Olfactory coding in honeybees

Abstract

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.

Keywords: Honeybee; Olfaction; Olfactory coding; Olfactory learning; Olfactory system.

Fig. 1

Comparing neurophysiological and perceptual similarity of odorants. a Neural correlates of different olfactory stimuli based on Sachse et al. . On the left, a schematic antennal lobe with glomerular labels (light gray, glomeruli innervated by T1 antennal nerve tract; dark grey, glomeruli innervated by T3 antennal nerve tract). On the right, glomerular response maps of 16 odorants, arranged according to their chemical structures (vertical: ketones, aldehydes, secondary and primary alcohols) and carbon chain lengths (horizontal). Response intensity is color coded in five bins, and percentage of glomerular responses is referred to the maximum response intensity to a given odorant. b The glomerular response maps in a were used to generate an olfactory response similarity matrix based on the Pearson’s correlation coefficient between glomerular response maps. c Olfactory generalization matrix based on Guerrieri et al. (2005). After three conditioning trials, 2048 bees were tested for PER to four random stimuli (among which the conditioned one). The response rates to conditioned and novel stimuli are shown on a scale from 0 (= no bee showed PER) to 1 (all tested bees showed PER). A correlation analysis between the two matrices shows that 54% of the behavioral variability can be explained by odorant representation within the antennal lobe (Guerrieri et al. 2005)

Fig. 2

The honeybee olfactory circuit: scheme of the main neuron types of the honeybee olfactory pathway. For clarity, different neuron types and neuronal tracts are labelled with different colors and presented in different hemispheres. Four antennal nerve (AN) tracts (T1 to T4) comprising the axons of ~ 60,000 olfactory sensory neurons (OSNs) innervate the first olfactory neuropil of the bee brain, the antennal lobe (AL). Each OSN innervates a single glomerulus. All OSNs bearing the same olfactory receptor converge onto one of ~ 163 glomeruli, the structural and functional units of the AL. Within the AL, the olfactory input is processed by a local network of ~ 4000 homogeneous and heterogeneous local interneurons (homo- and hetero-LNs), before being relayed to higher order processing centers by the AL output neurons, the projection neurons (PNs). ~ 800 PNs receive uniglomerular input (uniglomerular PNs) and leave the AL via the medial and lateral antennal lobe tracts (m- and l-ALT), two antiparallel tracts projecting to the ipsilateral mushroom body (MB) and lateral horn (LH) of the protocerebrum in opposite order. A second group of projection neurons collects sensory information from multiple glomeruli (multiglomerular PNs), converges into three mediolateral ALTs (here compressed into one for clarity, ml-ALT), and conveys olfactory information to the lateral protocerebrum only. Projection neurons running along the m- and l-ALT innervate the lip and the basal ring of the MB calyces—whereas the collar region is dedicated to the processing of visual input—and synapse onto the MB intrinsic neurons, the Kenyon cells (KCs): ~ 170,000 type I (spiny) KCs innervate the MB calyces with extended and spiny dendritic arborizations, each spine contacting a different PN terminal; ~ 14,000 class II KCs extend short dendrite-like branches ending in clawed specialization forming multiple synapses around a single PN terminal. KCs’ axons descend in parallel fibers from the calyces to the pedunculus: type I KCs bifurcate and innervate the MB ɑ- and β-lobes, whereas type II KCs terminate in the γ-lobe. Inhibitory feedback neurons from the A3 cell cluster (A3_FB) receive input in the MB lobes and provide a feedback signal to the calyces, acting both on the pre- and post-synaptic site of the PN-KC connections. A second population of A3 extrinsic neurons interconnects the medial and vertical lobes (lobe interconnecting neurons, A3_LC). From the MB lobes, mushroom body output neurons (MBONs, e.g., the pedunculus extrinsic neuron 1) relay the processed olfactory information to the LH, thus connecting experience-related olfactory information (from the MB) to innate odor information (in the LH)