Multiple olfactory receptor neurons and their axonal projections in the antennal lobe of the honeybee Apis mellifera

Abstract

The poreplate sensilla of honeybees are equipped with multiple olfactory receptor neurons (ORNs), which innervate glomeruli of the antennal lobe (AL). We investigated the axonal projection pattern in glomeruli of the AL (glomerular pattern), formed by the multiple ORNs of individual poreplate sensilla. We used the different glomerular patterns to draw conclusions about the equipment of poreplate sensilla with different ORN types. ORNs of single poreplate sensilla were stained and analyzed by laser-scanning confocal microscopy and 3D software (AMIRA). In 13 specimens we found between 7 and 23 ORNs. This is in accordance with data found in the literature (5-35 ORNs) suggesting that all ORNs of the single poreplate sensilla were stained. The ORNs innervate the AL via all four sensory tracts (T1-T4), and glomeruli of the anterior part of the AL are more often innervated. Each ORN innervates a single glomerulus (uniglomerular), and all ORNs of one poreplate sensillum project to different glomeruli. Visual inspection and individual identification of glomeruli, based on the honeybee digital AL atlas, were used to evaluate mapping of glomeruli by a rigid transformation of the experimental ALs onto a reference AL. ORNs belonging to individual poreplate sensilla form variable glomerular patterns, and we did not find a common organization of glomerular patterns. We conclude that poreplate sensilla are equipped with different ORN types but that the same ORN types can be found in different poreplate sensilla. The equipment of poreplate sensilla with ORNs is overlapping. The mapping of glomeruli by rigid transformation is revealed to be a powerful tool for comparative neuroanatomy.Indexing terms: sensilla placodea; 3D reconstruction; antennal lobe; odor representation; VOI; glomeruliIn many cases, animal behavior is guided by olfaction, and most animals have developed sensory organs and olfactory receptor neurons (ORNs) with remarkable sensitivity to detect and discriminate a vast diversity of different odors. The interface for detecting odors in the environment in vertebrates is the nasal mucosa, with its embedded dendrites of ORNs; in insects the interface is the antenna, with numerous olfactory sensilla and associated ORNs. ORN axons project to the first olfactory neuropil and terminate in glomeruli of the vertebrate olfactory bulb (OB) and the insect antennal lobe (AL). The glomeruli represent functional units of the first olfactory neuropil that receive input from ORNs such that a chemotopic representation emerges. The first olfactory neuropil shares many common design principles across phyla (Hildebrand and Shepherd, 1997;Strausfeld and Hildebrand, 1999).

Distinct antennal lobe phenotypes in the leaf‐cutting ant (Atta vollenweideri)

“…For another hymenopteran species, the honeybee, it has been shown that each glomerulus is innervated by a single ORN type, and the spatial position of glomeruli is species specific and conserved across individuals (Galizia et al, 1998(Galizia et al, , 1999Kelber et al, 2006). We selected a number of glomeruli within the region of the AL where the MG is located in large workers.…”

Millisecond Stimulus Onset-Asynchrony Enhances Information about Components in an Odor Mixture

“…In honeybees, ORNs are mainly located in sensilla placodea. These sensilla contain up to 30 ORNs that innervate the AL with highly diverse glomerular patterns (Kelber et al, 2006), thus maximizing the chance that two arbitrary odors may activate two ORNs within the same sensillum. The ORNs that respond to the leading odor could suppress the ORN responses to the trailing odor in the same sensillum.…”

The Antennal Lobes of Fungus-Growing Ants (Attini): Neuroanatomical Traits and Evolutionary Trends

“…Individual olfactory sensilla on the antennae are generally equipped with a high number of ORNs [Schneider and Steinbrecht, 1968;Esslen and Kaissling, 1976;Kelber et al, 2006] compared, for example, to moths or flies that have only one to three receptor neurons in a single sensillum. The advantages of multiple ORNs are not yet clear.…”