Martin Giurfa

CNRS - Paul Sabatier University - Toulouse III · Research Center on Animal Cognition

Humans and non-human primates learn conceptual relationships such as ‘same’ and ‘different, which have to be encoded independently of the physical nature of objects linked by the relation. Consequently, concepts are associated with high-level cognition and are not expected in an insect brain. Yet, various works have shown that the miniature brain o...

The superiority of spaced over massed learning is an established fact in the formation of long-term memories (LTM). Here we addressed the cellular processes and the temporal demands of this phenomenon using a weak spatial object recognition (wSOR) training, which induces short-term memories (STM) but not LTM. We observed SOR-LTM promotion when two...

Intraspecific floral colour polymorphism is a common trait of food deceptive orchids, which lure pollinators with variable, attractive signals, without providing food resources. The variable signals are thought to hinder avoidance learning of deceptive flowers by pollinators. Here, we analysed the cognitive mechanisms underlying the choice of free-...

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 me...

The Argentine ant, Linepithema humile, is native from South America but has become one of the most invasive species in the world. These ants heavily rely on trail pheromones for foraging and previous studies have focused on this signal to develop a strategy of chemical control. Here, we studied the effect of pre-exposure to the trail pheromone on s...

Memory reconsolidation occurs when a retrieving event destabilizes transiently a consolidated memory, triggering thereby a new process of restabilization that ensures memory persistence. Although this phenomenon has received wide attention, the effect of new information cooccurring with the reconsolidation process has been less explored. Here we de...

Conditioned taste aversion (CTA) learning induces the devaluation of a preferred food through its pairing with a stimulus inducing internal illness. In invertebrates, it is still unclear how this aversive learning impairs the memories of stimuli that had been associated with the appetitive food prior to its devaluation. Here we studied this phenome...

Supporting information for Aguiar et al. (2020) A cognitive analysis of deceptive pollination: associative mechanisms underlying pollinators’ choices in non-rewarding colour polymorphic scenarios

Research on honeybee memory has led to a widely accepted model in which a single pairing of an odor stimulus with sucrose induces memories that are independent of protein synthesis but is unable to form protein-synthesis-dependent long-term memory (LTM). The latter is said to arise only after three or more pairings of odor and sucrose. Here, we sho...

Non-elemental learning constitutes a cognitive challenge because events to be learned are usually ambiguous in terms of reinforcement outcome, contrary to elemental learning, which relies on unambiguous associations. Negative patterning (NP) constitutes a paradigmatic case of non-elemental learning, as subjects have to learn that single elements ar...

Honeybees are a standard model for the study of appetitive learning and memory. Yet, fewer attempts have been performed to characterize aversive learning and memory in this insect and uncover its molecular underpinnings. Here, we took advantage of the positive phototactic behavior of bees kept away from the hive in a dark environment and establishe...

Recent studies revealed numerosity judgments in bees, which include the concept of zero, subtraction and addition, and matching symbols to numbers. Despite their distant origins, bees and vertebrates share similarities in their numeric competences, thus suggesting that numerosity is evolutionary conserved and can be implemented in miniature brains...

Various vertebrate species use relative numerosity judgements in comparative assessments of quantities for which they use larger/smaller relationships rather than absolute number. The numerical ability of honeybees shares basic properties with that of vertebrates but their use of absolute or relative numerosity has not been explored. We trained fre...

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 land...

Foraging exposes organisms to rewarding and aversive events, providing a selective advantage for maximizing the former while minimizing the latter. Honey bees (Apis mellifera) associate environmental stimuli with appetitive or aversive experiences, forming preferences for scents, locations, and visual cues. Preference formation is influenced by int...

The ecological and evolutionary success of social insects relies on their ability to efficiently discriminate between group members and aliens. Nestmate recognition occurs by phenotype matching, the comparison of the referent (colony) phenotype to the one of an encountered individual. Based on the level of dissimilarity between the two, the discrim...

Social insects commonly exhibit division of labor in non-reproductive tasks. Task allocation may be related to size, form, and ergonomic differences when workers are anatomically variable. Carpenter ants Camponotus mus collecting nectar exhibit a wide forager size variation, thus raising the question of whether large and minor workers differ in the...

