cues or both. Antennae ablation was not only unnecessary for learning to occur but it even impaired visual SEA conditioning because of a concomitant reduction of responsiveness to the electric shock. We thus established the first visual conditioning protocol on harnessed honeybees that does not require injuring the experimental subjects. This novel experimental approach opens new doors for accessing the neural correlates of visual learning and memory in honeybees. [ABSTRACT FROM AUTHOR]

The honeybee Apis mellifera represents a valuable model for studying the neural segregation and integration of visual information. Vision in honeybees has been extensively studied at the behavioral level and, to a lesser degree, at the physiological level using intracellular electrophysiological recordings of single neurons. However, our knowledge of visual processing in honeybees is still limited by the lack of functional studies of visual processing at the circuit level. Here we contribute to filling this gap by providing a neuroanatomical and neurophysiological characterization at the circuit level of a practically unstudied visual area of the bee brain, the anterior optic tubercle (AOTu). First, we analyzed the internal organization and neuronal connections of the AOTu. Second, we established a novel protocol for performing optophysiological recordings of visual circuit activity in the honeybee brain and studied the responses of AOTu interneurons during stimulation of distinct eye regions. Our neuroanatomical data show an intricate compartmentalization and connectivity of the AOTu, revealing a dorsoventral segregation of the visual input to the AOTu. Light stimuli presented in different parts of the visual field (dorsal, lateral, or ventral) induce distinct patterns of activation in AOTu output interneurons, retaining to some extent the dorsoventral input segregation revealed by our neuroanatomical data. In particular, activity patterns evoked by dorsal and ventral eye stimulation are clearly segregated into distinct AOTu subunits. Our results therefore suggest an involvement of the AOTu in the processing of dorsoventrally segregated visual information in the honeybee brain. [ABSTRACT FROM AUTHOR]

Background: Deterrent substances produced by plants are relevant due to their potential toxicity. The fact that most of these substances have an unpalatable taste for humans and other mammals contrasts with the fact that honeybees do not reject them in the range of concentrations in which these compounds are present in flower nectars. Here we asked whether honeybees detect and ingest deterrent substances and whether these substances are really toxic to them. Results: We show that pairing aversive substances with an odor retards learning of this odor when it is subsequently paired with sucrose. Harnessed honeybees in the laboratory ingest without reluctance a considerable volume (20 μl) of various aversive substances, even if some of them induce significant post-ingestional mortality. These substances do not seem, therefore, to be unpalatable to harnessed bees but induce a malaise-like state that in some cases results in death. Consistently with this finding, bees learning that one odor is associated with sugar, and experiencing in a subsequent phase that the sugar was paired with 20 μl of an aversive substance (devaluation phase), respond less than control bees to the odor and the sugar. Such stimulus devaluation can be accounted for by the malaise-like state induced by the aversive substances. Conclusion: Our results indicate that substances that taste bitter to humans as well as concentrated saline solutions base their aversive effect on the physiological consequences that their ingestion generates in harnessed bees rather than on an unpalatable taste. This conclusion is only valid for harnessed bees in the laboratory as freely-moving bees might react differently to aversive compounds could actively reject aversive substances. Our results open a new possibility to study conditioned taste aversion based on post-ingestional malaise and thus broaden the spectrum of aversive learning protocols available in honeybees. [ABSTRACT FROM AUTHOR]

Background: Learning and perception of visual stimuli by free-flying honeybees has been shown to vary dramatically depending on the way insects are trained. Fine color discrimination is achieved when both a target and a distractor are present during training (differential conditioning), whilst if the same target is learnt in isolation (absolute conditioning), discrimination is coarse and limited to perceptually dissimilar alternatives. Another way to potentially enhance discrimination is to increase the penalty associated with the distractor. Here we studied whether coupling the distractor with a highly concentrated quinine solution improves color discrimination of both similar and dissimilar colors by free-flying honeybees. As we assumed that quinine acts as an aversive stimulus, we analyzed whether aversion, if any, is based on an aversive sensory input at the gustatory level or on a post-ingestional malaise following quinine feeding. Methodology/Principal Findings: We show that the presence of a highly concentrated quinine solution (60 mM) acts as an aversive reinforcer promoting rejection of the target associated with it, and improving discrimination of perceptually similar stimuli but not of dissimilar stimuli. Free-flying bees did not use remote cues to detect the presence of quinine solution; the aversive effect exerted by this substance was mediated via a gustatory input, i.e. via a distasteful sensory experience, rather than via a post-ingestional malaise. Conclusion: The present study supports the hypothesis that aversion conditioning is important for understanding how and what animals perceive and learn. By using this form of conditioning coupled with appetitive conditioning in the framework of a differential conditioning procedure, it is possible to uncover discrimination capabilities that may remain otherwise unsuspected. We show, therefore, that visual discrimination is not an absolute phenomenon but can be modulated by experience. [ABSTRACT FROM AUTHOR]

