Aurore Avarguès-Weber

Visual Cognition in Social Insects

Visual learning admits different levels of complexity, from the formation of a simple associative link between a visual stimulus and its outcome, to more sophisticated performances, such as object categorization or rules learning, that allow flexible responses beyond simple forms of learning. Not surprisingly, higher-order forms of visual learning have been studied primarily in vertebrates with larger brains, while simple visual learning has been the focus in animals with small brains such as insects. This dichotomy has recently changed as studies on visual learning in social insects have shown that these animals can master extremely sophisticated tasks. Here we review a spectrum of visual learning forms in social insects, from color and pattern learning, visual attention, and top-down image recognition, to interindividual recognition, conditional discrimination, category learning, and rule extraction. We analyze the necessity and sufficiency of simple associations to account for complex visual learning in Hymenoptera and discuss possible neural mechanisms underlying these visual performances.

Aversive Reinforcement Improves Visual Discrimination Learning in Free-Flying Honeybees

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.

Conceptualization of above and below relationships by an insect

Relational rules such as ‘same’ or ‘different’ are mastered by humans and non-human primates and are considered as abstract conceptual thinking as they require relational learning beyond perceptual generalization. Here, we investigated whether an insect, the honeybee (Apis mellifera), can form a conceptual representation of an above/below spatial relationship. In experiment 1, bees were trained with differential conditioning to choose a variable target located above or below a black bar that acted as constant referent throughout the experiment. In experiment 2, two visual stimuli were aligned vertically, one being the referent, which was kept constant throughout the experiment, and the other the target, which was variable. In both experiments, the distance between the target and the referent, and their location within the visual field was systematically varied. In both cases, bees succeeded in transferring the learned concept to novel stimuli, preserving the trained spatial relation, thus showing an ability to manipulate this relational concept independently of the physical nature of the stimuli. Absolute location of the referent into the visual field was not a low-level cue used by the bees to solve the task. The honeybee is thus capable of conceptual learning despite having a miniature brain, showing that such elaborated learning form is not a prerogative of vertebrates.

Configural processing enables discrimination and categorization of face-like stimuli in honeybees

SUMMARY We studied whether honeybees can distinguish face-like configurations by using standardized stimuli commonly employed in primate and human visual research. Furthermore, we studied whether, irrespective of their capacity to distinguish between face-like stimuli, bees learn to classify visual stimuli built up of the same elements in face-like versus non-face-like categories. We showed that bees succeeded in discriminating both face-like and non-face-like stimuli and categorized appropriately novel stimuli in these two classes. To this end, they used configural information and not just isolated features or low-level cues. Bees looked for a specific configuration in which each feature had to be located in an appropriate spatial relationship with respect to the others, thus showing sensitivity for first-order relationships between features. Although faces are biologically irrelevant stimuli for bees, the fact that they were able to integrate visual features into complex representations suggests that face-like stimulus categorization can occur even in the absence of brain regions specialized in face processing.

Conceptual learning by miniature brains

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.

Simultaneous mastering of two abstract concepts by the miniature brain of bees

Sorting objects and events into categories and concepts is a fundamental cognitive capacity that reduces the cost of learning every particular situation encountered in our daily lives. Relational concepts such as “same,” “different,” “better than,” or “larger than”—among others—are essential in human cognition because they allow highly efficient classifying of events irrespective of physical similarity. Mastering a relational concept involves encoding a relationship by the brain independently of the physical objects linked by the relation and is, therefore, consistent with abstraction capacities. Processing several concepts at a time presupposes an even higher level of cognitive sophistication that is not expected in an invertebrate. We found that the miniature brains of honey bees rapidly learn to master two abstract concepts simultaneously, one based on spatial relationships (above/below and right/left) and another based on the perception of difference. Bees that learned to classify visual targets by using this dual concept transferred their choices to unknown stimuli that offered a best match in terms of dual-concept availability: their components presented the appropriate spatial relationship and differed from one another. This study reveals a surprising facility of brains to extract abstract concepts from a set of complex pictures and to combine them in a rule for subsequent choices. This finding thus provides excellent opportunities for understanding how cognitive processing is achieved by relatively simple neural architectures.