Non-elemental learning constitutes a cognitive challenge because, contrary to elemental learning forms, it does not rely on simple associations, as events to be learned are usually ambiguous in terms of reinforcement outcome. Negative patterning constitutes a paradigmatic case of non-elemental learning, as subjects have to learn that single element...

Honeybees maintain their colony throughout the cold winters, a strategy that enables them to make the most of early spring flowers. During this period, their activity is mostly limited to thermoregulation, while foraging and brood rearing are stopped. Less is known about seasonal changes to the essential task of defending the colony against intrude...

To study visual learning in honey bees, we developed a virtual reality (VR) system in which tethered bees walk stationary on a treadmill while they experience visual stimuli with different outcomes projected onto a semi-circular screen placed in front of them. The bee movements translate into corresponding modifications of the visual panorama (clos...

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...

Many flowering plants present variable complex fragrances, which usually include different isomers of the same molecule. As fragrance is an essential cue for flower recognition by pollinators, we ask if honey bees discriminate between floral-fragrance isomers in an appetitive context. We used the olfactory conditioning of the proboscis extension re...

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 acces...

Lateralization is a fundamental property of the human brain that affects perceptual, motor, and cognitive processes. It is now acknowledged that left–right laterality is widespread across vertebrates and even some invertebrates such as fruit flies and bees. Honeybees, which learn to associate an odorant (the conditioned stimulus, CS) with sucrose s...

The defence of a society often requires that some specialized members coordinate to repel a threat at personal risk. This is especially true for honey bee guards, which defend the hive and may sacrifice their lives upon stinging. Central to this cooperative defensive response is the sting alarm pheromone, which has isoamyl acetate (IAA) as its main...

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 eval...

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,...

Taste perception allows discriminating edible from non-edible items and is crucial for survival. In the honey bee, the gustatory sense has remained largely unexplored, as tastants have been traditionally used as reinforcements rather than as stimuli to be learned and discriminated. Here we provide the first characterization of antennal gustatory pe...

Pheromones are chemical messengers that trigger stereotyped behaviors and/or physiological processes in individuals of the same species. Recent reports suggest that pheromones can modulate behaviors not directly related to the pheromonal message itself and contribute, in this way, to behavioral plasticity. We tested this hypothesis by studying the...

Free-flying honeybees exhibit remarkable cognitive capacities but the neural underpinnings of these capacities cannot be studied in flying insects. Conversely, immobilized bees are accessible to neurobiological investigation but display poor visual learning. To overcome this limitation, we aimed at establishing a controlled visual environment in wh...

Ants have recently emerged as useful models for the study of olfactory learning. In this framework, the development of a protocol for the appetitive conditioning of the maxilla-labium extension response (MaLER) provided the possibility of studying Pavlovian odor-food learning in a controlled environment. Here we extend these studies by introducing...

Iridescence—change of colour with changes in the angle of view or of illumina-tion—is widespread in the living world, but its functions remain poorly understood. The presence of iridescence has been suggested in flowers where diffraction gratings generate iridescent colours. Such colours have been suggested to serve plant–pollinator communication....

While our conceptual understanding of emotions is largely based on human subjective experiences, research in comparative cognition has shown growing interest in the existence and identification of “emotion-like” states in non-human animals. There is still ongoing debate about the nature of emotions in animals (especially invertebrates), and certain...

Dopamine (DA) plays a fundamental role in insect behavior as it acts both as a general modulator of behavior and as a value system in associative learning where it mediates the reinforcing properties of unconditioned stimuli (US). Here we aimed at characterizing the dopaminergic neurons in the central nervous system of the honey bee, an insect that...

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 report...

Tuning response of 36 different olfactory receptor neuron types. A) Each histogram illustrates the firings rate of an olfactory receptor neuron (ORN) type activated by 100 random odours shown in panel B. The odours on the horizontal axis are sorted according to the firing rate while the higher firing rate is located closer to the centre. The red li...

Parameters of the response curve of the olfactory receptor neuron model. A and B) left and right matrices show the molecular Hill equivalent and binding affinity for different olfactory receptor neuron (ORN) types, respectively. Index of ORNs is arranged in the vertical dimension. C) The probability distribution of the binding affinity for one ORN...