In Pavlovian conditioning, an originally neutral stimulus (conditioned stimulus or CS) gains control over an animal's reflex after its association with a biologically relevant stimulus (unconditioned stimulus or US). As a consequence, a conditioned response is emitted by the animal upon further CS presentations. In such a situation, the subject exhibits a reflex response, so that whether the CS thereby acquires a positive or a negative value for the animal is difficult to assess. In honeybees, Apis mellifera, an odour (CS) can be associated either with sucrose solution (US) in the appetitive conditioning of the proboscis extension reflex (PER), or with an electric shock (US) in the aversive conditioning of the sting extension reflex (SER). The term 'aversive' may not apply to the latter as bees do not suppress SER as a consequence of learning but, on the contrary, start emitting SER to the CS. To determine whether the CS acquires a positive or a negative value in these conditioning forms, we compared the orientation behaviour of freely walking honeybees in an olfactory-cued V-maze after training them with an odour-sucrose association (PER conditioning) or an odour-shock association (SER conditioning). We show that the same odours can acquire either a positive value when associated to sucrose, or a negative value when associated to an electric shock, as bees respectively approach or avoid the CS in the V-maze. Importantly, these results clearly establish the aversive nature of SER conditioning in honeybees. [ABSTRACT FROM AUTHOR]

Abstract: In insects, γ-aminobutyric acid (GABA) and glutamate mediate fast inhibitory neurotransmission through ligand-gated chloride channel receptors. Both GABA and glutamate have been identified in the olfactory circuit of the honeybee. Here we investigated the role of inhibitory transmission mediated by GABA and glutamate-gated chloride channels (GluCls) in olfactory learning and memory in honeybees. We combined olfactory conditioning with injection of ivermectin, an agonist of GluCl receptors. We also injected a blocker of glutamate transporters (l-trans-PDC) or a GABA analog (TACA). We measured acquisition and retention 1, 24 and 48h after the last acquisition trial. A low dose of ivermectin (0.01ng/bee) impaired long-term olfactory memory (48h) while a higher dose (0.05ng/bee) had no effect. Double injections of ivermectin and l-trans-PDC or TACA had different effects on memory retention, depending on the doses and agents combined. When the low dose of ivermectin was injected after Ringer, long-term memory was again impaired (48h). Such an effect was rescued by injection of both TACA and l-trans-PDC. A combination of the higher dose of ivermectin and TACA decreased retention at 48h. We interpret these results as reflecting the involvement of both GluCl and GABA receptors in the impairment of olfactory long-term memory induced by ivermectin. These results illustrate the diversity of inhibitory transmission and its implication in long-term olfactory memory in honeybees. [Copyright &y& Elsevier]

Although the forelegs of honeybees are one of their main gustatory appendages, tarsal gustation in bees has never been systematically studied. To provide a more extensive account on honeybee tarsal gustation, we performed a series of behavioral experiments aimed at characterizing (1) tarsal sucrose sensitivity under different experimental conditions and (2) the capacity of tarsal sucrose stimulation to support olfactory conditioning. We quantified the proboscis extension reflex to tarsal sucrose stimulation and to odors paired with tarsal sucrose stimulation, respectively. Our experiments show that tarsal sucrose sensitivity is lower than antennal sucrose sensitivity and can be increased by starvation time. In contrast, antennae amputation decreases tarsal sucrose sensitivity. Furthermore, we show that tarsal sucrose stimulation can support olfactory learning and memory even if the acquisition level reached is relatively low (40%). [ABSTRACT FROM AUTHOR]