Observational conditioning in flower choice copying by bumblebees (Bombus terrestris): influence of observer distance and demonstrator movement.

Background Bumblebees use information provided inadvertently by conspecifics when deciding between different flower foraging options. Such social learning might be explained by relatively simple associative learning mechanism: the bee may learn to associate conspecifics with nectar or pollen reward through previous experience of foraging jointly. However, in some studies, observers were guided by choices of ‘demonstrators’ viewed through a screen, so no reward was given to the observers at the time of seeing other bees’ flowers choice and no demonstrator bee was present at the moment of decision. This behaviour, referred to observational conditioning, implies an additional associative step as the positive value of conspecific is transferred to the associated flower. Here we explore the role of demonstrator movement, and the distance between observers and demonstrators that is required for observation conditioning to take place. Methodology/Principal Findings We identify the conditions under which observational conditioning occurs in the widespread European species Bombus terrestris. The presence of artificial demonstrator bees leads to a significant change in individual colour preference toward the indicated colour if demonstrators were moving and observation distance was limited (15 cm), suggesting that observational conditioning could only influence relatively short-range foraging decisions. In addition, the movement of demonstrators is a crucial factor for observational conditioning, either due to the more life-like appearance of moving artificial bees or an enhanced detectability of moving demonstrators, and an increased efficiency at directing attention to the indicated flower colour. Conclusion Bumblebees possess the capacity to learn the quality of a flower by distal observation of other foragers’ choices. This confirms that social learning in bees involves more advanced processes than simple associative learning, and indicates that observational conditioning might be widespread in pollinating insects, raising intriguing questions for the underlying mechanisms as well as the spread of social information in pollinator-plant interactions.

Learning context modulates aversive taste strength in honey bees

ABSTRACT The capacity of honey bees (Apis mellifera) to detect bitter substances is controversial because they ingest without reluctance different kinds of bitter solutions in the laboratory, whereas free-flying bees avoid them in visual discrimination tasks. Here, we asked whether the gustatory perception of bees changes with the behavioral context so that tastes that are less effective as negative reinforcements in a given context become more effective in a different context. We trained bees to discriminate an odorant paired with 1 mol l−1 sucrose solution from another odorant paired with either distilled water, 3 mol l−1 NaCl or 60 mmol l−1 quinine. Training was either Pavlovian [olfactory conditioning of the proboscis extension reflex (PER) in harnessed bees], or mainly operant (olfactory conditioning of free-walking bees in a Y-maze). PER-trained and maze-trained bees were subsequently tested both in their original context and in the alternative context. Whereas PER-trained bees transferred their choice to the Y-maze situation, Y-maze-trained bees did not respond with a PER to odors when subsequently harnessed. In both conditioning protocols, NaCl and distilled water were the strongest and the weakest aversive reinforcement, respectively. A significant variation was found for quinine, which had an intermediate aversive effect in PER conditioning but a more powerful effect in the Y-maze, similar to that of NaCl. These results thus show that the aversive strength of quinine varies with the learning context, and reveal the plasticity of the bees gustatory system. We discuss the experimental constraints of both learning contexts and focus on stress as a key modulator of taste in the honey bee. Further explorations of bee taste are proposed to understand the physiology of taste modulation in bees. Summary: Learning context is a key modulator of taste in the honey bee.

The forest or the trees: preference for global over local image processing is reversed by prior experience in honeybees

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 objects 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.

Conceptualization of relative size by honeybees.

The ability to process visual information using relational rules allows for decisions independent of the specific physical attributes of individual stimuli. Until recently, the manipulation of relational concepts was considered as a prerogative of large mammalian brains. Here we show that individual free flying honeybees can learn to use size relationship rules to choose either the larger or smaller stimulus as the correct solution in a given context, and subsequently apply the learnt rule to novel colors and shapes providing that there is sufficient input to the long wavelength (green) photoreceptor channel. Our results add a novel, size-based conceptual rule to the set of relational concepts that honeybees have been shown to master and underline the value of bees as an animal model for studying the emergence of conceptualization abilities.