Parameters for firing patterns of projection neuron (PN), local neuron (LN) and lateral horn neuron (LHN). (DOCX)

Examples of selectivity and sensitivity of olfactory receptor neurons. A) Firing rates of olfactory receptor neuron (ORNs) across 50 trials as a function of ligand concentration (solid line is mean, shaded area is standard error (SE)). The red curve indicates that this ORN is selective to Odour A. Here the slopes of curves show the degree of ORN se...

Effect of associative learning in the dorsal region of the antennal lobe. Weight matrices of the synaptic connectivity between 36 local neurons (LNs) in the presence of modulated STDP are reformed in these connections (From left to right: random weights before training; weights after training to odour 3 and to odour 5). After conditioning, differen...

Parameters of the spike timing-dependent plasticity rule. (DOCX)

Dynamic neural plasticity within the antennal lobe. The video shows how synaptic connectivity from 36 local neurons to 36 projection neurons within the antennal lobe varies with time. Thirty-six glomeruli are represented by nodes (arranged around a ring) whose numbers indicate the index of glomerulus in the model. Thickness of lines represents the...

Parameters for firing patterns of olfactory receptor neurons. (DOCX)

Differences in learning and memory dynamics between populations are suspected to result from differences in ecological constraints such as resource distribution. The two reproductive modes (strains) of the parasitoid wasp Venturia canescens share the same geographical areas but live in contrasting habitats: arrhenotokous wasps live in the wild (gen...

Decision-making in uncertain environments requires animals to evaluate, contrast and integrate various information sources to choose appropriate actions. In consensus-making groups, quorum responses are commonly used to combine private and social information, leading to both robust and flexible decisions. Here we show that in house-hunting ant colo...

Honeybees display a rich and interesting behavioral repertoire, in which learning and memory play a fundamental role. Besides elemental forms of learning, in which bees learn specific and univocal links between events in their environment, bees also master different forms of nonelemental learning both in the visual and in the olfactory domain. Cogn...

Ce dossier a préalablement été publié par l’Inra sur son site : http://institut.Inra.fr/Missions/Eclairer-les-decisions/Expertises/Toutes-les-actualites/Conscience-animale

Ce dossier a préalablement été publié par l’Inra sur son site : http://institut.Inra.fr/Missions/Eclairer-les-decisions/Expertises/Toutes-les-actualites/Conscience-animale

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,...

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 im...

Perceptual similarity between stimuli is often assessed via generalization, the response to stimuli that are similar to the one which was previously conditioned. Although conditioning procedures are variable, studies on how this variation may affect perceptual similarity remain scarce. Here, we use a combination of behavioural and computational ana...

The question of why animals sometimes ingest noxious substances is crucial to understand unknown determinants of feeding behaviour. Research on risk-prone feeding behaviour has largely focused on energy budgets as animals with low energy budgets tend to ingest more aversive substances. A less explored possibility is that risk-prone feeding arises f...

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 sec...

PER conditioning and generalization performances in m-ALT lesioned bees, after selection of bees responding to the CS at the end of the generalization phase. (A) Acquisition performances (n = 6 bees). (B) Responses in the generalization tests. (C,D) Significant correlation between the responses of these m-ALT lesioned bees (n = 6) during generaliza...

Honeybees defend their colonies aggressively against intruders and release a potent alarm pheromone to recruit nestmates into defensive tasks. The effect of floral odours on this behaviour has never been studied, despite the relevance of these olfactory cues for the biology of bees. Here we use a novel assay to investigate social and olfactory cues...

Learning theories distinguish elemental from configural learning based on their different complexity. Although the former relies on simple and unambiguous links between the learned events, the latter deals with ambiguous discriminations in which conjunctive representations of events are learned as being different from their elements. In mammals, co...

In reversal learning, subjects first learn to respond to a reinforced stimulus A and not to a non-reinforced stimulus B (A(+) vs. B(-)) and then have to learn the opposite when stimulus contingencies are reversed (A(-) vs. B(+)). This change in stimulus valence generates a transitory ambiguity at the level of stimulus outcome that needs to be overc...