Generalization occurs when a conditioned response formed to one stimulus is also elicited by other stimuli which have not been used in the course of conditioning. Here, we studied color generalization in honeybees Apis mellifera trained to two rewarded colors, S1+ and S2+. After training, bees were tested with non-rewarded novel stimuli, which lay between the trained stimuli in a honeybee color space (Int) or outside the range defined by the trained stimuli ( E 1 and E 2). We analyzed whether bees interpolated their choice to Int and/or extrapolated it to E 1 and E 2. We compared the performances of the group trained with S1+ and S2+ to those of control groups trained only with S1+ or S2+. Bees trained with S1+ and S2+ responded similarly and highly to all test stimuli. These results do not allow discerning between generalization models based on the presence of interpolation and/or extrapolation. Nevertheless, bee’s performance was consistent with a linear summation of the two generalization gradients generated by S1+ and S2+, respectively. These gradients were asymmetric because control bees responded to the test stimuli as if these belonged to different similarity classes in spite of the fact that they had similar perceptual distances separating them. Stimuli treated as similar were located in the same half of the color spaces, whereas stimuli treated as different were located in opposite halves. Our results suggest that color categories could exist in honeybees and may underlie the performance of the control groups. Under this assumption, color categories would be also present in simpler nervous systems, and would not require factors such as language to be expressed. [ABSTRACT FROM AUTHOR]

Equipped with a mini brain smaller than one cubic millimeter and containing only 950,000 neurons, honeybees could be indeed considered as having rather limited cognitive abilities. However, bees display a rich and interesting behavioral repertoire, in which learning and memory play a fundamental role in the framework of foraging activities. We focus on the question of whether adaptive behavior in honeybees exceeds simple forms of learning and whether the neural mechanisms of complex learning can be unraveled by studying the honeybee brain. Besides elemental forms of learning, in which bees learn specific and univocal links between events in their environment, bees also master different forms of non-elemental learning, including categorization, contextual learning and rule abstraction, both in the visual and in the olfactory domain. Different protocols allow accessing the neural substrates of some of these learning forms and understanding how complex problem solving can be achieved by a relatively simple neural architecture. These results underline the enormous richness of experience-dependent behavior in honeybees, its high flexibility, and the fact that it is possible to formalize and characterize in controlled laboratory protocols basic and higher-order cognitive processing using an insect as a model. [ABSTRACT FROM AUTHOR]

We focus on non-elemental forms of learning in honeybees in order to answer the question of whether retrospective learning can be found in an insect. We analyze three different forms of learning: category learning, rule learning and backward blocking. We provide examples showing that honeybees demonstrate these three forms of learning and propose that causal retrospection underlies them to different extents. We argue that an elemental associative account explains category learning whereas rule learning may require retrospection. Backward blocking, on the other hand, admits interpretations based on prospective learning. Consequently, because animals, including honeybees, solve these three types of problems, distinguishing between species on the basis of these capacities is inappropriate. [ABSTRACT FROM AUTHOR]

Natural olfactory stimuli occur as mixtures of many single odors. We studied whether the representation of a mixture in the brain retains single-odor information and how much mixture-specific information it includes. To understand mixture representation in the honeybee brain, we used in vivo calcium imaging at the level of the antennal lobe, and systematically measured odor-evoked activity in 24 identified glomeruli in response to four single odorants and all their possible binary, ternary and quaternary mixtures. Qualitatively, mixture-induced activity patterns always contained glomeruli belonging to the pattern of at least one of the components, suggesting a high conservation of component information in olfactory mixtures. Quantitatively, glomerular activity saturated quickly and increasing the number of components resulted in an increase of cases in which the response of a glomerulus to the mixture was lower than that to the strongest component (‘suppression’). This shows global inhibition in the antennal lobe, probably acting as overall gain control. Single components were not equally salient (in terms of number of active glomeruli) and mixture activity patterns were always more similar to the more salient components, in a way that could be predicted linearly. Thus, although a gain control system in the honeybee antennal lobe prevents saturation of the olfactory system, mixture representation follows essentially elemental rules. [ABSTRACT FROM AUTHOR]

