Understanding the Logics of Pheromone Processing in the Honeybee Brain: From Labeled-Lines to Across-Fiber Patterns

Honeybees employ a very rich repertoire of pheromones to ensure intraspecific communication in a wide range of behavioral contexts. This communication can be complex, since the same compounds can have a variety of physiological and behavioral effects depending on the receiver. Honeybees constitute an ideal model to study the neurobiological basis of pheromonal processing, as they are already one of the most influential animal models for the study of general odor processing and learning at behavioral, cellular and molecular levels. Accordingly, the anatomy of the bee brain is well characterized and electro- and opto-physiological recording techniques at different stages of the olfactory circuit are possible in the laboratory. Here we review pheromone communication in honeybees and analyze the different stages of olfactory processing in the honeybee brain, focusing on available data on pheromone detection, processing and representation at these different stages. In particular, we argue that the traditional distinction between labeled-line and across-fiber pattern processing, attributed to pheromone and general odors respectively, may not be so clear in the case of honeybees, especially for social-pheromones. We propose new research avenues for stimulating future work in this area

Differential Interactions of Sex Pheromone and Plant Odour in the Olfactory Pathway of a Male Moth

Most animals rely on olfaction to find sexual partners, food or a habitat. The olfactory system faces the challenge of extracting meaningful information from a noisy odorous environment. In most moth species, males respond to sex pheromone emitted by females in an environment with abundant plant volatiles. Plant odours could either facilitate the localization of females (females calling on host plants), mask the female pheromone or they could be neutral without any effect on the pheromone. Here we studied how mixtures of a behaviourally-attractive floral odour, heptanal, and the sex pheromone are encoded at different levels of the olfactory pathway in males of the noctuid moth Agrotis ipsilon. In addition, we asked how interactions between the two odorants change as a function of the males' mating status. We investigated mixture detection in both the pheromone-specific and in the general odorant pathway. We used a) recordings from individual sensilla to study responses of olfactory receptor neurons, b) in vivo calcium imaging with a bath-applied dye to characterize the global input response in the primary olfactory centre, the antennal lobe and c) intracellular recordings of antennal lobe output neurons, projection neurons, in virgin and newly-mated males. Our results show that heptanal reduces pheromone sensitivity at the peripheral and central olfactory level independently of the mating status. Contrarily, heptanal-responding olfactory receptor neurons are not influenced by pheromone in a mixture, although some post-mating modulation occurs at the input of the sexually isomorphic ordinary glomeruli, where general odours are processed within the antennal lobe. The results are discussed in the context of mate localization

Pheromones as modulators of insect behavior

International audienc

The Effect of Similarity between Elemental Stimuli and Compounds in Olfactory Patterning Discriminations

We studied the ability of honeybees to discriminate between single odorants and binary olfactory mixtures. We analyzed the effect of the number of common elements between these two stimulus classes on olfactory discrimination. We used olfactory conditioning of the honeybees' proboscis extension reflex (PER), a paradigm in which odors can be associated with a reinforcement of sucrose solution. Bees were asked to discriminate reinforced from nonreinforced olfactory stimuli. They were trained with two elemental odors (A and B) versus a binary olfactory mixture. The mixture was either AB (group 2CE, two common elements), AC (group 1CE, one common element A), or CD (group 0CE, no common element). Three groups followed a positive patterning schedule (mixture reinforced and elements nonreinforced: groups 2CE+, 1CE+, and 0CE+) and three other groups a negative patterning schedule (mixture nonreinforced and elements reinforced: groups 2CE−, 1CE−, and 0CE−). We showed that a reduction of similarity (number of common elements) between elemental odors and compounds enhanced the ability to discriminate elements from compounds and that the kind of compound processing used by the bees supports theories that assume nonelemental compound processing (i.e., that exclude the mere summation of the elemental associative strengths upon compound presentation)

Odour mixture coding, processing and learning in the honeybee, [i]Apis mellifera[/i]

absen

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

Behaviour

Raw data for behavioural experiments (corresponding to Figure 1

Seasonality, alarm pheromone and serotonin: insights on the neurobiology of honeybee defence from winter bees

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 intruders, which is regulated by the sting alarm pheromone. We studied the stinging responsiveness of winter bees exposed to this scent or a control (solvent). Surprisingly, winter bees, while maintaining their responsiveness in control conditions, did not increase stinging frequency in response to the alarm pheromone. This was not owing to the bees not perceiving the pheromone, as shown by calcium imaging of the antennal lobes. As the alarm pheromone is thought to act through an increase in brain serotonin levels, ultimately causing heightened defensiveness, we checked if serotonin treatments would affect the stinging behaviour of winter bees. Indeed, treated winter bees became more inclined to sting. Thus, we postulate that loss of responsiveness to the sting alarm pheromone is based on a partial or total disruption of the mechanism converting alarm pheromone perception into high serotonin levels in winter bees