Olfactory coding in honeybees.

With less than a million neurons, the western honeybee Apis mellifera is capable of complex olfactory behaviors and provides an ideal model for investigating the neurophysiology of the olfactory circuit and the basis of olfactory perception and learning. Here, we review the most fundamental aspects of honeybee's olfaction: first, we discuss which odorants dominate its environment, and how bees use them to communicate and regulate colony homeostasis; then, we describe the neuroanatomy and the neurophysiology of the olfactory circuit; finally, we explore the cellular and molecular mechanisms leading to olfactory memory formation. The vastity of histological, neurophysiological, and behavioral data collected during the last century, together with new technological advancements, including genetic tools, confirm the honeybee as an attractive research model for understanding olfactory coding and learning.

Chemosensation: Hate Mosquitoes? Peel Beetroots!

Finding the right lure for trapping pest insects is difficult. The typical smell of rain and humid soil, geosmin, now turns out to be a strong attractant for the yellow fever mosquito Aedes aegypti.

Task-Related Phasing of Circadian Rhythms in Antennal Responsiveness to Odorants and Pheromones in Honeybees.

The insect antennae receive olfactory information from the environment. In some insects, it has been shown that antennal responsiveness is dynamically regulated by circadian clocks. However, it is unknown how general this phenomenon is and what functions it serves. Circadian regulation in honeybee workers is particularly interesting in this regard because they show natural task-related chronobiological plasticity. Forager bees show strong circadian rhythms in behavior and brain gene expression, whereas nurse bees tend brood around-the-clock and have attenuated circadian rhythms in activity and whole-brain gene expression. Here, we tested the hypothesis that there is task-related plasticity in circadian rhythms of antennal responsiveness to odorants in worker honeybees. We used electroantennogram (EAG) to measure the antennal responsiveness of nurses and foragers to general odorants and pheromones around the day. The capacity to track 10-Hz odorant pulses varied with time of day for both task groups but with different phases. The antennal pulse-tracking capacity was higher during the subjective day for the day-active foragers, whereas it was better during the night for around-the-clock active nurses. The task-related phases of pulse-tracking rhythms were similar for all the tested stimuli. We also found evidence for circadian rhythms in the EAG response magnitude of foragers but not of nurses. To the best of our knowledge, these results provide the first evidence for circadian regulation of antennal olfactory responsiveness and odorant pulse-tracking capacity in bees or any other hymenopteran insect. Importantly, our study shows for the first time that the circadian phase of olfactory responsiveness may be socially regulated.

Synaptic Organization of Microglomerular Clusters in the Lateral and Medial Bulbs of the Honeybee Brain.

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 pre-synaptic region appears as a large cup-shaped profile that embraces numerous post-synaptic 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.

Odourant dominance in olfactory mixture processing: what makes a strong odourant?

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.