We combined behavioural and electrophysiological experiments to study whether bitter taste is perceived at the antennal level in honeybees, Apis mellifera. Our behavioural studies showed that neither quinine nor salicin delivered at one antenna at different concentrations induced a retraction of the proboscis once it was extended in response to 1 m sucrose solution delivered to the opposite antenna. Bees that extended massively their proboscis to 1 m sucrose responded only partially when stimulated with a mixture of 1 m sucrose and 100 m m quinine. The mixture of 1 m sucrose and 100 m m salicin had no such suppressive effect. No behavioural suppression was found for mixtures of salt solution and either bitter substance. Electrophysiological recordings of taste sensillae at the antennal tip revealed sensillae that responded specifically either to sucrose or salt solutions, but none responded to the bitter substances quinine and salicin at the different concentrations tested. The electrophysiological responses of sensillae to 15 m m sucrose solution were inhibited by a mixture of 15 m m sucrose and 0.1 m m quinine, but not by a mixture of 15 m m sucrose and 0.1 m m salicin. The responses of sensillae to 50 m m NaCl were reduced by a mixture of 50 m m NaCl and 1 m m quinine but not by a mixture of 50 m m NaCl and 1 m m salicin. We concluded that no receptor cells for the bitter substances tested, exist at the level of the antennal tip of the honeybee and that antennal bitter taste is not represented as a separate perceptual quality. [ABSTRACT FROM AUTHOR]

The question of whether or not neural activity patterns recorded in the olfactory centres of the brain correspond to olfactory perceptual measures remains unanswered. To address this question, we studied olfaction in honeybees Apis mellifera using the olfactory conditioning of the proboscis extension response. We conditioned bees to odours and tested generalisation responses to different odours. Sixteen odours were used, which varied both in their functional group (primary and secondary alcohols, aldehydes and ketones) and in their carbon-chain length (from six to nine carbons). The results obtained by presentation of a total of 16 × 16 odour pairs show that (i) all odorants presented could be learned, although acquisition was lower for short-chain ketones; (ii) generalisation varied depending both on the functional group and the carbon-chain length of odours trained; higher generalisation was found between longchain than between short-chain molecules and between groups such as primary and secondary alcohols; (iii) for some odour pairs, cross-generalisation between odorants was asymmetric; (iv) a putative olfactory space could be defined for the honeybee with functional group and carbon-chain length as inner dimensions; (v) perceptual distances in such a space correlate well with physiological distances determined from optophysiological recordings of antennal lobe activity. We conclude that functional group and carbon-chain length are inner dimensions of the honeybee olfactory space and that neural activity in the antennal lobe reflects the perceptual quality of odours. [ABSTRACT FROM AUTHOR]

The mushroom bodies (MBs) are central structures in the insect brain that have been associated with olfactory learning and memory. Here we used hydroxyurea (HU) to treat honeybee larvae and induce partial MB ablations at the adult stage. We studied olfactory learning in honeybees with unilateral loss of the median calyces of their MBs and compared their ability to solve different forms of olfactory discrimination. When odorants were delivered in a side-specific manner, ablated bees could not solve either discrimination of the unambiguous problem (Paradigm 1: A+, B– on one antenna, C+, D– on the other; A+B–/C+D–) whereas they could solve at least one of both discriminations of the ambiguous problem (Paradigm 2: A+B–/A–B+), namely that proposed to their intact brain side. Non-ablated bees could learn side-specific discriminations on both brain sides. When odorants were delivered simultaneously to both antennae (Paradigm 3: A+B–C+D–), HU-ablated bees learned slower than HU-normal bees. Thus, in all three paradigms, the unilateral loss of a median calyx affected olfactory learning. We propose that the MBs are required for solving elemental olfactory tasks whose complexity is increased by the number of stimuli involved and that MB ablations could have an effect on the inhibition of information exchange between brain hemispheres. [ABSTRACT FROM AUTHOR]

Generalization is a cognitive ability that allows similar stimuli along a given dimension to be treated as equivalents. Insects exhibit high levels of visual generalization. Honeybees trained to recognize complex visual stimuli on the basis of a single feature generalize their choice to novel stimuli sharing that common feature with the trained stimuli. The demonstration of this kind of performance has been limited to the use of a single visual feature, and the possibility that bees link different features in learning a visual pattern has been denied. Here we show that honeybees trained with a series of complex patterns sharing a common layout comprising four edge orientations remember these orientations simultaneously in their appropriate positions, and generalize their response to novel stimuli that preserve the trained layout. Honeybees also generalize their response to patterns with fewer correct orientations, depending on their match with the trained layout. Stimulation of the achromatic L-photoreceptor input is necessary for this task. The mini-brain of the honeybee can thus extract regularities in its environment and establish correspondences among correlated features. It can thus generate a large set of object descriptions from a finite set of elements. [ABSTRACT FROM AUTHOR]

The brain of a honeybee contains only 960 000 neurons and its volume represents only 1 mm3. However, it supports impressive behavioral capabilities. Honeybees are equipped with sophisticated sensory systems and have well developed learning and memory capacities, whose essential mechanisms do not differ drastically from those of vertebrates. Here, I focus on non-elemental forms of learning by honeybees. I show that bees exhibit learning abilities that have been traditionally ascribed to a restricted portion of vertebrates, as they go beyond simple stimulus–stimulus or response–stimulus associations. To relate these abilities to neural structures and functioning in the bee brain we focus on the antennal lobes and the mushroom bodies. We conclude that there is a fair chance to understand complex behavior in bees, and to identify the potential neural substrates underlying such behavior by adopting a cognitive neuroethological approach. In such an approach, behavioral and neurobiological studies are combined to understand the rules and mechanisms of plastic behavior in a natural context. [Copyright &y& Elsevier]

Floral shape is a visual cue used by pollinators to discriminate between competing flower species. We investigated whether discrimination is possible between closed shapes presenting the same colour and lacking a centrally presented fixation point. Free-flying honeybees, Apis mellifera L., had to discriminate between a solid square and a solid triangle of the same colour presented on the back walls of a Y-maze. Different colours were used to vary chromatic contrast and receptor-specific contrasts. Discrimination was possible whenever shapes presented contrast to the long wavelength receptor but was independent of chromatic contrast, overall intensity contrast or short and middle wavelength receptor contrast. We suggest that the bees used the edges of the closed shapes to solve the task. Bees failed when shapes were rotated, showing that a single shape edge was not sufficient for recognition. Copyright 2003 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved. [Copyright &y& Elsevier]

We addressed the question of whether the amount of individual experience determines the use of elemental or configural visual discrimination strategies in free-flying honeybees Apis mellifera. We trained bees to fly into a Y-maze to collect sucrose solution on a rewarded stimulus presented in one of the arms of the maze. Stimuli were colour disks, violet (V), green (G) or yellow (Y), which were of equal psychophysical salience for honeybees. Training followed an A+, BC+ design, followed by an AC versus BC test. Training consisted of 6 (3 A+ and 3 BC+), 20 (10 A+ and 10 BC+) or 40 (20 A+ and 20 BC+) acquisition trials. Elemental models of compound processing predict a preference for the non-trained stimulus AC while configural models predict a preference for the trained stimulus BC. Our results show that increasing the number of acquisition trials results in a change of the internal representation of stimuli. After six training trials, bees favoured an elemental strategy and preferred AC to BC during the tests. Generally, increasing the number of training trials resulted in an increase of the choice of BC. Thus, short training favoured processing of the compound as the sum of its elements (elemental account) while long training favoured its processing as being different from the sum of its elements (configural account). Additionally, we observed that the change in stimulus processing was also influenced by stimulus similarity. Colour perceptual similarity favoured configural processing with increasing experience. [Copyright &y& Elsevier]

We asked whether the detection range of two-coloured centre-surround patterns differs from that of single-coloured targets. Honeybees Apis mellifera were trained to distinguish between the presence and absence of a single-coloured disc or a coloured pattern at different visual angles. The patterns presented colours which were either different in chromatic and L-receptor contrasts to the background, equal in chromatic but different in L-receptor contrasts, or vice-versa. Patterns with colours presenting only chromatic contrast were also tested. Patterns with higher L-receptor contrast in its outer than in its inner element were better detected than patterns with a reversed L-contrast distribution. However, both were detected worse than single-coloured discs of the respective colours. When the L-receptor contrast was the same for both elements, the detection range of the two-coloured and single-coloured targets was the same. Patterns whose colours lacked L-receptor contrast were detected just as single-coloured targets of the same colours. These results demonstrate that both chromatic and L-receptor contrasts mediate the detection of coloured patterns and that particular distributions of L-receptor contrast within a target are better detected than others. This finding is consistent with the intervention of neurons with centre-surround receptive fields in the detection of coloured patterns. [ABSTRACT FROM AUTHOR]

Odour processing exhibits multiple parallels between vertebrate and invertebrate olfactory systems. Insects, in particular, have emerged as relevant models for olfactory studies because of the tractability of their olfactory circuits. Here, we used fast calcium imaging to track the activity of projection neurons in the honey bee antennal lobe (AL) during olfactory stimulation at high temporal resolution. We observed a heterogeneity of response profiles and an abundance of inhibitory activities, resulting in various response latencies and stimulus-specific post-odour neural signatures. Recorded calcium signals were fed to a mushroom body (MB) model constructed implementing the fundamental features of connectivity between olfactory projection neurons, Kenyon cells (KC), and MB output neurons (MBON). The model accounts for the increase of odorant discrimination in the MB compared to the AL and reveals the recruitment of two distinct KC populations that represent odorants and their aftersmell as two separate but temporally coherent neural objects. Finally, we showed that the learning-induced modulation of KC-to-MBON synapses can explain both the variations in associative learning scores across different conditioning protocols used in bees and the bees' response latency. Thus, it provides a simple explanation of how the time contingency between the stimulus and the reward can be encoded without the need for time tracking. This study broadens our understanding of olfactory coding and learning in honey bees. It demonstrates that a model based on simple MB connectivity rules and fed with real physiological data can explain fundamental aspects of odour processing and associative learning. [ABSTRACT FROM AUTHOR]

Since their discovery in insects, pheromones are considered as ubiquitous and stereotyped chemical messengers acting in intraspecific animal communication. Here we studied the effect of pheromones in a different context as we investigated their capacity to induce persistent modulations of associative learning and memory. We used honey bees, Apis mellifera, and combined olfactory conditioning and pheromone preexposure with disruption of neural activity and two-photon imaging of olfactory brain circuits, to characterize the effect of pheromones on olfactory learning and memory. Geraniol, an attractive pheromone component, and 2-heptanone, an aversive pheromone, improved and impaired, respectively, olfactory learning and memory via a durable modulation of appetitive motivation, which left odor processing unaffected. Consistently, interfering with aminergic circuits mediating appetitive motivation rescued or diminished the cognitive effects induced by pheromone components. We thus show that these chemical messengers act as important modulators of motivational processes and influence thereby animal cognition. David Baracchi et al. show that honey bees exposed to geraniol, a component of an attractant pheromone, exhibit improved olfactory learning and memory while the opposite effect was seen in honey bees exposed to the aversive pheromone, 2- heptanone. These changes occurred through a modulation of appetitive motivation without affecting odor processing, suggesting an important role for pheromones as modulators of motivational and learning processes. [ABSTRACT FROM AUTHOR]

The question of how animals process stimulus mixtures remains controversial as opposing views propose that mixtures are processed analytically, as the sum of their elements, or holistically, as unique entities different from their elements. Overshadowing is a widespread phenomenon that can help decide between these alternatives. In overshadowing, an individual trained with a binary mixture learns one element better at the expense of the other. Although element salience (learning success) has been suggested as a main explanation for overshadowing, the mechanisms underlying this phenomenon remain unclear. We studied olfactory overshadowing in honeybees to uncover the mechanisms underlying olfactory-mixture processing. We provide, to our knowledge, the most comprehensive dataset on overshadowing to date based on 90 experimental groups involving more than 2700 bees trained either with six odourants or with their resulting 15 binary mixtures. We found that bees process olfactory mixtures analytically and that salience alone cannot predict overshadowing. After normalizing learning success, we found that an unexpected feature, the generalization profile of an odourant, was determinant for overshadowing. Odourants that induced less generalization enhanced their distinctiveness and became dominant in the mixture. Our study thus uncovers features that determine odourant dominance within olfactory mixtures and allows the referring of this phenomenon to differences in neural activity both at the receptor and the central level in the insect nervous system. [ABSTRACT FROM AUTHOR]

Traditional models of insect vision have assumed that insects are only capable of low-level analysis of local cues and are incapable of global, holistic perception. However, recent studies on honeybee (Apis mellifera) vision have refuted this view by showing that this insect also processes complex visual information by using spatial configurations or relational rules. In the light of these findings, we asked whether bees prioritize global configurations or local cues by setting these two levels of image analysis in competition. We trained individual free-flying honeybees to discriminate hierarchical visual stimuli within a Y-maze and tested bees with novel stimuli in which local and/or global cues were manipulated. We demonstrate that even when local information is accessible, bees prefer global information, thus relying mainly on the object's spatial configuration rather than on elemental, local information. This preference can be reversed if bees are pre-trained to discriminate isolated local cues. In this case, bees prefer the hierarchical stimuli with the local elements previously primed even if they build an incorrect global configuration. Pre-training with local cues induces a generic attentional bias towards any local elements as local information is prioritized in the test, even if the local cues used in the test are different from the pre-trained ones. Our results thus underline the plasticity of visual processing in insects and provide new insights for the comparative analysis of visual recognition in humans and animals. [ABSTRACT FROM AUTHOR]

Huang et al. make an exciting claim about a human-like dopamine-regulated neuromodulatory mechanism underlying food-seeking behavior in honey bees. Comment on "Food wanting is mediated by transient activation of dopaminergic signaling in the honey bee brain" Andrew Barron et al. Full text: dx.doi.org/10.1126/science.adg3916 Response to Comment on "Food wanting is mediated by transient activation of dopaminergic signaling in the honey bee brain" Songkun Su and Martin Giurfa Barron et al. criticize the work of Huang et al., putting the accent on the quantification of dopamine levels via high-performance liquid chromatography, yet also including data interpretation through alternative hypotheses aimed at invalidating the original ones proposed by Huang et al. [Extracted from the article]

Concepts act as a cornerstone of human cognition. Humans and non-human primates learn conceptual relationships such as 'same', 'different', 'larger than', 'better than', among others. In all cases, the relationships have to be encoded by the brain independently of the physical nature of objects linked by the relation. Consequently, concepts are associated with high levels of cognitive sophistication and are not expected in an insect brain. Yet, various works have shown that the miniature brain of honeybees rapidly learns conceptual relationships involving visual stimuli. Concepts such as 'same', 'different', 'above/below of' or 'left/right are well mastered by bees. We review here evidence about concept learning in honeybees and discuss both its potential adaptive advantage and its possible neural substrates. The results reviewed here challenge the traditional view attributing supremacy to larger brains when it comes to the elaboration of concepts and have wide implications for understanding how brains can form conceptual relations. [ABSTRACT FROM AUTHOR]

The biological bases of wanting have been characterized in mammals, but whether an equivalent wanting system exists in insects remains unknown. In this study, we focused on honey bees, which perform intensive foraging activities to satisfy colony needs, and sought to determine whether foragers leave the hive driven by specific expectations about reward and whether they recollect these expectations during their waggle dances. We monitored foraging and dance behavior and simultaneously quantified and interfered with biogenic amine signaling in the bee brain. We show that a dopamine-dependent wanting system is activated transiently in the bee brain by increased appetite and individual recollection of profitable food sources, both en route to the goal and during waggle dances. Our results show that insects share with mammals common neural mechanisms for encoding wanting of stimuli with positive hedonic value. [ABSTRACT FROM AUTHOR]

Abstract: In the honeybee Apis mellifera, a sting pheromone produced by sting glands plays an important role in coordinating defensive behavior. This pheromone is a blend constituted by several components. Little is known about the neural substrates underlying sting pheromone processing in the bee brain. Here, we investigated the neural activity elicited by eight components (five acetates and three alcohols) of the sting pheromone, and by real bee stings at the level of the antennal lobe (AL) of worker honeybees. We used in vivo calcium imaging to record odor-induced neural activity of 22 identified glomeruli in the AL. We found that acetates mainly activated medial glomeruli while alcohols mainly activated lateral dorsal glomeruli. The sting preparation evoked a glomerular pattern that was clearly distinct from those of individual pheromone components. No particular region of the imaged AL was found to process sting pheromone or any of its components. Further analyses in a putative honeybee olfactory space showed that the neural activity elicited by sting preparation cannot be linearly predicted by those of pheromone components and that such components are not clearly separated from non-sting pheromone odors. We conclude that sting pheromone is processed in the worker honeybee AL following the same principles of general odors so that the chemical structure of odorants is the main determinant of glomerular activation, rather than their pheromonal values. We cannot exclude, however, that the distinctness of sting-pheromone representation with respect to that of its components constitutes a form of specialized neural processing strategy for this kind of substance. [Copyright &y& Elsevier]